Laterality and the evolution of the prefronto-cerebellar system in anthropoids

Abstract

There is extensive evidence for an early vertebrate origin of lateralized motor behavior and of related asymmetries in underlying brain systems. We investigate human lateralized motor functioning in a broad comparative context of evolutionary neural reorganization. We quantify evolutionary trends in the fronto-cerebellar system (involved in motor learning) across 46 million years of divergent primate evolution by comparing rates of evolution of prefrontal cortex, frontal motor cortex, and posterior cerebellar hemispheres along individual branches of the primate tree of life. We provide a detailed evolutionary model of the neuroanatomical changes leading to modern human lateralized motor functioning, demonstrating an increased role for the fronto-cerebellar system in the apes dating to their evolutionary divergence from the monkeys (∼30 million years ago (Mya)), and a subsequent shift toward an increased role for prefrontal cortex over frontal motor cortex in the fronto-cerebellar system in the Homo-Pan ancestral lineage (∼10 Mya) and in the human ancestral lineage (∼6 Mya). We discuss these results in the context of cortico-cerebellar functions and their likely role in the evolution of human tool use and speech.

Figure 1

Results from a phylogenetically generalized least squares analysis of correlations in the relative size of the posterior cerebellar hemispheres, frontal motor areas, and prefrontal cortex. Hemisphere-specific regressions between frontal and cerebellar structures were performed contralaterally, because evidence suggests the importance of contralateral connections in the fronto-cerebellar system.

Figure 2

Comparative analysis of evolutionary rates of the posterior cerebellar hemispheres (PCH), frontal motor areas (FM), and prefrontal cortex (PF). Rates were compared for individual branches of the primate phylogenetic tree, allowing detailed inferences of the evolutionary history of fronto-cerebellar systems across 46 million years of divergent primate evolution.