Rethinking Phylogeny and Ontogeny in Hominin Brain Evolution

Theories of hominin and human cognitive evolution have traditionally focused on the phylogeny of the human brain, and on comparisons of human and primate brains in relation to social or ecological variables. Far less attention has been paid to ontogenetic processes, despite the recognition that experience has a profound influence on adult cognition. In this paper we discuss the interplay between phylogeny and ontogeny by examining relationships between human brain size, developmental scheduling and cognition. The correlates of large brains include not only altered subsistence and life-history strategies to meet associated energetic costs, but also on macro- and micro-scale structural adaptations required to meet increased processing costs. This means that larger brains are of necessity more highly interconnected brains, with higher degrees of folding of the neocortex (gyrification) and higher ratios of myelinated connections between neurons (white matter) to neurons themselves (grey matter). Here we argue that the combination of these evolutionary trends underpins the complexity of human behaviour, as the neural circuits involved in cognitive mechanisms such as the mirror neuron system (the system governing motor emulation and imitation) and theory of mind (fundamental in social cognition) mature only slowly, and require considerable socially-scaffolded experience to develop to their full potential. These abilities are likely to be fundamental in characteristically human behaviours such as the cultural transmission of complex forms of tool manufacture and use, attested to in the archaeological record. Their elaborated modern human forms, we argue, are possible only in the context of the evolution of relatively slower trajectories of brain growth and hence longer periods during which the growing brain can be influenced by experience among modern humans relative to other primates. Here we review some of the differences in ontogenetic brain development between humans and other primates, and compare the rates and trajectories of neural development between ourselves and our closest living relatives the chimpanzees to suggest that the human pattern of expanded periods of growth coupled with slower trajectories of neural development is likely to have been of huge significance during hominin evolution. In addition, we discuss fossil and archaeological proxies which might allow the reconstruction of evolutionary patterns of development, suggesting that it is only post-Homo erectus and specifically among Homo heidelbergensis and Homo neanderthalensis populations that developmental patterns approximate those of modern humans, arguing for a similar – but not identical – role for socially-scaffolded learning of complex technical skills as among modern groups in these species