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Review
. 2015 Apr 24:9:135.
doi: 10.3389/fnins.2015.00135. eCollection 2015.

Cellular dynamics of neuronal migration in the hippocampus

Kanehiro Hayashi  1 , Ken-Ichiro Kubo  1 , Ayako Kitazawa  1 , Kazunori Nakajima  1
Affiliations
Review

Cellular dynamics of neuronal migration in the hippocampus

Kanehiro Hayashi et al. Front Neurosci. .

Abstract

A fine structure of the hippocampus is required for proper functions, and disruption of this formation by neuronal migration defects during development may play a role in some psychiatric illnesses. During hippocampal development in rodents, pyramidal neurons in the Ammon's horn are mostly generated in the ventricular zone (VZ), spent as multipolar cells just above the VZ, and then migrate radially toward the pial surface, ultimately settling into the hippocampal plate. Although this process is similar to that of neocortical projection neurons, these are not identical. In addition to numerous histological studies, the development of novel techniques gives a clear picture of the cellular dynamics of hippocampal neurons, as well as neocortical neurons. In this article, we provide an overview of the cellular mechanisms of rodent hippocampal neuronal migration including those of dentate granule cells, especially focusing on the differences of migration modes between hippocampal neurons and neocortical neurons. The unique migration mode of hippocampal pyramidal neurons might enable clonally related cells in the Ammon's horn to distribute in a horizontal fashion.

Keywords: Ammon's horn; climbing mode; dentate gyrus; hippocampus; layer pattern; migration.

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Figures

Figure 1
Figure 1
Schematic diagrams of migration and layer arrangement on the neocortex and hippocampal CA1 during cortical development. (A) Neocortical neurons born between E10 and E12 radially migrate using the somal translocation mode. In contrast, late-born neurons transform their migration mode sequentially to multipolar migration, locomotion mode, and terminal translocation mode during their radial migration. These neurons form neocortical layers in a birthdate-dependent inside-out manner. (B) Hippocampal CA1 neurons born at late developmental stages change the migration mode to multipolar migration and then to the climbing mode. The migration mode used by early-born CA1 neurons remains unknown (somal translocation mode is a candidate). The layer arrangement in the Ammon's horn is thought to occur roughly in a birth-date dependent inside-out manner (another claim was also reported; see text for details). PP, preplate; VZ, ventricular zone; MZ, marginal zone; CP, cortical plate; IZ, intermediated zone; MAZ, multipolar cell accumulation zone; WM, white matter; HP, hippocampal plate; SLM, stratum lacunosum-moleculare; SR, stratum radiatum; SP, stratum pyramidale; SO, stratum oriens.
Figure 2
Figure 2
Schema of migration of dentate cells during hippocampal development. Newborn granule cells from the dentate notch migrate to the secondary dentate matrix (SDM) (indicated by a brown arrow). The cells then migrate to the subpial surface to form the outer part of the dentate granule cell layer (light blue arrow 1), followed by the dentate hilus (light blue arrow 2), which is called the tertiary dentate matrix (TDM) at this stage, to later form the inner part of the layer. Cells in the TDM exhibit proliferative activities into adulthood, although the proliferative region becomes restricted to the subgranular zone. In contrast, pyramidal neurons in the hippocampal CA1 and neocortex are generated in the Ammonic ventricular zone and the neocortical ventricular zone, respectively, and migrate in a radial direction (indicated by magenta and black arrows, respectively).
See this image and copyright information in PMC

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