Primate-specific origins and migration of cortical GABAergic neurons

Zdravko Petanjek

doi:10.3389/neuro.05.026.2009

Abstract

Gamma-aminobutyric-acidergic (GABAergic) cells form a very heterogeneous population of neurons that play a crucial role in the coordination and integration of cortical functions. Their number and diversity increase through mammalian brain evolution. Does evolution use the same or different developmental rules to provide the increased population of cortical GABAergic neurons? In rodents, these neurons are not generated in the pallial proliferative zones as glutamatergic principal neurons. They are produced almost exclusively by the subpallial proliferative zones, the ganglionic eminence (GE) and migrate tangentially to reach their target cortical layers. The GE is organized in molecularly different subdomains that produce different subpopulations of cortical GABAergic neurons. In humans and non-human primates, in addition to the GE, cortical GABAergic neurons are also abundantly generated by the proliferative zones of the dorsal telencephalon. Neurogenesis in ventral and dorsal telencephalon occurs with distinct temporal profiles. These dorsal and ventral lineages give rise to different populations of GABAergic neurons. Early-generated GABAergic neurons originate from the GE and mostly migrate to the marginal zone and the subplate. Later-generated GABAergic neurons, originating from both proliferative sites, populate the cortical plate. Interestingly, the pool of GABAergic progenitors in dorsal telencephalon produces mainly calretinin neurons, a population known to be significantly increased and to display specific features in primates. We conclude that the development of cortical GABAergic neurons have exclusive features in primates that need to be considered in order to understand pathological mechanisms leading to some neurological and psychiatric diseases.

Highlights

IntroductionThe cerebral cortex, including the hippocampal formation, is composed of two main classes of neurons: principal and nonprincipal cells.The first and the more numerous class (around 80% of the neurons) corresponds mainly to pyramidal cells, which are excitatory glutamatergic neurons (for reviews see DeFelipe and Jones, 1988; Spruston, 2008)
The cerebral cortex, including the hippocampal formation, is composed of two main classes of neurons: principal and nonprincipal cells.The first and the more numerous class corresponds mainly to pyramidal cells, which are excitatory glutamatergic neurons
The authors suggested that the dorsal telencephalic origin of cortical GABAergic neurons might be human-specific (Letinic et al, 2002), but we demonstrated more recently that this occurs in the macaque monkey (Macaca rhesus and Macaca fascicularis) (Petanjek et al, 2009)

Summary

Introduction

The cerebral cortex, including the hippocampal formation, is composed of two main classes of neurons: principal and nonprincipal cells.The first and the more numerous class (around 80% of the neurons) corresponds mainly to pyramidal cells, which are excitatory glutamatergic neurons (for reviews see DeFelipe and Jones, 1988; Spruston, 2008). Several types of such so-called interneurons have an axon that project to distant brain regions (Ribak et al, 1986; Toth and Freund, 1992; Jinno et al, 2007; Tomioka and Rockland, 2007; for review see Jinno, 2009). These GABAergic neurons form a very heterogenous population that plays a crucial role in regulating the activity of neuronal networks and complex interactions among principal cells (Somogyi and Klausberger, 2005; Skaggs et al, 2007). The coordination and integration of cortical functions depends on the number and diversity of GABAergic neurons

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