Embodied cognitive evolution and the cerebellum

Abstract

Much attention has focused on the dramatic expansion of the forebrain, particularly the neocortex, as the neural substrate of cognitive evolution. However, though relatively small, the cerebellum contains about four times more neurons than the neocortex. I show that commonly used comparative measures such as neocortex ratio underestimate the contribution of the cerebellum to brain evolution. Once differences in the scaling of connectivity in neocortex and cerebellum are accounted for, a marked and general pattern of correlated evolution of the two structures is apparent. One deviation from this general pattern is a relative expansion of the cerebellum in apes and other extractive foragers. The confluence of these comparative patterns, studies of ape foraging skills and social learning, and recent evidence on the cognitive neuroscience of the cerebellum, suggest an important role for the cerebellum in the evolution of the capacity for planning, execution and understanding of complex behavioural sequences--including tool use and language. There is no clear separation between sensory-motor and cognitive specializations underpinning such skills, undermining the notion of executive control as a distinct process. Instead, I argue that cognitive evolution is most effectively understood as the elaboration of specialized systems for embodied adaptive control.

Figure 1.

White matter proportion increases more steeply with size in neocortex than in cerebellum. The proportion of volume of (a) neocortex and (b) cerebellum that is white matter, plotted against volume of each structure (mm³). The graphs plot data for the same species and the PGLS slopes are significantly different (see text).

Figure 2.

Contrast in the pattern of variation in the proportion of the brain composed of neocortex versus cerebellum when expressed as (a) volume proportion and (b) proportional number of neurons. Dark bars represent cortical proportions and light bars denote cerebellar proportions.

Figure 3.

Difference in relative numbers of neurons in (a) the neocortex and (b) cerebellum of primates (open circles) compared to other mammals (filled circles). Controlling for numbers of neurons in the rest of the brain, the difference between primates and non-primates is significant for neocortex (PGLS; λ = 0.86, t_3,23 = 3.43, p = 0.002) and cerebellum (PGLS; λ = 0.76, t_3,23 = 4.54, p = 0.0002). The effect is stronger for cerebellar neurons and the primate–non-primate difference in cerebellar neurons is still near-significant after controlling for neocortical neurons (PGLS; λ = 0.61, t_4,23 = 2.02, p = 0.06).

Figure 4.

Correlated evolution of neocortex and cerebellum size in mammals. Neocortex size and cerebellum size are positively correlated after controlling for phylogenetic effects and volume of other brain regions (PGLS, neocortex volume regressed on volume of cerebellum controlling for volume of the rest of the brain; λ = 0.97, t_3,298 = 8.85, p < 0.0001).