The evolution of the human brain, long before human

An overarching goal of cognitive neuroscience is to understand how the human brain implements mental functions such as attention, memory storage and retrieval, decision-making, etc. However, mapping structure to function in the brain is proving to be difficult, and neural data persistently violates our assumptions about the distinctions between functional systems. I suggest that this is because the organization of the brain was never aimed at implementing the functions we now ascribe to its modern form, but is instead the result of a long and idiosyncratic history of adaptations to different species-typical environments, each of which was accomplished by modifications to an ancestral developmental “Bauplan” that strongly constrains the phenotype of descendants. Consequently, the real distinctions are determined more by developmental processes than by the functional capacities that they may ultimately achieve. Fortunately, comparative data make it possible to reconstruct the major stages in the long and idiosyncratic history of brain adaptations along the lineage that leads to humans, which we can then use as a baseline set of constraints for developing a theory of the functional organization of the brain that respects the evolutionary process that produced it. In my talk, I will outline some of these major stages and suggest the functional adaptations they made possible. I will begin with the formation of the chordate neural tube and its differentiation in early vertebrates into a spinal cord, a sensorimotor midbrain, and a modulatory prosencephalon capable of reinforcement learning. I will then discuss the transition to land and the specialization of pallial segments to support local exploitation and long-range exploration in early tetrapods. Next I will discuss the retreat into a nocturnal niche in mammals, accompanied by the expansion of the dorsal pallium into a neocortex subdivided into a dorsomedial sector supporting sensorimotor action maps for search, handling, ingestion, and defense, and a ventrolateral sector supporting key stimulus detection and interoceptive integration. Finally, I will discuss the primate return to diurnal life in the arboreal niche, and the expansion of fronto-parietal action maps for visually-guided interaction and temporo-orbital mechanisms for object classification and valuation. I will then return to neural data and suggest how it may be better interpreted using such a phylogenetically-based functional architecture than by mainstream models in cognitive neuroscience.