Connectivity at the origins of domain specificity in the cortical face and place networks

Bibliographic Collection: 
Publication Type: Journal Article
Authors: Kamps, Frederik S.; Hendrix, Cassandra L.; Brennan, Patricia A.; Dilks, Daniel D.
Year of Publication: 2020
Journal: Proceedings of the National Academy of Sciences
Pagination: 201911359
Date Published: 2020/02/26
Publication Language: eng

Where does knowledge come from? We addressed this classic question using the test cases of the cortical face and scene networks: two well-studied examples of specialized “knowledge” systems in the adult brain. We found that neonates already show domain-specific patterns of functional connectivity between regions that will later develop full-blown face and scene selectivity. Furthermore, the proto face network showed stronger functional connectivity with foveal than with peripheral primary visual cortex, while the proto scene network showed the opposite pattern, revealing that these networks already receive differential visual inputs. Our findings support the hypothesis that innate connectivity precedes the emergence of domain-specific function in cortex, shedding new light on the age-old question of the origins of human knowledge.It is well established that the adult brain contains a mosaic of domain-specific networks. But how do these domain-specific networks develop? Here we tested the hypothesis that the brain comes prewired with connections that precede the development of domain-specific function. Using resting-state fMRI in the youngest sample of newborn humans tested to date, we indeed found that cortical networks that will later develop strong face selectivity (including the “proto” occipital face area and fusiform face area) and scene selectivity (including the “proto” parahippocampal place area and retrosplenial complex) by adulthood, already show domain-specific patterns of functional connectivity as early as 27 d of age (beginning as early as 6 d of age). Furthermore, we asked how these networks are functionally connected to early visual cortex and found that the proto face network shows biased functional connectivity with foveal V1, while the proto scene network shows biased functional connectivity with peripheral V1. Given that faces are almost always experienced at the fovea, while scenes always extend across the entire periphery, these differential inputs may serve to facilitate domain-specific processing in each network after that function develops, or even guide the development of domain-specific function in each network in the first place. Taken together, these findings reveal domain-specific and eccentricity-biased connectivity in the earliest days of life, placing new constraints on our understanding of the origins of domain-specific cortical networks.

Short Title: Proc Natl Acad Sci USA