Evolution of the cerebellar cortex: The selective expansion of prefrontal-projecting cerebellar lobules

Abstract

It has been suggested that interconnected brain areas evolve in tandem because evolutionary pressures act on complete functional systems rather than on individual brain areas. The cerebellar cortex has reciprocal connections with both the prefrontal cortex and motor cortex, forming independent loops with each. Specifically, in capuchin monkeys cerebellar cortical lobules Crus I and Crus II connect with prefrontal cortex, whereas the primary motor cortex connects with cerebellar lobules V, VI, VIIb, and VIIIa. Comparisons of extant primate species suggest that the prefrontal cortex has expanded more than cortical motor areas in human evolution. Given the enlargement of the prefrontal cortex relative to motor cortex in humans, our hypothesis would predict corresponding volumetric increases in the parts of the cerebellum connected to the prefrontal cortex, relative to cerebellar lobules connected to the motor cortex. We tested the hypothesis by comparing the volumes of cerebellar lobules in structural MRI scans in capuchins, chimpanzees and humans. The fractions of cerebellar volume occupied by Crus I and Crus II were significantly larger in humans compared to chimpanzees and capuchins. Our results therefore support the hypothesis that in the cortico-cerebellar system, functionally related structures evolve in concert with each other. The evolutionary expansion of these prefrontal-projecting cerebellar territories might contribute to the evolution of the higher cognitive functions of humans.

Human frontal lobes are not relatively large

“…Neocortex, cerebellum, and intermediate nuclei, for example, show closely correlated evolution in terms of both volume and neuron numbers, after controlling for variability in the size or neuron numbers of other brain regions (15,32,37,38), suggesting that selective expansion of cortico-cerebellar systems was a general feature of primate brain evolution. Frontal and more posterior cortical regions both exhibit this pattern, though they have different correlations with specific regions of the cerebellum and basal ganglia (38,39). Thus, the evolution of frontal regions such as PFC may be best understood in terms of their participation in more distributed networks.…”

The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost

“…This is a strong argument against neocorticalization (in what concerns numbers of neurons) and in favor of the coordinated increase in numbers of neurons across the cortex and cerebellum related to the behavioral and cognitive (not only sensorimotor) functions that corticocerebellar circuits mediate as brain size increased on multiple, independent occasions in evolution. The coordinated addition of neurons to cerebral cortex and cerebellum thus argues for coordinated corticocerebellar function and a joint evolution of the processing abilities of the two structures (32-34), a view also supported by the concerted increase in size of the prefrontal cerebral cortex, prefrontal inputs to the corticopontine system, and prefrontal-projecting cerebellar lobules in primates (33,34). The issue then becomes accounting for how the cerebral cortex increases in size faster than the cerebellum as both gain neurons coordinately.…”

Clonal analysis reveals granule cell behaviors and compartmentalization that determine the folded morphology of the cerebellum

“…It will be important to determine whether neural progenitor behaviors in gyrencephalic mammals are differentially regulated in distinct neocortex folds. Finally, as the number of cells in the Cb and neocortex have scaled together during evolution, along with a selective expansion of cerebellar folia connected to prefrontal cortex circuits from simian to human (Balsters et al, 2010;Herculano-Houzel, 2010), the spatial segregation of neurons into folia might have played a crucial role in the coordinated expansion and co-evolution of functionally connected circuits in the two brain regions.…”