Neurodevelopmental timing and socio-cognitive development in a prosocial cooperatively breeding primate (Callithrix jacchus)

Abstract

Primate, and especially human, brain development is experience-dependent: it is shaped by the inputs received during critical periods. During early development, these inputs systematically differ between independently and cooperatively breeding species, because in cooperative breeders infants are interacting from birth with multiple caretakers and have to thrive in a richer and more challenging social environment. Here, we study the neurodevelopmental timing of the cooperatively breeding common marmoset and how it maps onto behavioral and developmental milestones. To obtain meaningful correlations of structure-function co-constructions, we combine behavioral, imaging (anatomical and functional) and neural tracing experiments. We focus on brain areas that are critically involved when observing conspecifics interacting with others and find that (i) these areas develop in clusters; (ii) these areas reach their maximum gray matter volume shortly after peak provisioning, when immatures are intensely provisioned by group members; (iii) the differentiation of these areas coincides with the period of intense negotiation between immatures and multiple adults over food, the birth of the next set of siblings, and the task of becoming a helper. Moreover, like in humans, differentiation is not fully completed at the age of first reproduction. In sum, we find that the developmental timing of social brain areas coincides with key social and developmental milestones in marmosets, and extends into early adulthood. This rich social input is likely critical for the emergence of the particularly strong prosociality and socio-cognitive skills of marmosets. Since humans are cooperative breeders too, these findings have strong implications for the evolution of human social cognition.