The adaptive significance of adult neurogenesis: an integrative approach

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.

Keywords: adaptive significance; adult neurogenesis; evolution; olfaction; pattern separation.

Figure 1

Schematic of adult neurogenesis in the DG and OB. Sagittal view of rodent brain (Top left) showing sites of neurogenesis in the SVZ/OB and SGZ/DG. Cells proliferate mainly in the SVZ, migrate along the rostral migratory stream (RMS) to the OB where (Right) they migrate radially and undergo differentiation and integration into OB circuit. Neuron precursors from the SGZ proliferate and migrate a short distance to the DG (left) before differentiation into granule neurons and integration into the DG circuit.

Figure 2

Newborn neurons proliferate in the SGZ and migrate to the DG where they differentiate and integrate into the hippocampal circuitry. Newborn DG neurons become excitatory granule cells receiving input from the entorhinal cortex and projecting to the CA3 subregion of the hippocampus.

Figure 3

Neuroblasts migrate to the OB from the SVZ, then differentiate and integrate into the OB circuitry. Newborn neurons in the OB become (A) inhibitory granule cells and (B) periglomerular interneurons (also inhibitory) which both modulate mitral cell activity. Olfactory receptor neurons express one type of odor receptor and receptor neurons with the same receptor type project to the same glomerulus where they synapse onto mitral cells. Mitral cells receive information from olfactory receptor neurons and project to the olfactory cortex.

Figure 4

The molecular signatures of tumor subtypes parallel the stages of adult neurogenesis. Adapted from Phillips et al. (2006).

Figure 5

Pattern separation hypothesis of adult neurogenesis, developed for the dentate gyrus but recently extended to the olfactory bulb. Pattern separation refers to the discrimination between similar, complex sets of environmental stimuli (e.g., spatial information) for the generation of representations in memory (Aimone et al., 2010). Here, “events” refer to components of memories that are very similar and easily confused for one another. (e.g., similar spatial cues in a similar environment). Pattern separation enables these components of memory to be encoded into distinct complex memory representations that are unique and less easily confused. They also retain their temporal structure which is largely provided by having immature neurons in the DG circuitry.

Figure 6

Memory resolution hypothesis of adult neurogenesis. Whereas pattern separation represents an effect or component of the primary, over-arching function of adult neurogenesis, memory resolution increases the amount and structure of information encoded by particular brain regions via a combination of (1) younger neuronal populations with low-specificity, densely-sampled representations, which better-encode novel environmental features, with (2) older neurons with high-specificity, sparsely-sampled representations, encoding more-familiar aspects of the environment. The diagram again shows that distinct, complex memory representations are encoded, but also that they are more separated from each other and more detail is encoded.

Figure 7

Olfactory spatial hypothesis of adult neurogenesis. By this hypothesis, adult neurogenesis subserves spatial-navigational functions by functionally decoding and mapping odorants (Jacobs, 2012). The hypothesis focuses on the central roles of high-resolution spatially-explicit olfaction in mammalian food location, individual recognition, homing, and anti-predator behavior. Diagram shows a “complex spatial” environment with various odors that are represented or encoded by adult born neurons, which then represent the visual and olfactory map space. This hypothesis can be extended to DG function, where other contextual information (e.g., emotional) can be spatially mapped.

Figure 8

Model that reconciles the pattern separation, memory resolution, and olfactory spatial hypothesis for adult neurogenesis. A complex series of events occurs in space and time (Left) which are encoded by the DG and OB where they are separated (Right, where events or stimuli are more distinguished from one another). Stimuli that are especially novel, complex, and fine-grained, and include spatial-contextual and spatial-odor information, are better processed via adult neurogenesis.

Figure 9

Structural equation models of the effect of population density and home range size, two variables of importance to the territorial social system of solitary primates, on the allometry of brain components. Each standardized path coefficient indicates the number of standard deviations increase in the dependent variable caused by an increase of one standard deviation in the independent variable; coefficients are significant at α = 0.01 (two asterisks) or α = 0.05 (single asterisk).