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<ArticleTitle Language="En" OutputMedium="All">Untangling the dorsal diencephalic conduction system: a review of structure and function of the stria medullaris, habenula and fasciculus retroflexus</ArticleTitle>
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<GivenName>Elena</GivenName>
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<OrgDivision>Department of Psychiatry, Trinity College Institute of Neuroscience</OrgDivision>
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<OrgName>Trinity College Dublin</OrgName>
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<OrgDivision>Department of Psychiatry, Education and Research Centre , Royal College of Surgeons in Ireland</OrgDivision>
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<OrgDivision>Anatomy Department, Trinity Biomedical Sciences Institute</OrgDivision>
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<OrgDivision>Department of Anaesthetics, Intensive Care and Pain Medicine</OrgDivision>
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<Abstract Language="En" OutputMedium="All" ID="Abs1">
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<Heading>Abstract</Heading>
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<Para ID="Par1">The often-overlooked dorsal diencephalic conduction system (DDCS) is a highly conserved pathway linking the basal forebrain and the monoaminergic brainstem. It consists of three key structures; the stria medullaris, the habenula and the fasciculus retroflexus. The first component of the DDCS, the stria medullaris, is a discrete bilateral tract composed of fibers from the basal forebrain that terminate in the triangular eminence of the stalk of the pineal gland, known as the habenula. The habenula acts as a relay hub where incoming signals from the stria medullaris are processed and subsequently relayed to the midbrain and hindbrain monoaminergic nuclei through the fasciculus retroflexus. As a result of its wide-ranging connections, the DDCS has recently been implicated in a wide range of behaviors related to reward processing, aversion and motivation. As such, an understanding of the structure and connections of the DDCS may help illuminate the pathophysiology of neuropsychiatric disorders such as depression, addiction and pain. This is the first review of all three components of the DDCS, the stria medullaris, the habenula and the fasciculus retroflexus, with particular focus on their anatomy, function and development.</Para>
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</Abstract>
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<KeywordGroup Language="En" OutputMedium="All">
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<Heading>Keywords</Heading>
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<Keyword>Dorsal diencephalic conduction system</Keyword>
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<Keyword>Stria medullaris</Keyword>
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<Keyword>Habenula</Keyword>
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<Keyword>Fasciculus retroflexus</Keyword>
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</KeywordGroup>
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</ArticleHeader>
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<Body>
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<Section1 ID="Sec1">
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<Heading>Introduction</Heading>
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<Para ID="Par2">The dorsal diencephalic conduction system (DDCS) is a highly conserved integrative and modulatory pathway present in all vertebrates (Sutherland <CitationRef CitationID="CR245">1982</CitationRef>). This bilateral assembly consists of two white matter tracts with an intervening nucleus and is a key conduit connecting the cognitive-emotional basal forebrain to the modulatory monoamine areas of the brainstem (Sutherland <CitationRef CitationID="CR245">1982</CitationRef>; Gardon et al. <CitationRef CitationID="CR83">2014</CitationRef>). It is often overlooked in favor of its more ventral and larger companion, the medial forebrain bundle, which also connects the fore- and hindbrain regions. The similarity in connections (forebrain limbic–striatal to monoaminergic brainstem) and the fact that they converge upon each other anteriorly and posteriorly despite straddling either the dorsal (epithalamic route) or ventral (hypothalamic route) thalamus (Fig. <InternalRef RefID="Fig1">1</InternalRef>) led Nauta to suggest that they may have similar functions with respect to reward behaviors (Nauta <CitationRef CitationID="CR190">1958</CitationRef>). The DDCS first revealed a role in reward in 1970 (Boyd and Celso <CitationRef CitationID="CR27">1970</CitationRef>) and subsequently also showed functionality in the ‘top-down’ modulation of motivation, mood and pain. Highly conserved amongst vertebrates, (Beretta et al. <CitationRef CitationID="CR18">2012</CitationRef>; Concha and Wilson <CitationRef CitationID="CR44">2001</CitationRef>) this system, unlike the singular component of the medial forebrain that forms direct connections (Coenen et al. <CitationRef CitationID="CR42">2018</CitationRef>), is composed of three structures: the white matter stria medullaris, the intervening habenular nucleus and the white matter fasciculus retroflexus. Gathering inputs from diverse frontal areas including the septal nuclei (pleasure and motivation), hypothalamus (arousal and pain), fronto-cortical regions (decision-making), and basal ganglia (motor and behavioral control), the stria medullaris funnels information from these regions into the habenula, situated at the dorso-caudal end of the thalamus (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>; Geisler and Trimble <CitationRef CitationID="CR85">2008</CitationRef>). Information flow in the SM is almost entirely unidirectional (forebrain to habenula), apart from some reciprocal fibers arising from the lateral preoptic and lateral hypothalamic areas (Yamadori <CitationRef CitationID="CR280">1969</CitationRef>; Champney <CitationRef CitationID="CR38">2015</CitationRef>; Patestas and Gartner <CitationRef CitationID="CR198">2016</CitationRef>). After integrating these inputs and relaying in the habenula, output fibers project down through the fasciculus retroflexus to synapse among brainstem monoamine areas including the midbrain ventral tegmental area and hindbrain raphe nuclei. Through this system, distinct frontolimbic areas can modulate monoaminergic release in the brainstem and consequently influence whole brain monoaminergic tone.<Figure Float="Yes" Category="Standard" ID="Fig1">
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<Caption Language="En">
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<CaptionNumber>Fig. 1</CaptionNumber>
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<CaptionContent><SimplePara>The dorsal diencephalic conduction system, with the stria medullaris, habenula and fasciculus retroflexus highlighted. The SM can be seen arching over the thalamus and terminating in the Hb. The larger more wedged-shaped LHb is labeled and can be distinguished from the smaller MHb. The FR can also be identified with fibers arising from the MHb running through the core of the FR and fibers arising from the LHb traveling in the mantle of the FR. Brain photography courtesy of Professor Paul Tierney, Head of Discipline, Department of Anatomy, Trinity College Dublin. <Emphasis Type="Italic">SM</Emphasis> Stria Medullaris, <Emphasis Type="Italic">Hb</Emphasis> habenula, <Emphasis Type="Italic">FR</Emphasis> Fasciculus Retroflexus, <Emphasis Type="Italic">LHb</Emphasis> Lateral Habenula, <Emphasis Type="Italic">MHb</Emphasis> Medial Habenula</SimplePara></CaptionContent>
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</Caption><MediaObject ID="MO1"><ImageObject FileRef="406_2020_1128_Fig1_HTML.gif" Format="GIF" Color="BlackWhite" Type="Linedraw" Rendition="HTML"/>
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</MediaObject></Figure>
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</Para>
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<Para ID="Par3">In recent years, the DDCS has received increasing attention (Gardon et al. <CitationRef CitationID="CR83">2014</CitationRef>; Fakhoury et al. <CitationRef CitationID="CR70">2016b</CitationRef>; Roddy et al. <CitationRef CitationID="CR219">2018</CitationRef>; Fore and Yaksi <CitationRef CitationID="CR78">2019</CitationRef>; Ichijo and Toyama <CitationRef CitationID="CR124">2015</CitationRef>), with research suggesting a particular role in neuropsychiatric disorders due to its function in monoamine regulation (Fakhoury <CitationRef CitationID="CR68">2017</CitationRef>). This is the first review to collate the literature on the known anatomy, function and development of the human DDCS as a whole, as opposed to reviews which have focused exclusively on the habenula alone (Hikosaka et al. <CitationRef CitationID="CR115">2008</CitationRef>; Hikosaka <CitationRef CitationID="CR114">2010</CitationRef>; Fakhoury <CitationRef CitationID="CR68">2017</CitationRef>; Bianco and Wilson <CitationRef CitationID="CR20">2009</CitationRef>). Although initially aimed as a review of the human DDCS, due to the relative dearth of human studies, the review will be complemented by other vertebrate studies throughout.</Para>
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</Section1>
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<Section1 ID="Sec2">
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<Heading>Methods</Heading>
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<Para ID="Par4">A comprehensive literature search to investigate the range and destination (medial/lateral) of habenular inputs was undertaken for the purpose of this review. Online sources including PubMed/MEDLINE, Google Scholar, EMBASE, OVID, and PsycINFO were systematically searched by the primary and senior authors (ER and DWR) using the terms “HABENULA”/”DORSAL DEINCEPHALIC CONDUCTION SYSTEM”/”FASCICULUS RETROFLEXUS”/”HABENULOPEDUNCULAR TRACT”/”HABENULOINTERPEDUNCULAR TRACT” + “INPUT”/“EFFERENT”/“TRACING”/“CONNECTIONS”/”MIDBRAIN”/HINDBRAIN”. No time limit was imposed on search results. Once areas were identified, the search was rerun for each area separately, e.g., “HABENULA” + “HYPOTHALAMUS”, “HABENULA” + “AMYGDALA”. All vertebrate species were included in the search. For each article, references were checked and accessed if considered potentially relevant. A physical search of older literature and books archived in the Department of Anatomy, Trinity College Dublin was also undertaken. All studies were collated, and the data extracted and crosschecked by two researchers (ER and JW).</Para>
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<Para ID="Par5">To determine the mean volume of the habenula, we analyzed data from 14 studies examining normal habenulae (i.e., studies examining habenulae volumes in normal individuals, or control data from clinical studies) in a total of 356 subjects (excluding data from repeated studies). Data were extracted from the results of these studies, and the authors contacted if the raw data was unavailable from published sources. Many study data sets were unavailable and, therefore, mean habenular volumes could not be calculated. As such using the SPSS 24 “compute” command, the MEAN function was used to generate an available analysis (AIA) scale for the missing data (Parent <CitationRef CitationID="CR197">2013</CitationRef>).</Para>
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</Section1>
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<Section1 ID="Sec3">
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<Heading>Stria medullaris</Heading>
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<Para ID="Par6">(<Emphasis Type="Italic">Latin; inner strip/furrow</Emphasis>) The stria medullaris (SM), also known as stria medullaris thalami or habenular stria, is a discrete bilateral white matter tract forming the first part of the dorsal diencephalic conduction system (Sutherland <CitationRef CitationID="CR245">1982</CitationRef>). An unlabeled drawing of the SM can be clearly seen in Vesalius’ texts (Vesalius <CitationRef CitationID="CR267">1543</CitationRef>), but was first designated as the <Emphasis Type="Italic">medullary stria</Emphasis> by Wenzel and Wenzel (<CitationRef CitationID="CR277">1812</CitationRef>). Other terms over the years include the <Emphasis Type="Italic">columna medullaris</Emphasis> (Tarin <CitationRef CitationID="CR251">1750</CitationRef>), the <Emphasis Type="Italic">markiger Streisen</Emphasis> (Soemmerring <CitationRef CitationID="CR241">1791</CitationRef>) and <Emphasis Type="Italic">rené</Emphasis> (reins) (Cruveilhier <CitationRef CitationID="CR55">1836</CitationRef>). Previously considered part of the olfactory system due to its origins around the basal forebrain regions (Ramon y Cajal <CitationRef CitationID="CR211">1911</CitationRef>), it is now well established that the SM is the primary afferent of the behavior modifying DDCS (Fakhoury et al. <CitationRef CitationID="CR69">2016a</CitationRef>).</Para>
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<Section2 ID="Sec4">
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<Heading>Anatomy</Heading>
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<Para ID="Par7">The stria medullaris first appears as a bilateral compact fascicle just posterior to the anterior commissure (Buchanan and Newton <CitationRef CitationID="CR31">1948</CitationRef>). At this point, it is in contact with the fornix and stria terminalis as all three tracts converge around the anterior commissure. The SM runs caudally along the roof of the third ventricle, attached to the tela chordae (Faucette <CitationRef CitationID="CR72">1969</CitationRef>) and arches dorsally over the thalamus. Coursing along the dorsomedial border of the thalamus, it forms a distinct horizontal ridge. In the 80% of individuals where an interthalamic adhesion is present (Allen and Gorski <CitationRef CitationID="CR5">1991</CitationRef>; Carpenter <CitationRef CitationID="CR36">1991</CitationRef>), it arches superior to this. The SM then descends caudally, its lateral fibers terminating in the habenula (Buchanan and Frazer <CitationRef CitationID="CR30">1937</CitationRef>; Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>). Cadaveric measurements place the diameter of the stria medullaris at between 1.5 and 2.5 mm across its length (Roddy et al. <CitationRef CitationID="CR219">2018</CitationRef>), being widest caudally where it merges with the habenula. Both the SM and habenula can be seen as a combined rod-like structure on the posteromedial aspect of the thalamus, protruding into the lateral ventricle with an expansion towards the caudal thalamus. The SM white matter tract occupies 30% of the cross-sectional area of the habenula in humans. This SM–habenular interface is greatly enlarged in humans compared to that in rodents, with the SM taking up only 12% of the cross-sectional area in rats (Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>).</Para>
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<Para ID="Par8">In contrast to the lateral fibers, the medial SM fibers flex inwards towards the base of the pineal gland and cross to the opposite side. These terminate in the contralateral habenula (Buchanan and Frazer <CitationRef CitationID="CR30">1937</CitationRef>; Naidich and Duvernoy <CitationRef CitationID="CR186">2009</CitationRef>; Diaz et al. <CitationRef CitationID="CR58">2011</CitationRef>). This decussation is known as the habenular commissure (Strotmann et al. <CitationRef CitationID="CR244">2014</CitationRef>). Note that the nearby posterior commissure found in the inferior part of the pineal stalk is not anatomically or functionally part of the DDCS. The habenular commissure lying across the superior part of the pineal stalk together with the SM and habenulae form what is anatomically known as the habenular trigone (Strotmann et al. <CitationRef CitationID="CR244">2014</CitationRef>). The lateral habenula also contributes to the habenular commissure in rats (Kim <CitationRef CitationID="CR137">2009</CitationRef>); however, in humans, it is unclear what proportion of these commissural fibers derive from the SM, medial or lateral habenulae.</Para>
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<Para ID="Par9">Three distinct groups of fibers are found in the human stria medullaris. Within the dorsolateral cross section of the tract travel fibers originating from the amygdala and striatal regions (Marburg <CitationRef CitationID="CR166">1944</CitationRef>). Fibers from the basal forebrain areas lie dorsomedial and centrally within the SM; whereas, fibers that originate from the thalamus and hypothalamus are found ventrally. The course and relative position of these fibers remain unchanged through the SM as far as the habenula (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) and correspond with the general trend of lateral habenula fibers being more striatal in origin, and medial fibers being more basal forebrain/septal in origin.</Para>
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<Para ID="Par10">The stria medullaris is also reported to have its own nucleus. A small compact group of cells thought to be the bed nucleus of the stria medullaris (BSM) was first reported in mice by Ramon y Cajal (<CitationRef CitationID="CR211">1911</CitationRef>). The nucleus, embedded among myelinated axons of the stria medullaris, is found caudally to the bed nucleus of the anterior commissure and between the stria medullaris and the fornix in rodents (Risold and Swanson <CitationRef CitationID="CR217">1995</CitationRef>; Ramon y Cajal <CitationRef CitationID="CR211">1911</CitationRef>). As a caudal extension of the septal region (Risold and Swanson <CitationRef CitationID="CR217">1995</CitationRef>), the BSM is reported to contain small multipolar neurons and dense collaterals thought to arise from the fornix (Ramon y Cajal <CitationRef CitationID="CR211">1911</CitationRef>). It has also been alluded to by others (Gurdjian <CitationRef CitationID="CR96">1927</CitationRef>; Watson and Paxinos <CitationRef CitationID="CR275">1986</CitationRef>; Jacobowitz and Palkovits <CitationRef CitationID="CR127">1974</CitationRef>); however, borders have been difficult to identify (Risold and Swanson <CitationRef CitationID="CR217">1995</CitationRef>) and connections of BSM itself have been difficult to establish, with only projections to the medial habenula identified thus far (Shinoda and Tohyama <CitationRef CitationID="CR236">1987</CitationRef>).</Para>
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<Para ID="Par11">Due to the thinness of the tract, the SM is often missed on standard resolution clinical MR imaging. As this tract has been identified as a potential therapeutic target for deep brain stimulation in depression and other neuropsychiatric diseases (Sartorius and Henn <CitationRef CitationID="CR223">2007</CitationRef>), recent efforts have focused in localizing the trajectory of the tract for stereotactic neurosurgery using diffusion-weighted imaging (Kochanski et al. <CitationRef CitationID="CR141">2016</CitationRef>; Roddy et al. <CitationRef CitationID="CR219">2018</CitationRef>).</Para>
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</Section2>
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<Section2 ID="Sec5">
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<Heading>Function</Heading>
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<Para ID="Par12">In general, the SM gathers fibers from frontal, septal, striatal and hypothalamic areas and relays information from these areas through a single tract to the lateral and medial habenulae. Information is transmitted through the tract in a mostly unidirectional <!-- Query ID="Q1" Text="Please confirm the section headings are correctly identified." -->manner from the forebrain regions to the habenula. To date, however, there have been no fiber tracing or staining studies of the human SM.</Para>
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<Para ID="Par13">The first-order inputs to the lateral habenula through the stria medullaris include the lateral preoptic area, the lateral hypothalamus, anterior hypothalamic nucleus, bed nucleus of the stria terminalis, the internal segment of the globus pallidus, substantia innominata and septum (Klemm <CitationRef CitationID="CR140">2004</CitationRef>; Hikosaka et al. <CitationRef CitationID="CR115">2008</CitationRef>). Second- and further-order inputs arise from medial, lateral and preoptic hypothalamic areas (Klemm <CitationRef CitationID="CR140">2004</CitationRef>). The SM also inputs information from the nucleus of the diagonal band of Broca, lateral hypothalamus, lateral preoptic area and medial septal nuclei into the medial habenula (Akagi and Powell <CitationRef CitationID="CR4">1968</CitationRef>; Klemm <CitationRef CitationID="CR140">2004</CitationRef>). SM afferents are primarily cholinergic, glutamatergic and GABAergic, with primary GABAergic and cholinergic input into the habenula being supplied by the nucleus of the diagonal band of Broca via the SM (Viswanath et al. <CitationRef CitationID="CR270">2013</CitationRef>; Klemm <CitationRef CitationID="CR140">2004</CitationRef>). This was supported when bilateral transection of the SM in rodents induced a 50% decrease in choline acetyltransferase, an enzyme responsible for acetylcholine synthesis, in the habenulae and the downstream interpeduncular nucleus, as well as a 65% decrease of glutamate decarboxylase in the habenula (Contestabile and Fonnum <CitationRef CitationID="CR48">1983</CitationRef>).</Para>
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<Para ID="Par14">The stria medullaris has recently been suggested as a therapeutic target for the treatment of depression and other neuropsychiatry diseases using deep brain stimulation (Sartorius and Henn <CitationRef CitationID="CR223">2007</CitationRef>). Even though modulation of the lateral habenula is the proposed mechanism of this technique, electrode placement occurs at the caudal end of the SM, just beside the habenula. To date, two patients with intractable depression have shown marked improvement with modulation of the DDCS through SM stimulation (Sartorius et al. <CitationRef CitationID="CR224">2010</CitationRef>; Kiening and Sartorius <CitationRef CitationID="CR134">2013</CitationRef>).</Para>
|
|
<Para ID="Par15">The SM and habenula, although discrete structures, are essentially a functional unit and defining a function for the SM independent of the habenula is impossible. As such, the function of the SM will be integrated in the below section.</Para>
|
|
</Section2>
|
|
</Section1>
|
|
<Section1 ID="Sec6">
|
|
<Heading>Habenula</Heading>
|
|
<Para ID="Par16">(Latin; <Emphasis Type="Italic">little reign</Emphasis>) The trigonum habenulae is a small triangular eminence encompassed by the pineal gland, the posterior part of the stria medullaris and the adjacent part of the thalamus (Buchanan and Frazer <CitationRef CitationID="CR30">1937</CitationRef>; Naidich and Duvernoy <CitationRef CitationID="CR186">2009</CitationRef>). A slight swelling in this trigone indicates the position of the evolutionary conserved gray matter structure called the habenula (also known as the habenular complex, due to being composed of multiple nuclei) (Nolte <CitationRef CitationID="CR192">2002</CitationRef>). It was first named by Meynert who described a small mass of gray matter on the posteromedial aspect of the thalamus (Meynert <CitationRef CitationID="CR172">1872</CitationRef>). Originally considered anatomically and functionally the stalk of the adjacent pineal gland, it refers to two distinct groups of nuclei at the caudal end of the stria medullaris.</Para>
|
|
<Para ID="Par17">The habenula is the central component of the DDCS and has been well conserved throughout vertebrate evolution (Loonen et al. <CitationRef CitationID="CR164">2017</CitationRef>). It acts as a hub, with limbic pathways traversing the stria medullaris to relay to the habenula prior to transmitting signals to brainstem modulatory areas (Carpenter <CitationRef CitationID="CR36">1991</CitationRef>). As such, it is vital for integrating motor, cognitive, emotional and sensory processing within a single locus to influence motivational processes and value-based decision-making (Gardon et al. <CitationRef CitationID="CR83">2014</CitationRef>). Recent studies highlighting the function of the habenula in encoding reward and aversive behavior have renewed the interest into this small structure.</Para>
|
|
<Section2 ID="Sec7">
|
|
<Heading>Anatomy</Heading>
|
|
<Para ID="Par18">The habenula, like many limbic structures, was initially believed to have primarily olfactory connections (Ramon y Cajal <CitationRef CitationID="CR211">1911</CitationRef>); however, repeated studies have revealed its connections with a wide variety of regions across the brain (Rausch and Long <CitationRef CitationID="CR214">1971</CitationRef>; Powell et al. <CitationRef CitationID="CR206">1965</CitationRef>; Greatrex and Phillipson <CitationRef CitationID="CR91">1982</CitationRef>; Gamble <CitationRef CitationID="CR82">1952</CitationRef>). The habenula has both medial and lateral nuclei (see below). The literature strategy revealed that 135 studies have investigated habenular connections in diverse vertebrates from lizards to primates. Only one study to date has traced the connections of the human habenular complex (Marburg <CitationRef CitationID="CR166">1944</CitationRef>). The results are presented in Table <InternalRef RefID="Tab1">1</InternalRef>. Although some overlap, broadly speaking, motor, frontal, thalamic, hypothalamic, basal ganglia and associated areas (e.g., ventral tegmental area) project to the lateral habenula; whereas, septal and limbic associated areas (e.g., hippocampus) project to the medial habenula.<Table ID="Tab1" Float="Yes">
|
|
<Caption Language="En">
|
|
<CaptionNumber>Table 1</CaptionNumber>
|
|
<CaptionContent><SimplePara>Habenular inputs collated from previous tracing studies</SimplePara></CaptionContent>
|
|
</Caption>
|
|
<tgroup cols="3">
|
|
<colspec colnum="1" colname="c1" align="left"/>
|
|
<colspec colnum="2" colname="c2" align="left"/>
|
|
<colspec colnum="3" colname="c3" align="left"/>
|
|
<thead>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara>Area of input</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>References</SimplePara></entry>
|
|
</row>
|
|
</thead>
|
|
<tbody>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Cortical regions</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Piriform cortex</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Gurdjian <CitationRef CitationID="CR95">1925</CitationRef>) (rat), (Carl Huber and Crosby <CitationRef CitationID="CR34">1929</CitationRef>) (bird), (Hines <CitationRef CitationID="CR116">1929</CitationRef>) (platypus), (Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Young <CitationRef CitationID="CR286">1936</CitationRef>) (rabbit), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander), (Gamble <CitationRef CitationID="CR82">1952</CitationRef>) (lizard), (Gamble <CitationRef CitationID="CR81">1956</CitationRef>) (tortoise), (Ban <CitationRef CitationID="CR13">1962</CitationRef>) (rat), (Powell et al. <CitationRef CitationID="CR206">1965</CitationRef>) (rat), (Millhouse <CitationRef CitationID="CR173">1969</CitationRef>) (mouse), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Kim and Lee <CitationRef CitationID="CR138">2012</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Hippocampus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Hines <CitationRef CitationID="CR116">1929</CitationRef>) (platypus), (Young <CitationRef CitationID="CR286">1936</CitationRef>) (rabbit), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Amygdala</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>“Nucleus Taenia” (Carl Huber and Crosby <CitationRef CitationID="CR34">1929</CitationRef>) (bird), (Young <CitationRef CitationID="CR286">1936</CitationRef>) (rabbit), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) ( human), (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander), (Gamble <CitationRef CitationID="CR82">1952</CitationRef>) (lizard), (Laursen <CitationRef CitationID="CR150">1955</CitationRef>) (monkey), (Kusama and Hagino <CitationRef CitationID="CR146">1961</CitationRef>) (rabbit), (Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cats), (Cowan et al. <CitationRef CitationID="CR52">1965</CitationRef>) (rat), (Johnson <CitationRef CitationID="CR129">1965</CitationRef>) (cat), (Millhouse <CitationRef CitationID="CR173">1969</CitationRef>) (mouse), (Leonard and Scott <CitationRef CitationID="CR155">1971</CitationRef>) (rats), (Iwahori <CitationRef CitationID="CR126">1977</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Prelimbic cortex</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Gamble <CitationRef CitationID="CR82">1952</CitationRef>) (lizard), (Kim and Lee <CitationRef CitationID="CR138">2012</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Infralimbic cortex</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Kim and Lee <CitationRef CitationID="CR138">2012</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anterior cingulate cortex</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Kim and Lee <CitationRef CitationID="CR138">2012</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anterior insular cortex</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Vertes <CitationRef CitationID="CR263">2002</CitationRef>) (rat), (Vertes <CitationRef CitationID="CR264">2004</CitationRef>) (rat), (Kim and Lee <CitationRef CitationID="CR138">2012</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Basal forebrain</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Septum undifferentiated</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Gurdjian <CitationRef CitationID="CR95">1925</CitationRef>) (rat), (Carl Huber and Crosby <CitationRef CitationID="CR34">1929</CitationRef>) (bird), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Nauta <CitationRef CitationID="CR188">1956</CitationRef>) (Rat), (Nauta <CitationRef CitationID="CR190">1958</CitationRef>) (cat), (Valenstein and Nauta <CitationRef CitationID="CR259">1959</CitationRef>) (Rat, guinea pig, cat and monkey), (Guillery <CitationRef CitationID="CR94">1959</CitationRef>) (Cat), (Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (rabbit, rat and cat), (Ban <CitationRef CitationID="CR13">1962</CitationRef>) (rat), (Powell <CitationRef CitationID="CR202">1963</CitationRef>) (rat), (Zyo <CitationRef CitationID="CR292">1963</CitationRef>) (rabbit), (Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cats), (Johnson <CitationRef CitationID="CR129">1965</CitationRef>) (cat), (Raisman <CitationRef CitationID="CR210">1966</CitationRef>) (rat), (Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), (Powell <CitationRef CitationID="CR204">1968</CitationRef>) (Rat, cat and monkey), (Mizuno et al. <CitationRef CitationID="CR175">1969</CitationRef>) (cat), (Genton <CitationRef CitationID="CR86">1969</CitationRef>) (mouse), (Price and Powell <CitationRef CitationID="CR207">1970</CitationRef>) (Rat), (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>) (opossum and cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Iwahori <CitationRef CitationID="CR126">1977</CitationRef>) (cat), (Meibach and Siegel <CitationRef CitationID="CR170">1977</CitationRef>) (rat), (Swanson and Cowan <CitationRef CitationID="CR248">1979</CitationRef>) (rat), (Gottesfeld and Jacobowitz <CitationRef CitationID="CR89">1979</CitationRef>) (rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard), (Shinoda and Tohyama <CitationRef CitationID="CR236">1987</CitationRef>) (rat),(Kawaja et al. <CitationRef CitationID="CR131">1990</CitationRef>) (rat), “septal nucleus impar” (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Medial septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), (Qin and Luo <CitationRef CitationID="CR208">2009</CitationRef>) (mouse)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lateral septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Powell <CitationRef CitationID="CR202">1963</CitationRef>) (rat), (Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), (Powell <CitationRef CitationID="CR204">1968</CitationRef>) (Rat, cat and monkey), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Gottesfeld and Jacobowitz <CitationRef CitationID="CR89">1979</CitationRef>) (rat), (Sim and Joseph <CitationRef CitationID="CR237">1991</CitationRef>) (rats), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Risold and Swanson <CitationRef CitationID="CR218">1997</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Posterior septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), (Powell <CitationRef CitationID="CR204">1968</CitationRef>) (Rat, cat and monkey)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Septofibrial nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Young <CitationRef CitationID="CR286">1936</CitationRef>) (rabbit), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Staines et al. <CitationRef CitationID="CR243">1988</CitationRef>) (Rat), (Kawaja et al. <CitationRef CitationID="CR131">1990</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Triangular nucleus of septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Staines et al. <CitationRef CitationID="CR243">1988</CitationRef>) (Rat), (Kawaja et al. <CitationRef CitationID="CR131">1990</CitationRef>) (rat), (Qin and Luo <CitationRef CitationID="CR208">2009</CitationRef>) (mouse)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Precommissural septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral/unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Zyo <CitationRef CitationID="CR292">1963</CitationRef>) (rabbit), (Johnson <CitationRef CitationID="CR129">1965</CitationRef>) (cat), “rostral septum” (Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), “rostral septum” (Powell <CitationRef CitationID="CR204">1968</CitationRef>) (Rat, cat and monkey)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Supracommissural septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Nauta <CitationRef CitationID="CR188">1956</CitationRef>) (Rat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Postcommissural septum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (rabbit, rat and cat), (Ban <CitationRef CitationID="CR13">1962</CitationRef>) (rat), (Johnson <CitationRef CitationID="CR129">1965</CitationRef>) (cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Staines et al. <CitationRef CitationID="CR243">1988</CitationRef>) (Rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Diagonal band of Broca</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Guillery <CitationRef CitationID="CR94">1959</CitationRef>) (Cat), (Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), (Price and Powell <CitationRef CitationID="CR207">1970</CitationRef>) (Rat), (Conrad and Pfaff <CitationRef CitationID="CR47">1976b</CitationRef>) (rat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Meibach and Siegel <CitationRef CitationID="CR170">1977</CitationRef>) (rat), (Gottesfeld and Jacobowitz <CitationRef CitationID="CR89">1979</CitationRef>) (rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Staines et al. <CitationRef CitationID="CR243">1988</CitationRef>) (Rat), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Qin and Luo <CitationRef CitationID="CR208">2009</CitationRef>) (mouse), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Susbtantia innominata</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (rabbit, rat and cat), (Kim et al. <CitationRef CitationID="CR136">1976</CitationRef>) (monkey), “nucleus basalis” (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Troiano and Siegel <CitationRef CitationID="CR256">1978a</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Nucleus accumbens</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>“pars medialis of nucleus accumbens” (Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Powell <CitationRef CitationID="CR203">1966</CitationRef>) (cat), (Powell and Leman <CitationRef CitationID="CR205">1976</CitationRef>) (monkey), (Conrad and Pfaff <CitationRef CitationID="CR47">1976b</CitationRef>) (Rat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Troiano and Siegel <CitationRef CitationID="CR256">1978a</CitationRef>) (cat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anterior olfactory nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Gurdjian <CitationRef CitationID="CR95">1925</CitationRef>) (rat), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Gamble <CitationRef CitationID="CR82">1952</CitationRef>) (lizard), (Gamble <CitationRef CitationID="CR81">1956</CitationRef>) (tortoise), (Millhouse <CitationRef CitationID="CR173">1969</CitationRef>) (mouse), (Ferrer <CitationRef CitationID="CR74">1969</CitationRef>) (hamster, (Heimer <CitationRef CitationID="CR105">1972</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Olfactory tubercle</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Morin <CitationRef CitationID="CR179">1950</CitationRef>) (Guinea Pig), (Kusama and Hagino <CitationRef CitationID="CR146">1961</CitationRef>) (rabbit), (Ban <CitationRef CitationID="CR13">1962</CitationRef>) (rat), (Millhouse <CitationRef CitationID="CR173">1969</CitationRef>) (mouse), (Heimer <CitationRef CitationID="CR105">1972</CitationRef>) (rat), (Iwahori <CitationRef CitationID="CR126">1977</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Olfactory bulb</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Ramon y Cajal <CitationRef CitationID="CR211">1911</CitationRef>) (vertebrates), (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Central white matter nuclei</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Nucleus of posterior pallial commissure</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Bed nucleus of anterior commissure</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Carl Huber and Crosby <CitationRef CitationID="CR34">1929</CitationRef>) (bird), Herrick <CitationRef CitationID="CR112">1948</CitationRef> (tiger salamander), (Staines et al. <CitationRef CitationID="CR243">1988</CitationRef>) (Rat), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Bed nucleus of stria terminalis</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (Rabbit), (Conrad and Pfaff <CitationRef CitationID="CR47">1976b</CitationRef>) (Albino Rats), (Swanson and Cowan <CitationRef CitationID="CR248">1979</CitationRef>) (rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Weller and Smith <CitationRef CitationID="CR276">1982</CitationRef>) (rat), (Staines et al. <CitationRef CitationID="CR243">1988</CitationRef>) (Rat), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Dong and Swanson <CitationRef CitationID="CR60">2006</CitationRef>) (rats), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Basal Ganglia</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Globus pallidus externa</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral/unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Ranson and Ranson <CitationRef CitationID="CR213">1941</CitationRef>) (monkey), (Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cats), (Nauta and Mehler <CitationRef CitationID="CR189">1966</CitationRef>) (monkey), (Kim et al. <CitationRef CitationID="CR136">1976</CitationRef>) (monkey), (Gottesfeld et al. <CitationRef CitationID="CR90">1977</CitationRef>) (rat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (Rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard), (Araki et al. <CitationRef CitationID="CR10">1984</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Globus Pallidus interna (Entopeduncular Nucleus)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral/unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cat), (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander), (Nauta and Mehler <CitationRef CitationID="CR189">1966</CitationRef>) (Monkey), (Kim et al. <CitationRef CitationID="CR136">1976</CitationRef>) (monkey), (Iwahori <CitationRef CitationID="CR126">1977</CitationRef>) (cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Gottesfeld et al. <CitationRef CitationID="CR90">1977</CitationRef>) (rat), (Nagy et al. <CitationRef CitationID="CR185">1978</CitationRef>) (rat), (Filion and Harnois <CitationRef CitationID="CR75">1978</CitationRef>) (cat), (Carter and Fibiger <CitationRef CitationID="CR37">1978</CitationRef>) (rat), (Larsen and Sutin <CitationRef CitationID="CR149">1978</CitationRef>) (cat), (Parent <CitationRef CitationID="CR194">1979</CitationRef>) (squirrel monkey), (Larsen and McBride <CitationRef CitationID="CR148">1979</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Van Der Kooy and Carter <CitationRef CitationID="CR260">1981</CitationRef>) (rat), (McBride <CitationRef CitationID="CR169">1981</CitationRef>) (cat), (Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard), (Vincent et al. <CitationRef CitationID="CR268">1982</CitationRef>) (rat), (Garland and Mogenson <CitationRef CitationID="CR84">1983</CitationRef>) (rats), (Araki et al. <CitationRef CitationID="CR10">1984</CitationRef>) (Rat), (Vincent and Brown <CitationRef CitationID="CR269">1986</CitationRef>) (Rat), (Shinoda and Tohyama <CitationRef CitationID="CR236">1987</CitationRef>) (rat), (Hazrati and Parent <CitationRef CitationID="CR104">1991</CitationRef>) (squirrel monkey), (Moriizumi and Hattori <CitationRef CitationID="CR178">1992</CitationRef>) (rat), “lobus subhippocampus” (Yañez and Anadon <CitationRef CitationID="CR282">1994</CitationRef>) (Lamprey), “rostral thalamus” (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout), (Kha et al. <CitationRef CitationID="CR133">2000</CitationRef>) (rats), (Parent et al. <CitationRef CitationID="CR196">2001</CitationRef>) (monkey), (Folgueira et al. <CitationRef CitationID="CR76">2004</CitationRef>) (rainbow trout), (Wallace et al. <CitationRef CitationID="CR273">2017</CitationRef>) (mice)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Ventral Pallidum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Kim et al. <CitationRef CitationID="CR136">1976</CitationRef>) (monkey), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Troiano and Siegel <CitationRef CitationID="CR257">1978b</CitationRef>) (cat), (Parent <CitationRef CitationID="CR194">1979</CitationRef>) (squirrel monkey), (Groenewegen et al. <CitationRef CitationID="CR92">1993</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Haber et al. <CitationRef CitationID="CR97">1993</CitationRef>) (monkey), (Zahm et al. <CitationRef CitationID="CR287">1996</CitationRef>) (rats), (Hendricks and Jesuthasan <CitationRef CitationID="CR106">2007</CitationRef>) (Zebrafish), (Tripathi et al. <CitationRef CitationID="CR254">2013</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Thalamic nuclei</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Thalamus undifferentiated</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Hines <CitationRef CitationID="CR116">1929</CitationRef>) (platypus), “dorsal thalamus” (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander), (Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cats), (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>) (opossum and cat), “dorsal thalamus” (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), “thalamic eminence” (Krug et al. <CitationRef CitationID="CR145">1993</CitationRef>) (Axolotl—fish), “thalamic eminence” (Hendricks and Jesuthasan <CitationRef CitationID="CR106">2007</CitationRef>) (Zebrafish)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anterior Group</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (rabbit), (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>) (opossum and cat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anterodorsal nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Yañez and Anadon <CitationRef CitationID="CR282">1994</CitationRef>) (Lamprey)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anteroventral nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Paramedian thalamus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (rabbit), (Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Reticular nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara>Epithalamus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>“pineal gland” (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout) </SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Hypothalamus</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Hypothalamus undifferentiated</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Carl Huber and Crosby <CitationRef CitationID="CR34">1929</CitationRef>) (bird), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cats), (Zyo <CitationRef CitationID="CR292">1963</CitationRef>) (rabbit), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lateral nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Nauta <CitationRef CitationID="CR190">1958</CitationRef>) (cat), (Kusama and Hagino <CitationRef CitationID="CR146">1961</CitationRef>) (rabbit), (Zyo <CitationRef CitationID="CR292">1963</CitationRef>) (rabbit), (Wolf and Sutin <CitationRef CitationID="CR278">1966</CitationRef>) (Rat), (Mizuno et al. <CitationRef CitationID="CR175">1969</CitationRef>) (cat), (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>) (opossum and cat), (Troiano and Siegel <CitationRef CitationID="CR255">1975</CitationRef>) (cat), (Swanson <CitationRef CitationID="CR247">1976</CitationRef>) (rat), (Iwahori <CitationRef CitationID="CR126">1977</CitationRef>) (cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (Rat), (Parent <CitationRef CitationID="CR194">1979</CitationRef>) monkey), (Saper et al. <CitationRef CitationID="CR222">1979</CitationRef>) (rat), (McBride <CitationRef CitationID="CR169">1981</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Berk and Finkelstein <CitationRef CitationID="CR19">1982</CitationRef>) (Rat), (Araki et al. <CitationRef CitationID="CR10">1984</CitationRef>) (Rat), (Shinoda and Tohyama <CitationRef CitationID="CR236">1987</CitationRef>) (rat), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat), (Kowski et al. <CitationRef CitationID="CR143">2008</CitationRef>) (rat), (Hahn and Swanson <CitationRef CitationID="CR98">2010</CitationRef>) (rat), (Hahn and Swanson <CitationRef CitationID="CR99">2012</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Dorsomedial nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Paraventricular nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>“magnocellular nucleus” (Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>) (opossum and cat), (von Bartheld and Meyer <CitationRef CitationID="CR272">1990</CitationRef>) (lungfish), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Suprachiasmatic nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Buijs <CitationRef CitationID="CR32">1978</CitationRef>) (rats), (Sofroniew et al. <CitationRef CitationID="CR242">1981</CitationRef>) (rats)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Ventromedial nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Anterior nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Conrad and Pfaff <CitationRef CitationID="CR47">1976b</CitationRef>) (Albino Rats), (McBride <CitationRef CitationID="CR169">1981</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Risold et al. <CitationRef CitationID="CR216">1994</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Supraoptic nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Posterior nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(McBride <CitationRef CitationID="CR169">1981</CitationRef>) (cat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Preoptic hypothalamus undifferentiated</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Gurdjian <CitationRef CitationID="CR95">1925</CitationRef>) (rat), (Gurdjian <CitationRef CitationID="CR96">1927</CitationRef>) (rat), (Hines <CitationRef CitationID="CR116">1929</CitationRef>) (platypus), (Carl Huber and Crosby <CitationRef CitationID="CR34">1929</CitationRef>) (bird), (Loo <CitationRef CitationID="CR163">1931</CitationRef>) (Opossum), (Humphrey <CitationRef CitationID="CR121">1936</CitationRef>) (bat), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander), (Zyo <CitationRef CitationID="CR292">1963</CitationRef>) (rabbit), (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>) (opossum and cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (Rat), (McBride <CitationRef CitationID="CR169">1981</CitationRef>) (cat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Medial preoptic nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Gurdjian <CitationRef CitationID="CR95">1925</CitationRef>) (rat), (Young <CitationRef CitationID="CR286">1936</CitationRef>) (rabbit), (Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Conrad and Pfaff <CitationRef CitationID="CR46">1976a</CitationRef>) (Albino Rat), (Anderson and Shen <CitationRef CitationID="CR8">1980</CitationRef>) (guinea pig), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lateral preoptic nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Young <CitationRef CitationID="CR286">1936</CitationRef>) (rabbit), (Nauta <CitationRef CitationID="CR190">1958</CitationRef>) (cat), (Cragg <CitationRef CitationID="CR54">1961</CitationRef>) (Rabbit), (Kusama and Hagino <CitationRef CitationID="CR146">1961</CitationRef>) (rabbit), (Zyo <CitationRef CitationID="CR292">1963</CitationRef>) (rabbit), (Cowan et al. <CitationRef CitationID="CR52">1965</CitationRef>) (rat), (Wolf and Sutin <CitationRef CitationID="CR278">1966</CitationRef>) (rat), (Mizuno et al. <CitationRef CitationID="CR175">1969</CitationRef>) (cat), (Troiano and Siegel <CitationRef CitationID="CR255">1975</CitationRef>) (cat), (Swanson <CitationRef CitationID="CR247">1976</CitationRef>) (rat), (Iwahori <CitationRef CitationID="CR126">1977</CitationRef>) (cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Troiano and Siegel <CitationRef CitationID="CR257">1978b</CitationRef>) (cat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Garland and Mogenson <CitationRef CitationID="CR84">1983</CitationRef>) (rats), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat), (Kowski et al. <CitationRef CitationID="CR143">2008</CitationRef>) (Rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Mammillary bodies</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Premammillary nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c3" namest="c1"><SimplePara>Brainstem</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Tectum</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Marburg <CitationRef CitationID="CR166">1944</CitationRef>) (human), (Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Tegmentum undifferentiated</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Laterodorsal tegmental nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral/unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>“nucleus isthmi” (Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard), (Cornwall et al. <CitationRef CitationID="CR51">1990</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Dorsal tegmental area</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Goto et al. <CitationRef CitationID="CR87">2001</CitationRef>) (rat), (Olucha‐Bordonau et al. <CitationRef CitationID="CR193">2003</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Ventral tegmental area</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Lindvall and Björklund <CitationRef CitationID="CR162">1974</CitationRef>) (rat), (Kizer et al. <CitationRef CitationID="CR139">1976</CitationRef>) (rat),), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), “ventral tegmental pars lateralis” (Simon et al. <CitationRef CitationID="CR238">1979</CitationRef>) (rat), (Beckstead et al. <CitationRef CitationID="CR16">1979</CitationRef>) (rat), “ventral tegmental interfascicular nucleus” and “ventral tegmental median paranigral” (Phillipson and Griffith <CitationRef CitationID="CR199">1980</CitationRef>) (rat), (Parent et al. <CitationRef CitationID="CR195">1981</CitationRef>) (rat, cat and monkey), (Phillipson and Pycock <CitationRef CitationID="CR200">1982</CitationRef>) (rat), (Swanson <CitationRef CitationID="CR246">1982</CitationRef>) (rat), (Skagerberg et al. <CitationRef CitationID="CR239">1984</CitationRef>) (rat), (Díaz and Puelles <CitationRef CitationID="CR57">1992</CitationRef>) (Lizard), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Gruber et al. <CitationRef CitationID="CR93">2007</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Pretectal area</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Herrick <CitationRef CitationID="CR112">1948</CitationRef>) (tiger salamander)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Periaqueductal gray</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Locus coeruleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Unspecified</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard), (Gottesfeld <CitationRef CitationID="CR88">1983</CitationRef>) (rat), (Yañez and Anadón <CitationRef CitationID="CR283">1996</CitationRef>) (rainbow trout), (Gruber et al. <CitationRef CitationID="CR93">2007</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Substantia nigra compacta</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Kizer et al. <CitationRef CitationID="CR139">1976</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Interpeduncular nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Massopust Jr and Thompson 1962) (rats and cats), (Mitchell <CitationRef CitationID="CR174">1963</CitationRef>) (cats)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Raphe Nuclei undifferentiated</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Moore et al. <CitationRef CitationID="CR176">1978</CitationRef>) (rat), (McBride <CitationRef CitationID="CR169">1981</CitationRef>) (cat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat),(Morin and Meyer-Bernstein <CitationRef CitationID="CR180">1999</CitationRef>) (hamster), (Felton et al. <CitationRef CitationID="CR73">1999</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat), (Muzerelle et al. <CitationRef CitationID="CR184">2016</CitationRef>) (mouse)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Raphe nuclei dorsal</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Conrad et al. <CitationRef CitationID="CR45">1974</CitationRef>) (rat), (Pierce et al. <CitationRef CitationID="CR201">1976</CitationRef>) (cat), (Azmitia and Segal <CitationRef CitationID="CR11">1978</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Raphe nuclei median</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial/lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Conrad et al. <CitationRef CitationID="CR45">1974</CitationRef>) (rat), “superior raphe” (Bobillier et al. <CitationRef CitationID="CR23">1975</CitationRef>) (cat), “superior raphe” (Bobillier et al. <CitationRef CitationID="CR25">1976</CitationRef>) (cat), (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>) (rat), (Azmitia and Segal <CitationRef CitationID="CR11">1978</CitationRef>) (rat), “superior raphe” (Bobillier et al. <CitationRef CitationID="CR24">1979</CitationRef>) (rat), “superior raphe” (Hoogland <CitationRef CitationID="CR118">1982</CitationRef>) (lizard), (Hallanger et al. <CitationRef CitationID="CR100">1987</CitationRef>) (rat), (Vertes and Martin <CitationRef CitationID="CR266">1988</CitationRef>) (rat), (Vertes et al. <CitationRef CitationID="CR265">1999</CitationRef>) (rat), (Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat), (Yetnikoff et al. <CitationRef CitationID="CR285">2015</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Interfascicular nucleus</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Li et al. <CitationRef CitationID="CR159">1993</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Superior Cervical ganglion</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>(Björklund et al. <CitationRef CitationID="CR22">1972</CitationRef>) (rat), (Lindvall and Björklund <CitationRef CitationID="CR162">1974</CitationRef>) (rat), (Gottesfeld <CitationRef CitationID="CR88">1983</CitationRef>) (rat)</SimplePara></entry>
|
|
</row>
|
|
</tbody>
|
|
</tgroup>
|
|
</Table>
|
|
</Para>
|
|
<Para ID="Par19">Although easily distinguishable as the thick caudal expansion of the combined SM–habenula rod-like structure that protrudes into the lateral ventricle, defining the rostral most boundaries of the habenula is challenging in gross dissections. This is because the SM tapers caudally and dorsally into the habenula. Regional microscopic differences in cellular distribution, however, allow the habenula to be distinguished from the white matter fibers of the SM and the multipolar cells of the adjacent thalamus (Marburg <CitationRef CitationID="CR166">1944</CitationRef>; Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>). The habenular width is approximately 5–9 mm across (Strotmann et al. <CitationRef CitationID="CR244">2014</CitationRef>), as such the structure is difficult to visualize accurately using standard clinical MRI. However, using high-resolution magnetic resonance imaging (resolution < 1.5mm<Superscript>3</Superscript>), it has recently been possible to determine the mean habenular volumes in a number of studies (Table <InternalRef RefID="Tab2">2</InternalRef>a). Extrapolated mean values for left and right habenular complex volumes were found to be 21.9 mm<Superscript>3</Superscript> (SD ± 6.5 mm<Superscript>3</Superscript>) and 20.6 mm<Superscript>3</Superscript> (SD ± 6.7 mm<Superscript>3</Superscript>), respectively. A single post-mortem study has investigated habenular volumes (Ranft et al. <CitationRef CitationID="CR212">2010</CitationRef>). This study suggested larger habenular volumes revealing lateral volumes of 27.57 mm (SD ± 5.05 mm) and 29.59 mm (SD ± 4.83 mm) and medial volumes of 3.35 mm (SD ± 1.33 mm) and 3.64 mm (SD ± 0.97 mm) for left and right sides, respectively. MRI resolution limitations, age variation and differences in measurement techniques between post-mortem and MRI studies could potentially account for the difference between the two methods of volume estimation.<Table ID="Tab2" Float="Yes">
|
|
<Caption Language="En">
|
|
<CaptionNumber>Table 2</CaptionNumber>
|
|
<CaptionContent><SimplePara>(A and B) Summary of habenular volumes given in mm<Superscript>3</Superscript> in the current literature</SimplePara></CaptionContent>
|
|
</Caption>
|
|
<tgroup cols="8">
|
|
<colspec colnum="1" colname="c1" align="left"/>
|
|
<colspec colnum="2" colname="c2" align="left"/>
|
|
<colspec colnum="3" colname="c3" align="left"/>
|
|
<colspec colnum="4" colname="c4" align="left"/>
|
|
<colspec colnum="5" colname="c5" align="left"/>
|
|
<colspec colnum="6" colname="c6" align="left"/>
|
|
<colspec colnum="7" colname="c7" align="left"/>
|
|
<colspec colnum="8" colname="c8" align="left"/>
|
|
<thead>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara>Name</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Participants</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Total volume</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>SD</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Left volume</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>SD</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>Right volume</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>SD</SimplePara></entry>
|
|
</row>
|
|
</thead>
|
|
<tbody>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c8" namest="c1"><SimplePara>(A) Magnetic resonance imaging</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Kim et al. (<CitationRef CitationID="CR135">2016</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>50</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>21.1</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>5.2</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>21.3</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>4.5</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Kim et al. (<CitationRef CitationID="CR135">2016</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>6</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>18.3</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>2.3</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>17.9</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>2.1</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lawson et al. (<CitationRef CitationID="CR151">2013</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>24</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>29.4</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>4.7</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>29.3</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>3.7</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Hétu et al. (<CitationRef CitationID="CR113">2016</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>34</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>27.88</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>8.49</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>28.03</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>8.18</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Carceller-Sindreu et al. (<CitationRef CitationID="CR33">2015</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>34</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>42.99</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>9.4</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>–</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Furman and Gotlib (<CitationRef CitationID="CR80">2016</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>13</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>28.7</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>2.5</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>27.3</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>7</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lawson et al. (<CitationRef CitationID="CR152">2017</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>25</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>22.31</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>9.29</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>–</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Savitz et al. (<CitationRef CitationID="CR225">2011a</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>75</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>36.9</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>8.5</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>19.8</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>5.1</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>17.1</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>4.6</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Savitz et al. (<CitationRef CitationID="CR226">2011b</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>74</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>36.5</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>8.7</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>19.5</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>5.2</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>17</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>4.7</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Schmidt et al. (<CitationRef CitationID="CR228">2017</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>20</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>34.92</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>11.34</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>17.63</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>5.49</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>17.29</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>6.12</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Zhang et al. (<CitationRef CitationID="CR288">2017</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>16</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>24.02</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>3.2</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>20.42</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>3.46</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Bocchetta et al. (<CitationRef CitationID="CR26">2016</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>15</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>23.6</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>2.2</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>23.3</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>2.2</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Torrisi et al. (<CitationRef CitationID="CR252">2017</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>32</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>18.8</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>6</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>14.9</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>4</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Hennigan et al. (<CitationRef CitationID="CR107">2015</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>18</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>35.35</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>13.3</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>–</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>–</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c2" namest="c1"><SimplePara> Extrapolated mean values</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>36.3</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>10.98</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>21.89</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>6.47</SimplePara></entry>
|
|
<entry align="left" colname="c7"><SimplePara>20.62</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>6.71</SimplePara></entry>
|
|
</row>
|
|
</tbody>
|
|
</tgroup>
|
|
<tgroup cols="12">
|
|
<colspec colnum="1" colname="c1" align="left"/>
|
|
<colspec colnum="2" colname="c2" align="char" char=""/>
|
|
<colspec colnum="3" colname="c3"/>
|
|
<colspec colnum="4" colname="c4"/>
|
|
<colspec colnum="5" colname="c5"/>
|
|
<colspec colnum="6" colname="c6"/>
|
|
<colspec colnum="7" colname="c7"/>
|
|
<colspec colnum="8" colname="c8" align="char" char=""/>
|
|
<colspec colnum="9" colname="c9"/>
|
|
<colspec colnum="10" colname="c10"/>
|
|
<colspec colnum="11" colname="c11"/>
|
|
<colspec colnum="12" colname="c12"/>
|
|
<thead>
|
|
<row>
|
|
<entry align="left" colname="c1" morerows="1"><SimplePara>Name</SimplePara></entry>
|
|
<entry align="left" colname="c2" morerows="1" nameend="c3" namest="c2"><SimplePara>Participants</SimplePara></entry>
|
|
<entry align="left" colname="c4" rowsep="1" nameend="c8" namest="c4"><SimplePara>Left habenula volume</SimplePara></entry>
|
|
<entry align="left" colname="c9" rowsep="1" nameend="c12" namest="c9"><SimplePara>Right HABENULA VOLUMe</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c4"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>SD</SimplePara></entry>
|
|
<entry align="left" colname="c6" nameend="c7" namest="c6"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c8"><SimplePara>SD</SimplePara></entry>
|
|
<entry align="left" colname="c9"><SimplePara>Medial</SimplePara></entry>
|
|
<entry align="left" colname="c10"><SimplePara>SD</SimplePara></entry>
|
|
<entry align="left" colname="c11"><SimplePara>Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c12"><SimplePara>SD</SimplePara></entry>
|
|
</row>
|
|
</thead>
|
|
<tbody>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c12" namest="c1"><SimplePara>(B) Postmortem</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c2" namest="c1"><SimplePara> Ranft et al. (<CitationRef CitationID="CR212">2010</CitationRef>)</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>13</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>3.35</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>1.33</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>27.57</SimplePara></entry>
|
|
<entry align="left" colname="c7" nameend="c8" namest="c7"><SimplePara>5.05</SimplePara></entry>
|
|
<entry align="left" colname="c9"><SimplePara>3.64</SimplePara></entry>
|
|
<entry align="left" colname="c10"><SimplePara>0.97</SimplePara></entry>
|
|
<entry align="left" colname="c11"><SimplePara>29.59</SimplePara></entry>
|
|
<entry align="left" colname="c12"><SimplePara>4.83</SimplePara></entry>
|
|
</row>
|
|
</tbody>
|
|
</tgroup>
|
|
</Table>
|
|
</Para>
|
|
<Para ID="Par20">In mammals, the habenula comprises of two functionally segregated nuclei, the medial habenula (MHb) and lateral habenula (LHb). The lateral is the larger of the two and is further divided into medial and lateral portions in humans and other mammals (Torrisi et al. <CitationRef CitationID="CR252">2017</CitationRef>; Fore et al. <CitationRef CitationID="CR77">2017</CitationRef>; Carpenter <CitationRef CitationID="CR36">1991</CitationRef>). These nuclei share many similar sources of afferent inputs and efferent nuclei but have distinct anatomy and connectivity within brain networks (Fakhoury <CitationRef CitationID="CR68">2017</CitationRef>; Bianco and Wilson <CitationRef CitationID="CR20">2009</CitationRef>; Gardon et al. <CitationRef CitationID="CR83">2014</CitationRef>).</Para>
|
|
<Section3 ID="Sec8">
|
|
<Heading>Medial habenula</Heading>
|
|
<Para ID="Par21">The medial habenula is the smaller and least studied of the two nuclei (Viswanath et al. <CitationRef CitationID="CR270">2013</CitationRef>; Iwahori <CitationRef CitationID="CR126">1977</CitationRef>; Ramon y Cajal <CitationRef CitationID="CR211">1911</CitationRef>). It borders the wall of the third ventricle and contains a more homogeneously densely packed array of cells when compared to the LHb. MHb volumes in human postmortem studies are reported in Table <InternalRef RefID="Tab2">2</InternalRef>b. The human MHb can be subdivided into five subnuclei, which can be most easily distinguished from each other in terms of cell packing density, as opposed to cell type. This is because most cells in each of the five nuclei are small round cells (Table <InternalRef RefID="Tab3">3</InternalRef>) (Diaz et al. <CitationRef CitationID="CR58">2011</CitationRef>). These cells have a soma diameter of 8.85.<Table ID="Tab3" Float="Yes">
|
|
<Caption Language="En">
|
|
<CaptionNumber>Table 3</CaptionNumber>
|
|
<CaptionContent><SimplePara>Summary of reported sub-nucleic histological characteristics of the human habenula</SimplePara></CaptionContent>
|
|
</Caption>
|
|
<tgroup cols="6">
|
|
<colspec colnum="1" colname="c1" align="left"/>
|
|
<colspec colnum="2" colname="c2" align="left"/>
|
|
<colspec colnum="3" colname="c3" align="left"/>
|
|
<colspec colnum="4" colname="c4" align="left"/>
|
|
<colspec colnum="5" colname="c5" align="left"/>
|
|
<colspec colnum="6" colname="c6" align="left"/>
|
|
<thead>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara>Subnuclei</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Cell shape and size</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Cellular distribution</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Fiber distribution</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Cell Packing</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>References</SimplePara></entry>
|
|
</row>
|
|
</thead>
|
|
<tbody>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c6" namest="c1"><SimplePara>Undifferentiated Habenula</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Ventromedial</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Very small celled, spindle shaped</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Densely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Marburg (<CitationRef CitationID="CR166">1944</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Medial</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small celled, larger and fewer cells, spindle shaped,</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Loosely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Marburg (<CitationRef CitationID="CR166">1944</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Dorsomedial</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small celled, larger and fewer cells, spindle shaped</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Loosely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Marburg (<CitationRef CitationID="CR166">1944</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Dorsolateral</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small spindle shaped and medium sized cells, polygonal, containing well-developed nuclei and trigoid bodies</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Marburg (<CitationRef CitationID="CR166">1944</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Large celled</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>-</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Marburg (<CitationRef CitationID="CR166">1944</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c6" namest="c1"><SimplePara>Medial habenula</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Dorsal</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Heterogenous with myelinated fibers</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Few fibers, forming bundles</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Intermediately packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Medial</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Homogenous</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Few fibers and very thin</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Loosely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Intermediate</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Homogenous</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Few fibers, forming a loose network</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Densely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Homogenous</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Few fibers and very thin</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Densely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Ventral</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round, medium round</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Homogenous</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Thin, with fibers emerging as fasciculus retroflexus</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Densely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1" nameend="c6" namest="c1"><SimplePara>Lateral habenula</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Dorsal</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>All cell types</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Heterogenous with myelinated fibers</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Many fibers, forming thick bundles</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Loosely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Medial</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round, medium round</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Heterogenous, with occasional clumping</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Very thin, reticulated pattern</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Loosely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Intermediate</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round, medium elongated, medium multipolar</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Heterogenous</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Few fibers and very thin, forming reticulated pattern</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Loosely packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Lateral</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round, small large multipolar</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Heterogenous with clumping</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Many fibers, forming a reticulated pattern</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Intermediately packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>Diaz et al. (<CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
<row>
|
|
<entry align="left" colname="c1"><SimplePara> Ventral</SimplePara></entry>
|
|
<entry align="left" colname="c2"><SimplePara>Small round, medium round and a few medium elongated</SimplePara></entry>
|
|
<entry align="left" colname="c3"><SimplePara>Heterogenous</SimplePara></entry>
|
|
<entry align="left" colname="c4"><SimplePara>Many fibers, thin, with fibers emerging as fasciculus retroflexus</SimplePara></entry>
|
|
<entry align="left" colname="c5"><SimplePara>Intermediately packed</SimplePara></entry>
|
|
<entry align="left" colname="c6"><SimplePara>(Diaz et al. <CitationRef CitationID="CR58">2011</CitationRef>)</SimplePara></entry>
|
|
</row>
|
|
</tbody>
|
|
</tgroup>
|
|
</Table>
|
|
</Para>
|
|
<Para ID="Par22">The medial habenula is richly innervated from multiple neuronal types. In animals, the predominant innervations to the MHb come from septal regions and are largely inhibitory through the action of GABAergic neurons (Torrisi et al. <CitationRef CitationID="CR252">2017</CitationRef>; Benarroch <CitationRef CitationID="CR17">2015</CitationRef>; Batalla et al. <CitationRef CitationID="CR14">2017</CitationRef>). Indeed, the medial habenula contains some of the highest concentration of GABA-B receptors in the rat brain (Wang et al. <CitationRef CitationID="CR274">2006</CitationRef>; Bischoff et al. <CitationRef CitationID="CR21">1999</CitationRef>; Durkin et al. <CitationRef CitationID="CR63">1999</CitationRef>; Charles et al. <CitationRef CitationID="CR39">2001</CitationRef>). However, other afferents terminate as cholinergic (Contestabile and Fonnum <CitationRef CitationID="CR48">1983</CitationRef>), substance P (Contestabile et al. <CitationRef CitationID="CR49">1987</CitationRef>) and glutamate (Qin and Luo <CitationRef CitationID="CR208">2009</CitationRef>). Additionally, the medial habenula abundantly expresses nicotinic acetylcholine receptors (Sheffield et al. <CitationRef CitationID="CR231">2000</CitationRef>). Monoamine inputs such as serotonin (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>), noradrenaline (Gottesfeld <CitationRef CitationID="CR88">1983</CitationRef>) and dopamine (Phillipson and Pycock <CitationRef CitationID="CR200">1982</CitationRef>) also target the MHb through feedback projections from the midbrain.</Para>
|
|
<Para ID="Par23">The MHb outputs extend through the core of the fasciculus retroflexus to the midbrain and hindbrain. MHb neurons are predominantly excitatory, releasing the neurotransmitters acetylcholine, substance P and glutamate (Aizawa et al. <CitationRef CitationID="CR3">2012</CitationRef>; Viswanath et al. <CitationRef CitationID="CR270">2013</CitationRef>). These neurons primarily target the serotonergic neurons of the median raphe nuclei directly or indirectly via interpeduncular nucleus (IPN) (Koppensteiner et al. <CitationRef CitationID="CR142">2016</CitationRef>; Contestabile et al. <CitationRef CitationID="CR49">1987</CitationRef>) and noradrenergic inputs from the locus coeruleus (Benarroch <CitationRef CitationID="CR17">2015</CitationRef>; Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>; Fakhoury <CitationRef CitationID="CR68">2017</CitationRef>; Bianco and Wilson <CitationRef CitationID="CR20">2009</CitationRef>). The IPN also provides feedback projections to brain areas that target the MHb such as the septal regions through the medial forebrain bundle (Hayakawa et al. <CitationRef CitationID="CR103">1981</CitationRef>) as well as the MHb itself (Benarroch <CitationRef CitationID="CR17">2015</CitationRef>). Of note, there are two principal subnuclei that can be identified using the transmitter acetylcholine in the ventral MHb and the expression of substance P in the dorsal MHb (Contestabile et al. <CitationRef CitationID="CR49">1987</CitationRef>; Hsu et al. <CitationRef CitationID="CR119">2016</CitationRef>). While they both project to the IPN, they innervate distinct structures within it (Hsu et al. <CitationRef CitationID="CR120">2014</CitationRef>).</Para>
|
|
</Section3>
|
|
<Section3 ID="Sec9">
|
|
<Heading>Lateral habenula</Heading>
|
|
<Para ID="Par24">The lateral habenula lies between the medial habenula and the thalamus. It is considerably larger than the MHb in most species and can be distinguished from the smaller structure microscopically by having a much less compacted and more heterogeneous cell population overall (Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>). The human LHb is greatly expanded compared to the MHb, with the LHb being about 8 times bigger than the MHb (Table <InternalRef RefID="other">2</InternalRef>). This suggests an increased influence of limbic and striatal afferents upon the DCSS in humans. The LHb can be further subdivided into medial LHb and lateral LHb subdomains. Five separate nuclei are observed in the LHb and these can be distinguished from each other in terms of the heterogenous cell shapes and sizes seen in the LHb as opposed to the packing density distinctions seen in the MHb (Table <InternalRef RefID="Tab3">3</InternalRef>) (Diaz et al. <CitationRef CitationID="CR58">2011</CitationRef>). The cellular organization within the LHb shows a larger degree of variability among individuals than the MHb and the distinction between nuclei is less precise; however, the broad overall cellular organization within the LHb is medial parvocellular and lateral magnocellular regions (Marburg <CitationRef CitationID="CR166">1944</CitationRef>).</Para>
|
|
<Para ID="Par25">The LHb innervations are generally more dispersed and heterogeneous than MHb afferents. Primary excitatory glutamatergic innervations originate from the prefrontal cortex, basal ganglia and lateral hypothalamus (Baker et al. <CitationRef CitationID="CR12">2016</CitationRef>; Batalla et al. <CitationRef CitationID="CR14">2017</CitationRef>). The majority of the fast-mediating excitatory transmission identified in the LHb is through the AMPA-type glutamate receptors (Meye et al. <CitationRef CitationID="CR171">2013</CitationRef>; Li et al. <CitationRef CitationID="CR158">2013</CitationRef>). The LHb receives strong inhibitory GABAergic inputs arising through long-range projections from areas such as the nucleus accumbens, diagonal band of Broca, the lateral preoptic area, substantia innominate and the ventral pallidum (Meye et al. <CitationRef CitationID="CR171">2013</CitationRef>; Benarroch <CitationRef CitationID="CR17">2015</CitationRef>). The medial globus pallidus GABA projections preferentially innervate the lateral portion of the LHb, whilst the diagonal band of Broca and lateral preoptic areas primarily target the medial portion (Herkenham and Nauta <CitationRef CitationID="CR110">1977</CitationRef>). Additionally, midbrain and hindbrain targets of the LHb provide dopaminergic (ventral tegmental area), noradrenergic (locus coeruleus) and serotonergic (median raphe nucleus) feedback projections, suggesting that dopamine, noradrenaline and serotonin have modulatory effects on the LHb (Meye et al. <CitationRef CitationID="CR171">2013</CitationRef>; Benarroch <CitationRef CitationID="CR17">2015</CitationRef>). Other inputs arise from the suprachiasmatic nucleus, providing GABA/vasopressinergic innervations into the LHb (Benarroch <CitationRef CitationID="CR17">2015</CitationRef>).</Para>
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<Para ID="Par26">In spite of sharing a singular output tract, there appears to be little overlap between efferents and function of the MHb and LHb (Quina et al. <CitationRef CitationID="CR209">2015b</CitationRef>). Through the external mantle of the FR, the LHb projects to multiple monoaminergic mesencephalic areas such as the ventral tegmental area (VTA) and periaqueductal gray and rhombencephalic areas such as raphe nucleus and locus coeruleus. In rodents, there exists a structure called the rostromedial tegmental nucleus (RMTg) which is essentially an inhibitory tail (Kaufling et al. <CitationRef CitationID="CR130">2009</CitationRef>) of the VTA (Holstege <CitationRef CitationID="CR117">2009</CitationRef>). It has been shown that most glutamatergic axons from the LHb primarily target the GABAergic neurons of the VTA and RMTg, leading to an overall inhibitory effect (Brinschwitz et al. <CitationRef CitationID="CR28">2010</CitationRef>). RMTg in particular exhibits a high density of habenular efferents, despite only accounting for less than 20% of the total outputs of the LHb to the hindbrain (Quina et al. <CitationRef CitationID="CR209">2015b</CitationRef>). The RMTg inhibits the nearby dopaminergic neurons of the VTA and substantia nigra pars compacta (SNc) directly and the serotonergic neurons of the raphe nuclei indirectly (Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>; Fakhoury <CitationRef CitationID="CR68">2017</CitationRef>). This intermediary structure has not been isolated as yet in human post-mortem studies (Hétu et al. <CitationRef CitationID="CR113">2016</CitationRef>). There are also direct bilateral innervations of the LHb to the VTA, with electrical stimulation of the LHb causing direct orthodromic reduction of dopaminergic tone in the VTA and its axons to the nucleus accumbens (Ji and Shepard <CitationRef CitationID="CR128">2007</CitationRef>; Christoph et al. <CitationRef CitationID="CR41">1986</CitationRef>). Similarly, lesioning the LHb causes an increase in serotoninergic activity in the dorsal raphe by activating the local GABAergic neurons (Varga et al. <CitationRef CitationID="CR262">2003</CitationRef>; Amat et al. <CitationRef CitationID="CR7">2001</CitationRef>) Retrograde studies have also identified the median raphe, caudal dorsal raphe, and pontine central gray as LHb targets (Quina et al. <CitationRef CitationID="CR209">2015a</CitationRef>). LHb efferents also feedback to the lateral hypothalamic area, septum and several thalamus nuclei (Benarroch <CitationRef CitationID="CR17">2015</CitationRef>; Batalla et al. <CitationRef CitationID="CR14">2017</CitationRef>).</Para>
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</Section3>
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</Section2>
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<Section2 ID="Sec10">
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<Heading>Function</Heading>
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<Para ID="Par27">Despite overlapping sources of connectivity, the medial and lateral habenula appear to represent largely distinct functional subcircuits within the DDCS. The MHb regulates inhibitory controls, cognition-dependent executive functions and place aversion learning (Gardon et al. <CitationRef CitationID="CR83">2014</CitationRef>). The MHb also has a role with respect to misery-fleeing behavior, stress responses, neural control of sleep and analgesia (Loonen et al. <CitationRef CitationID="CR164">2017</CitationRef>; Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>). These functions correspond with the inputs from the pleasure and motivational centers of the forebrain.</Para>
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<Para ID="Par28">Although the MHb has remained largely unstudied, it is proposed that two subnuclei, the ventral and dorsal subnuclei, are largely responsible for its functions. The ventral MHb, containing cholinergic neurons, has been associated with the somatic symptoms of nicotine withdrawal by inhibiting serotonin and dopamine within the IPN (Zhao-Shea et al. <CitationRef CitationID="CR290">2013</CitationRef>; Lee et al. <CitationRef CitationID="CR154">2019</CitationRef>). Whereas, the substance P containing dorsal MHb is implicated in fear responses (Lee et al. <CitationRef CitationID="CR154">2019</CitationRef>). A study in rodents demonstrated a reduction in activity of the dorsal medial habenula with fear conditioning. The authors suggested that diminished MHb may result due to interference with medial raphe nucleus activity, including hippocampal ripple activity and fear memory consolidation (Koppensteiner et al. <CitationRef CitationID="CR142">2016</CitationRef>).</Para>
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<Para ID="Par29">The LHb is involved in rewards signals, aversion and behavioral avoidance (Gardon et al. <CitationRef CitationID="CR83">2014</CitationRef>). These functions were first suggested following studies which revealed that the habenula was involved in reward through brain stimulation (Boyd and Celso <CitationRef CitationID="CR27">1970</CitationRef>). With the LHb long considered as the ‘missing link’ in the mechanisms of reward pathways (Brinschwitz et al. <CitationRef CitationID="CR28">2010</CitationRef>), efforts have been made to further uncover its exact functionality and underlying mechanisms. Studies in the lamprey show that when there is rewarding behavior, the LHb promotes the behaviour by intensifying stimulation of the phylogenetic homolog of the VTA (Loonen et al. <CitationRef CitationID="CR164">2017</CitationRef>). However, when the reward is smaller than expected or absent, the behavior is inhibited by affecting the VTA equivalent. Furthermore, the habenula has been implicated in circadian behaviour due to its connections with the nearby pineal and suprachiasmatic nucleus, with both MHb and in particular LHb cells showing increased firing during the day than night (Zhao and Rusak <CitationRef CitationID="CR289">2005</CitationRef>).</Para>
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<Para ID="Par30">Peptidomic analysis has identified a total of 262 and 177 neuropeptides in the medial and lateral habenula, respectively, with 126 present in both regions (Yang et al. <CitationRef CitationID="CR284">2018</CitationRef>). One of the peptides identified was somatostatin, often associated with chronic stress. Previously, stressed rats were reported to have significantly upregulated somatostatin receptors on the medial habenula (Faron-Górecka et al. <CitationRef CitationID="CR71">2016</CitationRef>). Additionally, multiple pain-related peptides (nociception, pro-enkephalin-A, pro-dynorphin-related prohormones) were also detected (Yang et al. <CitationRef CitationID="CR284">2018</CitationRef>). These peptides are involved in pain signaling mechanisms through the binding of opioid and nociception receptors. Such findings are consistent with current literature on habenular involvement in pain and analgesia (Shelton et al. <CitationRef CitationID="CR232">2012a</CitationRef>; Levins et al. <CitationRef CitationID="CR156">2019</CitationRef>).</Para>
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<Para ID="Par31">Significant findings from these extensive studies conducted in animals have led to investigations of the habenula in humans. All studies investigating the function of the human habenula have taken place using magnetic resonance imaging. Imaging the habenula suffers from resolution issues due to the size and shape of the structure and the resolution of standard functional MRI imaging. Also, due to position and shape, imaging this structure is further complicated as a result of its proximity to the third ventricle and subsequent partial volume effects. As such functional imaging studies of this structure are small in number and limited in scope. However, the habenula has been implicated in processing aversive stimuli (Lawson et al. <CitationRef CitationID="CR153">2014</CitationRef>; Hennigan et al. <CitationRef CitationID="CR107">2015</CitationRef>)and error detection (Ullsperger and von Cramon <CitationRef CitationID="CR258">2003</CitationRef>; Li et al. <CitationRef CitationID="CR157">2008</CitationRef>; Salas et al. <CitationRef CitationID="CR221">2010</CitationRef>; Ide and Li <CitationRef CitationID="CR125">2011</CitationRef>). The human habenula has been found to be functionally coupled with the insula, septum, thalamus, striatum, pons, substantia nigra/ventral tegmental area, periaqueductal gray, stria terminalis and parahippocampal regions (Hétu et al. <CitationRef CitationID="CR113">2016</CitationRef>; Torrisi et al. <CitationRef CitationID="CR252">2017</CitationRef>). The structure has also been functionally linked with pain responses (Shelton et al. <CitationRef CitationID="CR233">2012b</CitationRef>) subclinical depressive symptoms (Ely et al. <CitationRef CitationID="CR66">2016</CitationRef>), and anxious thoughts (Najafi et al. <CitationRef CitationID="CR187">2017</CitationRef>) in normal individuals. A promising new field of clinical research examining the habenula is underway with many studies implicating this diminutive structure in depression (Lawson et al. <CitationRef CitationID="CR152">2017</CitationRef>; Schmidt et al. <CitationRef CitationID="CR228">2017</CitationRef>), anxiety (Savitz et al. <CitationRef CitationID="CR225">2011a</CitationRef>), schizophrenia (Shepard et al. <CitationRef CitationID="CR235">2006</CitationRef>), frontotemporal dementia (Bocchetta et al. <CitationRef CitationID="CR26">2016</CitationRef>), addictions (Curtis et al. <CitationRef CitationID="CR56">2017</CitationRef>; Rose et al. <CitationRef CitationID="CR220">2017</CitationRef>) and chronic pain (Erpelding et al. <CitationRef CitationID="CR67">2014</CitationRef>), cancer-associated weight loss (Maldonado et al. <CitationRef CitationID="CR165">2018</CitationRef>) and Parkinson’s disease (Markovic et al. <CitationRef CitationID="CR167">2017</CitationRef>).</Para>
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<Section3 ID="Sec11">
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<Heading>Habenular asymmetry</Heading>
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<Section4 ID="Sec12">
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<Heading>Habenula</Heading>
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<Para ID="Par32">Many species exhibit asymmetries in size, anatomical organization and function (Schmidt and Pasterkamp <CitationRef CitationID="CR227">2017</CitationRef>; Bianco and Wilson <CitationRef CitationID="CR20">2009</CitationRef>; Concha and Ahumada-Galleguillos <CitationRef CitationID="CR43">2016</CitationRef>; Dreosti et al. <CitationRef CitationID="CR62">2014</CitationRef>; Ichijo et al. <CitationRef CitationID="CR122">2015</CitationRef>). The significance of this is unknown; however, an intriguing functional impact of left–right habenular differences has been found in zebrafish (Dreosti et al. <CitationRef CitationID="CR62">2014</CitationRef>; Krishnan et al. <CitationRef CitationID="CR144">2014</CitationRef>; Ichijo et al. <CitationRef CitationID="CR123">2017</CitationRef>; Halpern et al. <CitationRef CitationID="CR101">2003</CitationRef>) and in mice (Ichijo et al. <CitationRef CitationID="CR122">2015</CitationRef>, <CitationRef CitationID="CR123">2017</CitationRef>). In Zebrafish, lateralization appears more structurally fixed (Ichijo et al. <CitationRef CitationID="CR123">2017</CitationRef>), with habenular neurons shown to respond to light more frequently on the left; whereas, responses to odor were more likely to be found in the right habenula (Dreosti et al. <CitationRef CitationID="CR62">2014</CitationRef>). Meanwhile, in mice LHb lateralization appears more functionally flexible and occurs during postnatal development and in response to water-immersion restraint stress (Ichijo et al. <CitationRef CitationID="CR122">2015</CitationRef>, <CitationRef CitationID="CR123">2017</CitationRef>). However, small volume differences have also been described in mammals, including small asymmetries in the LHb in mice (Zilles et al. <CitationRef CitationID="CR291">1976</CitationRef>) and the MHb in rats (Wree et al. <CitationRef CitationID="CR279">1981</CitationRef>). Interestingly, a unique clump of cells has also been described on the left habenula only in the macrosomatic mole (Kemali <CitationRef CitationID="CR132">1984</CitationRef>).</Para>
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<Para ID="Par33">In primates and humans, the study of subtle habenular volume asymmetry is more difficult due to the small relative size of the habenula and its internal position deep within the brain. However, left–right asymmetry appears to occur in the lateral habenula in humans (independent of age, brain weight and total habenular size) and is more prominent in women (Ahumada-Galleguillos et al. <CitationRef CitationID="CR1">2017</CitationRef>). There also appears to be a functional asymmetry in the human habenula as evidenced by apparent differences in connectivity between left and right habenulae with the left habenula more coupled with the right parahippocampal regions and the right habenula more coupled with the substantia nigra/ventral tegmental regions (Hétu et al. <CitationRef CitationID="CR113">2016</CitationRef>). Additionally, a high-resolution volumetric MR study found a trend (but not of significance) towards a larger left habenula volume in both healthy controls and patients with depression and bipolar affective disorder (Savitz et al. <CitationRef CitationID="CR226">2011b</CitationRef>).</Para>
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</Section4>
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</Section3>
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</Section2>
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</Section1>
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<Section1 ID="Sec13">
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<Heading>Fasciculus retroflexus</Heading>
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<Para ID="Par34">(Lt; <Emphasis Type="Italic">backwards turning bunch/bundle</Emphasis>) The fasciculus retroflexus, also known as the fasciculus retroflexus of Meynert, habenulointerpeduncular tract, habenulopeduncular tract or retroflex tract, is the final component of the DDCS and principal efferent of the habenula, running ventrally from the habenula to the ventral midbrain and hindbrain (Aizawa et al. <CitationRef CitationID="CR2">2011</CitationRef>). Although originally described in 1872 as a tract originating from the habenula by Meynert (<CitationRef CitationID="CR172">1872</CitationRef>), Van Gehuchten was the first to define its distal end as joining the IPN (Van Gehuchten <CitationRef CitationID="CR261">1894</CitationRef>). Similar to the SM, the FR is also bidirectional tract and contains fibers originating from both the lateral and medial habenula (Herkenham <CitationRef CitationID="CR109">1981</CitationRef>).</Para>
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<Section2 ID="Sec14">
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<Heading>Anatomy</Heading>
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<Para ID="Par35">Although described since 1892 by Meynert, specific anatomical information regarding the precise trajectory of this tract in humans is sparse. This is due to the bending nature of the tract as well as the fact that it traverses a particularly structurally dense white matter region of the midbrain. Overall, the FR appears to take a lyre shape as it descends from the habenula to the IPN (Naidich and Duvernoy <CitationRef CitationID="CR186">2009</CitationRef>). In contrast to rats, where MHb fibers directly join the FR, human MHb fibers initially travel along the ventral part of the LHb before descending to unite with the FR (Díaz et al. <CitationRef CitationID="CR59">2011</CitationRef>). From the ventral aspect of the LHb, the FR travels down through the caudal thalamus, remaining medial to the centromedial nuclei (Naidich and Duvernoy <CitationRef CitationID="CR186">2009</CitationRef>). It then curves medially, continuing ventrally in front of the pretectal area along the rostromedial border of the red nucleus, penetrating the nucleus near its rostral pole. At the level of the basal plate, it subsequently turns at 90° caudally, to enter the IPN beneath the red nucleus. The abrupt change in direction is what gives this tract its name (retroflexus meaning recurve) Note that the FR enters the IPN from its rostral and dorsal borders (Naidich and Duvernoy <CitationRef CitationID="CR186">2009</CitationRef>). The fibers here cross and recross the midline IPN several times forming a figure eight pattern (Morley <CitationRef CitationID="CR181">1986</CitationRef>). Here they generate synapsis and appear to innervate both the ipsilatral and contralateral IPN (Contestabile and Flumerfelt <CitationRef CitationID="CR50">1981</CitationRef>; Moreno-Bravo et al. <CitationRef CitationID="CR177">2016</CitationRef>). An ill-defined nucleus of the interpeduncular tract has been documented in both animals (Rioch <CitationRef CitationID="CR215">1931</CitationRef>) and humans (Marburg <CitationRef CitationID="CR166">1944</CitationRef>). This nucleus consists of scattered neurons that lie between the medial and lateral parts of the tract and is of unknown function or significance.</Para>
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<Para ID="Par36">Structurally, the FR consists of two concentric regions. A bundle of very thin unmyelinated axons originating exclusively from the MHb travel through its core, and terminate after criss-crossing in both the contra and ipsilateral interpeduncular nuclei (Benarroch <CitationRef CitationID="CR17">2015</CitationRef>; Herkenham and Nauta <CitationRef CitationID="CR111">1979</CitationRef>; Moreno-Bravo et al. <CitationRef CitationID="CR177">2016</CitationRef>). Axons arising from the individual MHb subnuclei project down to specific regions of the IPN; dorsal MHb axons project to the lateral IPN, medial MHb axons to the ventral IPN, and lateral MHb axons to the dorsal IPN (Herkenham and Nauta <CitationRef CitationID="CR111">1979</CitationRef>; Ichijo and Toyama <CitationRef CitationID="CR124">2015</CitationRef>; Koppensteiner et al. <CitationRef CitationID="CR142">2016</CitationRef>). Projections from MHb to IPN decrease caudally, with no afferents of the MHb reaching the caudal pole of the IPN (Contestabile and Flumerfelt <CitationRef CitationID="CR50">1981</CitationRef>). The ventral MHb contains cholinergic neurons (Aizawa et al. <CitationRef CitationID="CR3">2012</CitationRef>) and the dorsal MHb contain Substance P neurons of the dorsal MHb (Contestabile et al. <CitationRef CitationID="CR49">1987</CitationRef>). The thicker myelinated fibers on the outer (mantle) FR emerge from the LHb (Benarroch <CitationRef CitationID="CR17">2015</CitationRef>; Herkenham <CitationRef CitationID="CR109">1981</CitationRef>), and to terminate directly in multiple monoaminergic nuclei including the ventral tegmental area, raphe nuclei, ventral periaqueductal gray and reticular formation. Note that the FR does not just consist of habenular efferents. Similar to other animals, the human FR also contains thalamic (pulvinar/midline nuclear group) fibers as well as ascending tectum fibers (Marburg <CitationRef CitationID="CR166">1944</CitationRef>).</Para>
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</Section2>
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<Section2 ID="Sec15">
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<Heading>Function</Heading>
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<Para ID="Par37">Information relayed from the SM through the habenula is ultimately transmitted through the FR (Batalla et al. <CitationRef CitationID="CR14">2017</CitationRef>) to the brainstem. Little specific information is available from human studies on the exact connectivity and function of the FR and as such most of its function is inferred from animal studies. Broadly speaking, the FR participates in inhibitory control of monoaminergic regions (Ellison <CitationRef CitationID="CR65">2002</CitationRef>).</Para>
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<Para ID="Par38">The core of the FR (i.e., originating from the MHb) is the principal cholinergic input of the interpeduncular nucleus (Hattori et al. <CitationRef CitationID="CR102">1977</CitationRef>). The IPN is well known for its widespread connections including ascending projections to the limbic system (hippocampus, entorhinal cortex and septal areas) and descending projections to the brainstem monoaminergic regions (VTA, raphe and periaqueductal gray) (Morley <CitationRef CitationID="CR181">1986</CitationRef>). The IPN outputs that synapse with these modulatory regions are GABAergic (Lima et al. <CitationRef CitationID="CR161">2017</CitationRef>). As such the MHb through the FR core exerts tonic inhibitory control on ascending monoaminergic neurons (Nishikawa et al. <CitationRef CitationID="CR191">1986</CitationRef>). Blocking muscarinic cholinergic transmission in the IPN results in increased levels of dopamine metabolism in more frontal areas such as the medial prefrontal cortex and nucleus accumbens (Nishikawa et al. <CitationRef CitationID="CR191">1986</CitationRef>). Bilateral lesioning of the FR in mice demonstrated a chronic increase in serotonin, noradrenaline and dopamine in the IPN (Takishita et al. <CitationRef CitationID="CR249">1990</CitationRef>). Following lesioning, there was evidence of hyperinnervation of the IPN by the afferent fibers from the locus coeruleus (NA) (Battisti et al. <CitationRef CitationID="CR15">1987</CitationRef>), raphe nucleus (serotonin) and other central areas (Takishita et al. <CitationRef CitationID="CR249">1990</CitationRef>). This progressive alteration in monoamines within the IPN is suggested to be implicated in cognitive processes, specifically the deterioration of choice accuracy (Bianco and Wilson <CitationRef CitationID="CR20">2009</CitationRef>).</Para>
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<Para ID="Par39">The FR mediates most of the negative feedback between the dopamine-receiving forebrain and the dopamine-releasing brainstem through the lateral habenula (Ellison <CitationRef CitationID="CR65">2002</CitationRef>). Continuous injections of dopaminergics, such as cocaine, MDMA, cathinone and amphetamine, in animals induced degeneration of the FR, particularly the outer sheath (Ellison <CitationRef CitationID="CR65">2002</CitationRef>). The disintegration of the FR may also underlie the development of progressive neuropsychiatric effects associated with repeated binges in addiction disorders, including paranoia (Carlson et al. <CitationRef CitationID="CR35">2000</CitationRef>; Ellison <CitationRef CitationID="CR64">1994</CitationRef>).</Para>
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<Para ID="Par40">Studies have demonstrated that the fasciculus retroflexus also has reciprocal ascending monoaminergic axons targeting the habenula (Smaha and Kaelber <CitationRef CitationID="CR240">1973</CitationRef>; Skagerberg et al. <CitationRef CitationID="CR239">1984</CitationRef>; Li et al. <CitationRef CitationID="CR159">1993</CitationRef>). These axons are confined to the outer sheath of the FR and as such specifically connect with the lateral habenula (Skagerberg et al. <CitationRef CitationID="CR239">1984</CitationRef>). The FR provides dense DA innervations to the LHb, particularly its medial region, from the VTA and substantia nigra pars compacts (Skagerberg et al. <CitationRef CitationID="CR239">1984</CitationRef>; Li et al. <CitationRef CitationID="CR159">1993</CitationRef>; Shen et al. <CitationRef CitationID="CR234">2012</CitationRef>). Previous literature suggest that DA has an inhibitory role in LHb and potentially is involved in the regulation of the habenular response to aversive and painful stimuli (Brown and Shepard <CitationRef CitationID="CR29">2013</CitationRef>; Shen et al. <CitationRef CitationID="CR234">2012</CitationRef>). Lesions of the FR weakened the density of dopaminergic nerve terminals in the LHb in rats (Shen et al. <CitationRef CitationID="CR234">2012</CitationRef>; Skagerberg et al. <CitationRef CitationID="CR239">1984</CitationRef>), indicating that the FR must be intact to transmit positive reward signals from the brainstem dopaminergic system to the LHb.</Para>
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</Section2>
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</Section1>
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<Section1 ID="Sec16">
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<Heading>Development</Heading>
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<Para ID="Par41">As the name suggests, the DDCS is embryologically part of the diencephalon, a prosencephalic (forebrain) structure between the telencephalon and mesen- and rhombencephalon. Indeed, the main function of the DDCS components are as processing conduits to relay information between telencephalic and mesen/rhombencephalic structures. Similar to the development of other epithalamic gray matter structures, initially the habenular nuclei form early on, closely followed by their efferent and then followed by their afferent connections (Cho et al. <CitationRef CitationID="CR40">2014</CitationRef>; Altman and Bayer <CitationRef CitationID="CR6">1979</CitationRef>).</Para>
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<Para ID="Par42">The diencephalon is formed of distinct segments, prosomeres (p1, p2 and p3) and neuromeres (D1, D2, D3, and D4), with circumferential axonal tracts forming around the neuromere boundaries (Funato et al. <CitationRef CitationID="CR79">2000</CitationRef>). The habenula forms from the alar plate of p2 (Schmidt and Pasterkamp <CitationRef CitationID="CR227">2017</CitationRef>), the SM is formed along D2 (Lim and Golden <CitationRef CitationID="CR160">2007</CitationRef>) and the FR is formed along the p1/p2 boundary (Funato et al. <CitationRef CitationID="CR79">2000</CitationRef>). Axon guidance molecules are expressed in adjacent neuromeres guiding the axonal growth (Funato et al. <CitationRef CitationID="CR79">2000</CitationRef>). Among these molecules is the repulsive axon guidance molecule Sema3F. This is found in the diencephalon and is expressed in p1, leading to repulsion from habenular explants. Whereas Netrin-1, an attractant, is expressed from the caudal to the ventral regions of the diencephalon (Funato et al. <CitationRef CitationID="CR79">2000</CitationRef>).</Para>
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<Para ID="Par43">The larger neurons of the lateral nucleus develop before the smaller neurons of the medial nucleus in rodents (Angevine <CitationRef CitationID="CR9">1970</CitationRef>), resulting in the establishment of a clear latero-medial or “outside-in” progression. This gradient appears to exist both across the whole habenula and within each lateral and medial habenular nuclei (Altman and Bayer <CitationRef CitationID="CR6">1979</CitationRef>). In humans, habenular cytogenesis starts around the fifth week and is completed by approximately weeks 7–8 (Muller and O'Rahilly <CitationRef CitationID="CR183">1997</CitationRef>) with the habenular commissure also present in most embryos by the start of the eighth week (Muller and O'Rahilly <CitationRef CitationID="CR182">1990</CitationRef>).</Para>
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<Para ID="Par44">The efferent white matter FR is characterized by immediate growth of axons from the developing habenula, with the FR extending towards the mesen/rhombencephalon and rapidly reaching the interpeduncular nucleus around the end of week 6. The relationship of the FR and the parvocellular red nucleus is variable during development (Cho et al. <CitationRef CitationID="CR40">2014</CitationRef>); however, the newly formed tract appears to migrate gradually towards the red nucleus to lodge into a deep groove on the medial aspect of the red nucleus sometime after week 12 (Yamaguchi and Goto <CitationRef CitationID="CR281">2008</CitationRef>). Embryologically, the FR appears to develop its complex trajectory along three decision points: (1) repulsive signals <Emphasis Type="Italic">Sema3F</Emphasis> and <Emphasis Type="Italic">Sema5A</Emphasis> complement the attractive signal <Emphasis Type="Italic">Netrin1</Emphasis> to funnel the developing FR along a corridor in front of the pretectum allowing dorsoventral extension from the habenula, (2) sudden retroflexion caudally due to <Emphasis Type="Italic">Slit1</Emphasis> repulsion from the floor plate, and (3) finally criss-crossing across the IPN complexes (Moreno-Bravo et al. <CitationRef CitationID="CR177">2016</CitationRef>). Myelination of the FR occurs much later in development, with completion sometime after 35 weeks (Yamaguchi and Goto <CitationRef CitationID="CR281">2008</CitationRef>). Similar to other epithalamic structures, the afferent tract develops slightly later, with the SM forming from the telencephalic nuclei and eventually reaching the habenula around week 8 (Muller and O'Rahilly <CitationRef CitationID="CR182">1990</CitationRef>).</Para>
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</Section1>
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<Section1 ID="Sec17">
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<Heading>Conclusion</Heading>
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<Para ID="Par45">This is the first review to describe in-depth all the components of the dorsal diencephalic conduction system: the stria medullaris, habenula and fasciculus retroflexus. The anatomy and connections of the DDCS reflect its function as an integrator of reward, motivational, cognitive and emotional information from diffuse basal forebrain regions within the habenular relay. From this hub, habenular outputs can modulate the regulatory brainstem regions. Despite the potential importance of this circuit in neuropsychiatric disorders, this review highlights the clear lack of human studies into the DDCS and its components in humans. What is known of the human DDCS appears inconsistent, particularly the specific networks of the habenular afferents and efferents. While there is an abundance of animal studies on the DDCS connections, there has been just one study that has physically traced the connections in humans (Marburg <CitationRef CitationID="CR166">1944</CitationRef>), as such it is not clear whether many of these animal networks map accurately onto the larger human forebrain (Herculano-Houzel <CitationRef CitationID="CR108">2009</CitationRef>). Furthermore, habenular function in humans has not been clearly defined, specifically with regards to the functional importance of known habenular laterality (Hétu et al. <CitationRef CitationID="CR113">2016</CitationRef>), which appears to be of particular significance in other vertebrates (Ahumada-Galleguillos et al. <CitationRef CitationID="CR1">2017</CitationRef>; Concha and Ahumada-Galleguillos <CitationRef CitationID="CR43">2016</CitationRef>). The difficulty of studying such small anatomical structures in humans is without a doubt a contributor to the lack of replicable research of this system. This is particularly relevant for human in vivo studies, where imaging techniques struggle to capture the structures at current resolutions. New advances in neuroimaging such as increased scanner strengths, image acquisition improvements, and higher-order diffusion tractography (Tournier et al. <CitationRef CitationID="CR253">2011</CitationRef>), functional imaging (Craddock et al. <CitationRef CitationID="CR53">2015</CitationRef>) and magnetic resonance spectroscopy protocol refinements (Drago et al. <CitationRef CitationID="CR61">2018</CitationRef>) may aid future investigations into the structure and function of the DDCS in humans in vivo. Additionally, more human post-mortem studies using established (e.g., DiI, horseradish peroxidase) (Von Bartheld et al. <CitationRef CitationID="CR271">1990</CitationRef>; Schmued <CitationRef CitationID="CR229">1994</CitationRef>; Tardif and Clarke <CitationRef CitationID="CR250">2001</CitationRef>) and pioneering neurotracing methods (e.g., viral tracers) (Schmued <CitationRef CitationID="CR230">2016</CitationRef>; Lai et al. <CitationRef CitationID="CR147">2018</CitationRef>) to determine the diffuse basal forebrain connections of the DDCS neurocircuitry are needed to reveal the complicated habenular connectome. Further exploration of this pivotal system may progress our insight into the pathophysiology of many neuropsychiatric disorders, particularly major depressive disorders, anxiety disorders, addiction and pain disorders, and open novel therapeutics targets for investigation.</Para>
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</Section1>
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</Body>
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<BodyRef FileRef="406_2020_1128_OnlinePDF.pdf" TargetType="OnlinePDF"/>
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<ArticleBackmatter>
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<Bibliography ID="Bib1">
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<Heading>References</Heading>
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<Citation ID="CR1">
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<BibArticle>
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<BibAuthorName>
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<Initials>P</Initials>
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<FamilyName>Ahumada-Galleguillos</FamilyName>
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</BibAuthorName>
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<BibAuthorName>
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<Initials>CG</Initials>
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<FamilyName>Lemus</FamilyName>
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</BibAuthorName>
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<BibAuthorName>
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<!-- Query ID="Q5" Text="AUTHOR: As References Quina et al., 2015a and Quina et al., 2015b are same, we have deleted the duplicate reference and renumbered accordingly. Please check and confirm." -->
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