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WIREs Dev Biol
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The development of hippocampal cellular assemblies

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The proper assembly of a cohort of distinct cell types is a prerequisite for building a functional hippocampus. In this review, we describe the major molecular events of the developmental program leading to the cellular construction of the hippocampus. Data from rodent studies are used here to elaborate on our understanding of these processes. WIREs Dev Biol 2014, 3:165–177. doi: 10.1002/wdev.127 This article is categorized under: Signaling Pathways > Cell Fate Signaling Nervous System Development > Vertebrates: Regional Development
Schema for the hippocampal structures, and lamination. (a) A schematic horizontal mouse brain section shows the structural organization of the hippocampal formation, which includes the dentate gyrus (DG), the hippocampus proper (CA1–CA3), the subiculum (S), the presubiculum (PrS), the parasubiculum (PaS), and the entorhinal cortex (EC). A cognitive functional map has been proposed for the hippocampal formation: DG for pattern separation, CA3 for pattern completion, CA1 for input integration, S for retrieval, and EC for brief retention. The inset in the bottom corner shows a sagittal section of adult mouse brain and the area in the green box corresponds to the general structures in the schematic diagram. (b) The schematic layer organization in the mature hippocampus is shown: Alveus is the deepest layer that contains the axons from the pyramidal neurons. Superficial to the alveolus is the stratum oriens (so), which mostly contains the inhibitory local interneurons. The stratum pyramidale (sp) is the principal cell layer in the hippocampus proper. Superficial to the stratum pyramidale of CA3 is the stratum lucidum (sl), which is occupied by mossy fibers projecting from the dentate granule cells. The stratum radiatum (sr) is located superficial to the stratum lucidum in CA3 and the pyramidal cell layer in the CA1 and CA2. The stratum radiatum of CA3 contains self‐associated fibers from the stratum pyramidale of CA3, whereas stratum radiatum of CA1 contains Schaffer collateral fibers projected from CA3. The most superficial layer in the hippocampus proper is called the stratum lacunosum‐moleculare (slm), which contains the perforant path fibers projected from the entorhinal cortex.The principal cell layer in the dentate gyrus is called the stratum granulosum (sg), or more commonly referred to as ‘granular cell layer’ in the literature. Superficial to the granule cell layer is the stratum moleculare (sm) or more commonly referred to as ‘molecular layer’ in the literature. The dentate molecular layer contains fibers projected from the hilus and the entorhinal cortex. The granule cell layer and molecular layer are sometimes collectively referred to as the fascia dentata. Deep to the granule cell layer is the polymorphic cell layer, usually referred to as the hilus (H). Mossy cells are the main projection neurons in the hilus. The region at the border between the granule cell layer and hilus is called the subgranular zone (SGZ). A, anterior; L, lateral; CA, the abbreviation of cornu ammonis; DG, dentate gyrus; EC, entorhinal cortex; F, fimbria; H, hilus; PrS, presubiculum; PaS, parasubiculum; S, subiculum; SO, stratum oriens; SP, stratum pyramidale; SR, stratum radiatum; SLM, stratum lacunosum‐moleculare; SL, stratum lucidum; SM, stratum moleculare; SG, stratum granulosum.
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Formation of the germinative matrices at different locations during the development of the dentate gyrus. This schematic shows the developmental program used during the formation of the dentate gyrus (see Figure for overall schema of adult hippocampal formation including dentate gyrus). (a) The primary germinative matrix (green dots) forms at the ventricular zone and the subventricular zone of the dentate primordium around E13.5. (b) The secondary germinative matrix (blue dots) develops around E15.5 in the junctional area between the fimbria and the developing dentate pole. (c) The tertiary matrix (orange dots) emerges in the hilus around perinatal ages, while the secondary germinative matrix further extends subpially and wraps around the presumptive dentate pole. (d) The final germinative matrix (red dots) is established in the subgruanular zone by the second postnatal week. D, dentate primordium; dgl, dentate granular layer; DN, dentate notch; F, fimbria; FDJ, fimbriodentate junction; H, hilus; HF, hippocampal fissure; Hip, hippocampal primordium. (Reprinted with permission from Ref. Copyright 2013, Academic press)
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Origins and migratory routes of hippocampal interneurons. (a) A schematic coronal section at the level that contains LGE and MGE at E15.5. (b) A schematic coronal section at the level that contains CGE at E15.5. (c) A schematic horizontal section that contains LGE, MGE and CGE at E15.5. Hippocampal interneurons originated at LGE, MGE, POA (a) or CGE (b) take a lateral route and course through the neocortex before reaching the hippocampus. Alternatively, some hippocampal interneurons from CGE (c) take a caudal route to enter the hippocampus. CGE, caudal ganglion eminence; hip, hippocampus; LGE, lateral ganglion eminence; MGE, medial ganglion eminence; ncx, neocortex; POA, preoptic area; S, septum. (Reprinted with permission from Ref. Copyright 2013, Academic press)
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The classic hippocampal migration defects. (a) The normal distribution of the projection neurons in the hippocampus. (b) Glia‐independent somal translocation is mostly affected in the mutants Relnrl/rl or Dab1scm/scm, in which the CA1 layer is duplicated (arrows) and the dentate pole is filled up with granule cells (arrowheads). (C) Glia‐dependent locomotion is mostly affected in the Cdk5 conditional mutant mediated by Emx1‐cre. The pyramidal layer (CA1–CA3) is loosely organized and the dentate gyrus fails to form distinct upper and lower blades (arrowheads). (d) Multipolar migration is mostly affected in the Dcx mutant, in which the CA3 field is discontinuous from other CA regions (arrowhead) and develops split layering (arrows).
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The different zones in the developing hippocampus and the different modes of neuronal migration. From deep to superficial in the E14 coronal mouse brain section, the hippocampal fields can be divided into different zones: VZ, SVZ, IZ, HP, and MZ (see text for more description). Migrating neurons derived from the radial glia adopt different modes of migration as they course through the different zones. Multipolar migration is dominant in the SVZ, and glia‐mediated locomotion is mostly seen in the IZ/HP. As their long processes attach to the MZ, they switch to the terminal somal translocation. VZ, ventricular zone; SVZ, subventricular zone; IZ, intermediate zone; HP, hippocampal plate; MZ, marginal zone.
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The specification of the hippocampal primordium. The schematic coronal sections from E9 to E11 (a, b, and c) show how the invagination of the dorsomedial telencephalon leads to the formation of the archipallium, which gives rise to the hippocampal complex.
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