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Neuronal diversity and reciprocal connectivity between the vertebrate hippocampus and septum

Advanced Review

Archana Iyer, Shubha Tole

Published Online: Dec 18 2019

DOI: 10.1002/wdev.370

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Abstract A hallmark of the nervous system is the precision with which myriad cell types are integrated into functional networks that control complex behaviors. The limbic system governs evolutionarily conserved processes essential for survival. The septum and the hippocampus are central to the limbic system, and control not only emotion‐related behaviors but also learning and memory. Here, we provide a developmental and evolutionary perspective of the hippocampus and septum and highlight the neuronal diversity and circuitry that connects these two central components of the limbic system. This article is categorized under: Nervous System Development > Vertebrates: Regional Development Nervous System Development > Vertebrates: General Principles Comparative Development and Evolution > Regulation of Organ Diversity

Embryonic origin of hippocampal interneurons. The Nkx2.1 lineage from the medial ganglionic eminence (MGE) gives rise to parvalbumin, somatostatin, nNOS, and reelin positive interneurons that populate all the layers in the developing hippocampus. The GAD65 lineage arising from the caudal ganglionic eminence (CGE) gives rise to VIP, CR, nNOS negative neurogliaform cells, reelin, and cholecystokinin (CCK) interneurons that are not found in the stratum oriens. Abbreviations: so, stratum oriens; sp, stratum pyramidale; sr, stratum radiatum; slm, stratum lacunosum moleculare. (Reprinted with permission from (Hirata et al., ). Copyright 2009 Springer Nature)

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Transcriptome‐based diversity within the hippocampus. (a) Schematic representation of the dorsal and ventral hippocampus in coronal sections of the adult rodent brain. (b) Schematics indicating the superficial and deep layers of the CA1, the proximal‐distal axis, and (c) the dorsal‐ventral axis. (Reprinted with permission from (Cembrowski, Bachman, et al., ; Cembrowski, Wang, et al., ). Copyright 2016 Elsevier)

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Origin of septal neurons and the contribution of different progenitor domains to the neuronal diversity in the septum. Illustration of a hemidissected coronal mouse brain at E13.5 marking progenitor domains from which different class of neurons destined for distinct septal nuclei arise (Bialowas & Frotscher, ; Colom et al., ; Magno et al., ; Sotty et al., ; Watanabe et al., ; Wei et al., ). Abbreviations: CB, calbindin; ChAT, choline acetyl transferase; CR, calretinin; MGE, medial ganglionic eminence; POA, pre optic area; PV, parvalbumin; SEP, septum; Sep NE, septal neuroepithelium; TE, thalamic eminence; vGlut2, vesicular glutamate transporter 2. The schematics for the progenitor domains obtained from Hirata et al. (). Mouse brain schematics for the septal nuclei reprinted with permission from Lein et al. (). Copyright 2004 Allen Institute for Brain Science. Allen Mouse Brain Atlas. Available from: https://mouse.brain‐map.org/static/brainexplorer

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Septal nuclei in the mouse brain. Schematic representation of the mouse brain. Dotted lines indicate the plane of the section. Coronal sections indicate the medial (red), lateral (green), and posterior (blue) septal complex. (Reprinted with permission from Lein et al. (). Copyright 2004 Allen Institute for Brain Science. Allen Mouse Brain Atlas. Available from: https://mouse.brain‐map.org/static/brainexplorer). Information on septal divisions was obtained from following references: (Jakab & Leranth, ; Risold, ; Risold & Swanson, ; Swanson & Cowan, ). Abbreviations: BAC, bed nucleus of anterior commissure; DB, diagonal band; LSc, lateral septum caudal; LSr, lateral septum rostral; LSv, lateral septum ventral; MS: medial septum; SF, septofimbrial; SH, septohippocampal; TRS, triangular septal nucleus

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The anatomy of the septum and the hippocampus in different vertebrate species. Abbreviations: DB, diagonal band; DC, dorsal cortex; Dld, dorsal part of area dorsalis telencephali; Hb, habenula; HP, hippocampus; HYP, hypothalamus; LSd, lateral septum, dorsal; LSv, lateral septum, ventral; MC, medial cortex; MP, medial pallium; MS, medial septum; OB, olfactory bulb; OC, optic chiasm; POA, pre optic area; Vl and Vv, lateral and ventral nuclei of area ventralis telencephali; SA, anterior septal nucleus; SL, lateral septal nucleus; SM, medial septal nucleus; SVM, ventromedial septal nucleus.For each species, red lines in the right cartoons indicate the plane of section shown in the left cartoon. (Reprinted with permission from the following references. Fish (Wullimann & Rink, ), Frog (González & López, ), Copyright 2002 Elsevier, Lizard (Font, Lanuza, Martinez‐marcos, Hoogland, & Martinez‐garcia, ), Copyright 1998 John Wiley and Sons, and Chick (Montagnese, Székely, Ádám, & Csillag, ), Copyright 2004 John Wiley and Sons.)

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The septum verum and septum pellucidum in the human brain. (a) Human brain (Courtesy: Pixabay and Allen brain Atlas) (b) Septum verum in the adult human brain from (Andy & Stephan, ) (c) and (d) cavum septi and the adjoining septum pellucidum in human fetal brain at 22 weeks of gestation (Rakic & Yakovlev, ). (b) and (c) reused with permission. Abbreviations: SP, septum pellucidum; CA, cavum septum; CC, corpus callosum

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