Abstract

Adult neurogenesis in mammals is predominantly restricted to two brain regions, the dentate gyrus (DG) of the hippocampus and the olfactory bulb (OB), suggesting that these two brain regions uniquely share functions that mediate its adaptive significance. Benefits of adult neurogenesis across these two regions appear to converge on increased neuronal and structural plasticity that subserves coding of novel, complex, and fine-grained information, usually with contextual components that include spatial positioning. By contrast, costs of adult neurogenesis appear to center on potential for dysregulation resulting in higher risk of brain cancer or psychological dysfunctions, but such costs have yet to be quantified directly. The three main hypotheses for the proximate functions and adaptive significance of adult neurogenesis, pattern separation, memory consolidation, and olfactory spatial, are not mutually exclusive and can be reconciled into a simple general model amenable to targeted experimental and comparative tests. Comparative analysis of brain region sizes across two major social-ecological groups of primates, gregarious (mainly diurnal haplorhines, visually-oriented, and in large social groups) and solitary (mainly noctural, territorial, and highly reliant on olfaction, as in most rodents) suggest that solitary species, but not gregarious species, show positive associations of population densities and home range sizes with sizes of both the hippocampus and OB, implicating their functions in social-territorial systems mediated by olfactory cues. Integrated analyses of the adaptive significance of adult neurogenesis will benefit from experimental studies motivated and structured by ecologically and socially relevant selective contexts.

Highlights

  • To understand the adaptive significance of adult neurogenesis, in terms of how and why it has evolved, three main questions can usefully be addressed: First, what are the specific advantages of adult neurogenesis, and why, at least among mammals, is it largely restricted to the dentate gyrus (DG) and olfactory bulb (OB), in contrast to other brain regions? Presumably these two regions share some particular functional, information processing roles that benefit from neurogenetic plasticity in addition to the universal system of synaptic plasticity (Lemaire et al, 2012)

  • We have provided an overview of the mechanisms and adaptive significance of adult neurogenesis in mammals focused on the question of why this process is largely restricted to two brain regions, the DG and OB that otherwise appear unrelated in their functions and forms of information processing

  • A primary conclusion is that the benefits of adult neurogenesis in the DG and OB appear to involve encoding and decoding of relatively novel and complex information that commonly includes spatial components, and that such benefits appear to rely on the properties of relatively-young neurons

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Summary

Introduction

The pattern separation hypothesis (Figure 5) proposes that adult neurogenesis serves to generate neuronal networks better-capable of discriminating between similar, complex sets of environmental stimuli for generation of representations in memory (Clelland et al, 2009; Aimone et al, 2011; Sahay et al, 2011; Kesner, 2013).

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