A cerebellar substrate for cognition evolved multiple times independently in mammals

Abstract

Given that complex behavior evolved multiple times independently in different lineages, a crucial question is whether these independent evolutionary events coincided with modifications to common neural systems. To test this question in mammals, we investigate the lateral cerebellum, a neurobiological system that is novel to mammals, and is associated with higher cognitive functions. We map the evolutionary diversification of the mammalian cerebellum and find that relative volumetric changes of the lateral cerebellar hemispheres (independent of cerebellar size) are correlated with measures of domain-general cognition in primates, and are characterized by a combination of parallel and convergent shifts towards similar levels of expansion in distantly related mammalian lineages. Results suggest that multiple independent evolutionary occurrences of increased behavioral complexity in mammals may at least partly be explained by selection on a common neural system, the cerebellum, which may have been subject to multiple independent neurodevelopmental remodeling events during mammalian evolution.

eLife digest

The brains of mammals consist of the same basic structures, but each of these structures varies from one species to the next. A given structure may be larger in one species than another, for example. It may contain different numbers or sizes of cells. It may even have different connections to other brain regions. By comparing individual brain structures between species, we can map how the mammalian brain has evolved.

Smaers et al. have now done this for the cerebellum, a structure at the back of the brain. The mammalian cerebellum consists of three main areas: the vermis, paravermis, and the lateral hemispheres. Smaers et al. show that in apes, dolphins and seals, the lateral hemispheres are unusually large relative to the cerebellum as a whole. This could indicate that these three groups of animals share a common ancestor with enlarged lateral hemispheres. Yet, genetic studies suggest that this is not the case.

Another possibility is that apes, dolphins and seals independently evolved enlarged lateral hemispheres. This may have given rise to a trait that proved beneficial for each of them. But what might this be? Studies in people suggest that the lateral hemispheres help to support some forms of learning. Apes, dolphins and seals are among only a few species of mammal with the ability to learn new calls and vocalizations. The expansion of the lateral cerebellum may therefore have contributed to the evolution of vocal learning, and this may have occurred independently on at least three separate occasions.

Future work should extend this analysis to other cognitive skills, as well as to other species. Bats, for example, would be of particular interest because of their ability to echolocate. Finally, the lateral hemispheres consist of several subregions that play different roles in learning and information processing. Further experiments should explore whether different subregions have increased in size in different species.