Cellular dynamics of neuronal migration in the hippocampus

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.

CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

“…In rodents, PCs in the CA regions are generated in the ventricular zone, and then migrate toward the pial surface (the hippocampal fissure), ultimately settling into the hippocampal plate, the future PC layer 137 . Hippocampal laminar formation takes places in an inside-out pattern, in which earlier-born cells form the deeper part of the PC layer, whereas the later-born neurons pass the older cells and settle in the more superficial part, as in the neocortex 138–140 .…”

“…However, in contrast to the relatively straight path of the radially migrating neocortical neurons, hippocampal cells migrate toward the hippocampal plate obliquely at first, followed by a more conventional radial route 141 . In addition, neocortical migrating neurons typically proceed using a single radial fiber as scaffold, whereas migrating future hippocampal pyramidal neurons use multiple radial glial fibers and migrate considerably more slowly 137 . Furthermore, clonally related CA1 neurons are distributed in a more horizontal manner, not in a well-defined vertical column as in the case of neocortical PCs 109 .…”

“…Furthermore, clonally related CA1 neurons are distributed in a more horizontal manner, not in a well-defined vertical column as in the case of neocortical PCs 109 . The obscuring of the basic inside-out pattern may be related to the ongoing horizontal expansion of the relatively thin hippocampal plate during development, which may make it difficult for clonally related cells to be strictly vertically aligned 137 . It should be noted that postmitotic cells can migrate tangentially from one to another radial glia even in the neocortex 142 , and it is possible that the difference in dispersion is related to the more tortuous path taken by radial glia in the hippocampus.…”

Actin Aggregations Mark the Sites of Neurite Initiation

“…In both the cerebral cortex and hippocampus, neurons are born in the ventricular zone (VZ) and then migrate respectively to the cortical plate (CP) and stratum pyramidale (SP) [56,57], with the net effect that neurons in the VZ/subventricular zone (SVZ) region are less mature than those in CP or SP. We thus in utero electroporated GFP-actinin, which binds to and crosslinks F-actin [52], together with cytoplasmic tdTomato, in E15.5 rat embryos and examined the F-actin distribution in neurons of the VZ/ SVZ and CP/SP regions in E18.5 embryos.…”

Excessive activation of AhR signaling disrupts neuronal migration in the hippocampal CA1 region in the developing mouse

“…Mammalian brain development is temporally and spatially regulated by several physiological processes in an orchestrated manner. Neurite outgrowth and neuronal migration are essential processes for the formation of neural circuits, and these processes are regulated by complex molecular mechanisms (Hayashi et al, 2015;Whitford et al, 2002). Thus, it is reasonable to speculate that the disruption of AhR signaling impairs the molecular mechanisms that control neural circuit formation during development, which leads to behavioral abnormalities in adulthood.…”