Embracing covariation in brain evolution

Behavioral and Evolutionary Neuroscience Group, Department of Psychology, Cornell University, Ithaca NY, USA.
Progress in brain research (Impact Factor: 2.83). 01/2012; 195:71-87. DOI: 10.1016/B978-0-444-53860-4.00004-0
Source: PubMed


Brain size, body size, developmental length, life span, costs of raising offspring, behavioral complexity, and social structures are correlated in mammals due to intrinsic life-history requirements. Dissecting variation and direction of causation in this web of relationships often draw attention away from the factors that correlate with basic life parameters. We consider the "social brain hypothesis," which postulates that overall brain and the isocortex are selectively enlarged to confer social abilities in primates, as an example of this enterprise and pitfalls. We consider patterns of brain scaling, modularity, flexibility of brain organization, the "leverage," and direction of selection on proposed dimensions. We conclude that the evidence supporting selective changes in isocortex or brain size for the isolated ability to manage social relationships is poor. Strong covariation in size and developmental duration coupled with flexible brains allow organisms to adapt in variable social and ecological environments across the life span and in evolution.

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Available from: Barbara Finlay
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    • "The main biological substrate for mammalian mental abilities is the neuronal circuitry of the cerebral cortex. Tremendous evolutionary increase in the neuron number and cortical connections (DeFelipe, 2011; Charvet and Finlay, 2012) allowed humans to adopt language and mathematical skills, to make affective modulation of emotional cues, possess self-conceptualization, mentalization, as well as to have high capacity of cognitive flexibility and working memory (Rakic, 2009). Such complex functioning is strongly related to distinct expansion of multimodal – high order associative areas, particularly the granular areas of the frontal lobe (i.e., associative prefrontal cortex; Teffer and Semendeferi, 2012). "
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    ABSTRACT: In this article we first point at the expansion of associative cortical areas in primates, as well as at the intrinsic changes in the structure of the cortical column. There is a huge increase in proportion of glutamatergic cortical projecting neurons located in the upper cortical layers (II/III). Inside this group, a novel class of associative neurons becomes recognized for its growing necessity in both inter-areal and intra-areal columnar integration. Equally important to the changes in glutamatergic population, we found that literature data suggest a 50% increase in the proportion of neocortical GABAergic neurons between primates and rodents. This seems to be a result of increase in proportion of calretinin interneurons in layers II/III, population which in associative areas represents 15% of all neurons forming those layers. Evaluating data about functional properties of their connectivity we hypothesize that such an increase in proportion of calretinin interneurons might lead to supra-linear growth in memory capacity of the associative neocortical network. An open question is whether there are some new calretinin interneuron subtypes, which might substantially change micro-circuitry structure of the primate cerebral cortex.
    Full-text · Article · Sep 2014 · Frontiers in Neuroanatomy
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    • "The observation that variation in isocortical anatomy is systematic across primates despite these species filling different niches suggests that the large-scale global changes in the isocortex described here are not directly tied to behavior, ecology or niches. That is, the isocortex employs these developmental changes and its flexible nature may allow the organism to adapt to its environment [Charvet and Finlay, 2012]. "
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    ABSTRACT: Spatial gradients in the initiation and termination of basic processes, such as cytogenesis, cell-type specification and dendritic maturation, are ubiquitous in developing nervous systems. Such gradients can produce a niche adaptation in a particular species. For example, the high density of photoreceptors and neurons in the 'area centralis' of some vertebrate retinas result from the early maturation of its center relative to its periphery. Across species, regularities in allometric scaling of brain regions can derive from conserved spatial gradients: longer neurogenesis in the alar versus the basal plate of the neural tube is associated with relatively greater expansion of alar plate derivatives in larger brains. We describe gradients of neurogenesis within the isocortex and their effects on adult cytoarchitecture within and across species. Longer duration of neurogenesis in the caudal isocortex is associated with increased neuron number and density per column relative to the rostral isocortex. Later-maturing features of single neurons, such as soma size and dendritic spine numbers reflect this gradient. Considering rodents and primates, the longer the duration of isocortical neurogenesis in each species, the greater the rostral-to-caudal difference in neuron number and density per column. Extended developmental duration produces substantial, predictable changes in the architecture of the isocortex in larger brains, and presumably a progressively changed functional organization, the properties of which we do not yet fully understand. Many features of isocortical architecture previously viewed as species- or niche-specific adaptations can now be integrated as the natural outcomes of spatiotemporal gradients that are deployed in larger brains. © 2014 S. Karger AG, Basel.
    Full-text · Article · Sep 2014 · Brain Behavior and Evolution
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    • "This has been attributed to natural selection favoring either a high level of general intelligence (Reader et al., 2011) or similarities in evolution of domain-specific cognitive modules (Fodor, 1983; Cosmides et al., 2010), due to shared socioecological pressures in these lineages. The extent to which cognition has evolved as a modular process remains an ongoing source of debate among neuroscientists (recently reviewed in Charvet and Finlay, 2012; Vilarroya, 2012). However, given the importance of distinct ecological skills needed to solve different foraging challenges (e.g., spatial memory for relocating fruit, innovative problem solving for tool use) and new data correlating sensorimotor intelligence with a specific brain structure , the cerebellum (Barton, 2012), we hypothesize that distinct cognitive skills, driven by different ecological challenges, were favored in some primate lineages over the course of evolution. "
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    ABSTRACT: The parallel evolution of increased sensorimotor intelligence in humans and capuchins has been linked to the cognitive and manual demands of seasonal extractive faunivory. This hypothesis is attractive on theoretical grounds, but it has eluded widespread acceptance due to lack of empirical data. For instance, the effects of seasonality on the extractive foraging behaviors of capuchins are largely unknown. Here we report foraging observations on four groups of wild capuchins (Cebus capucinus) inhabiting a seasonally dry tropical forest. We also measured intra-annual variation in temperature, rainfall, and food abundance. We found that the exploitation of embedded or mechanically protected invertebrates was concentrated during periods of fruit scarcity. Such a pattern suggests that embedded insects are best characterized as a fallback food for capuchins. We discuss the implications of seasonal extractive faunivory for the evolution of sensorimotor intelligence (SMI) in capuchins and hominins and suggest that the suite of features associated with SMI, including increased manual dexterity, tool use, and innovative problem solving are cognitive adaptations among frugivores that fall back seasonally on extractable foods. The selective pressures acting on SMI are predicted to be strongest among primates living in the most seasonal environments. This model is proffered to explain the differences in tool use between capuchin lineages, and SMI as an adaptation to extractive foraging is suggested to play an important role in hominin evolution.
    Full-text · Article · Jun 2014 · Journal of Human Evolution
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