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Visual specialization and brain evolution in primates.

ABSTRACT: Several theories have been proposed to explain the evolution of species differences in brain size, but no consensus has emerged. One unresolved question is whether brain size differences are a result of neural specializations or of biological constraints affecting the whole brain. Here I show that, among primates, brain size variation is associated with visual specialization. Primates with large brains for their body size have relatively expanded visual brain areas, including the primary visual cortex and lateral geniculate nucleus. Within the visual system, it is, in particular, one functionally specialized pathway upon which selection has acted: evolutionary changes in the number of neurons in parvocellular, but not magnocellular, layers of the lateral geniculate nucleus are correlated with changes in both brain size and ecological variables (diet and social group size). Given the known functions of the parvocellular pathway, these results suggest that the relatively large brains of frugivorous species are products of selection on the ability to perceive and select fruits using specific visual cues such as colour. The separate correlation between group size and visual brain evolution, on the other hand, may indicate the visual basis of social information processing in the primate brain.

SUBMITTER: Barton RA

PROVIDER: S-EPMC1689478 | biostudies-literature | 1998 Oct

REPOSITORIES: biostudies-literature

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Visual specialization and brain evolution in primates.

Barton R A RA

Proceedings. Biological sciences 19981001 1409

Several theories have been proposed to explain the evolution of species differences in brain size, but no consensus has emerged. One unresolved question is whether brain size differences are a result of neural specializations or of biological constraints affecting the whole brain. Here I show that, among primates, brain size variation is associated with visual specialization. Primates with large brains for their body size have relatively expanded visual brain areas, including the primary visual ...[more]

PMID: 9821360

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Project description:Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.

Project description:Recent branching (100 MYA) of the mammalian evolutionary tree has enhanced brain complexity and functions at the putative cost of increased emotional circuitry vulnerability. Thus, to better understand psychopathology, a burden for the modern society, novel approaches should exploit evolutionary aspects of psychiatric-relevant molecular pathways. A handful of genes is nowadays tightly associated to psychiatric disorders. Among them, neuronal-enriched RbFOX1 modifies the activity of synaptic regulators in response to neuronal activity, keeping excitability within healthy domains. We here dissect a higher primates-restricted interaction between RbFOX1 and the transcriptional corepressor Lysine Specific Demethylase 1 (LSD1/KDM1A). A single nucleotide variation (AA to AG) in LSD1 gene appeared in higher primates and humans, endowing RbFOX1 with the ability to promote the alternative usage of a novel 3' AG splice site, which extends LSD1 exon E9 in the upstream intron (E9-long). Exon E9-long regulates LSD1 levels by Nonsense-Mediated mRNA Decay. As reintroduction of the archaic LSD1 variant (AA) abolishes E9-long splicing, the novel 3' AG splice site is necessary for RbFOX1 to control LSD1 levels. LSD1 is a homeostatic immediate early genes (IEGs) regulator playing a relevant part in environmental stress-response. In primates and humans, inclusion of LSD1 as RbFOX1 target provides RbFOX1 with the additional ability to regulate the IEGs. These data, together with extensive RbFOX1 involvement in psychiatric disorders and its stress-dependent regulation in male mice, suggest the RbFOX1-LSD1-IEGs axis as an evolutionary recent psychiatric-relevant pathway. Notably, outside the nervous system, RbFOX2-dependent LSD1 modulation could be a candidate deregulated mechanism in cancer.SIGNIFICANCE STATEMENT To be better understood, anxiety and depression need large human genetics studies aimed at further resolving the often ambiguous, aberrant neuronal pathomechanisms that impact corticolimbic circuitry physiology. Several genetic associations of the alternative splicing regulator RbFOX1 with psychiatric conditions suggest homeostatic unbalance as a neuronal signature of psychopathology. Here we move a step forward, characterizing a disease-relevant higher primates-specific pathway by which RbFOX1 acquires the ability to regulate neuronal levels of Lysine Specific Demethylase 1, an epigenetic modulator of environmental stress response. Thus, two brain-enriched enzymes, independently shown to homeostatically protect neurons with a clear readout in terms of emotional behavior in lower mammals, establish in higher primates and humans a new functional cooperation enhancing the complexity of environmental adaptation and stress vulnerability.

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Visual specialization and brain evolution in primates.

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Visual specialization and brain evolution in primates.

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