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

Abstract

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.

Keywords: development; fMRI; fusiform face area; neonates; parahippocampal place area.

Fig. 1.

ROIs of interest in three example neonates (Left) and three example adults (Right). OFA, light blue; FFA, dark blue; PPA, red; RSC, pink; V1, green. Note that V1 was split into three equal portions from posterior to anterior, as distinguished by alternating patterns of green and light green.

Fig. 2.

Domain-specific functional connectivity in neonates and adults. (A) Both neonates (n = 30) and adults (n = 15) show greater functional connectivity within domains (i.e., OFA-FFA and PPA-RSC) than between domains (i.e., any pair of a face and a scene region). (B) Functional connectivity between every possible pair of regions in both neonates and adults. (C) Greater functional connectivity within domains than between domains is found even in the between-hemisphere data, ensuring that effects are not driven by local spread of the fMRI signal. Furthermore, domain-specific functional connectivity is not found in noise data designed to simulate distance effects (Methods). Error bars indicate SEM.

Fig. 3.

Eccentricity-biased functional connectivity in neonates and adults. (A) Both neonates (n = 30) and adults (n = 15) show greater functional connectivity within eccentricity (i.e., face regions to foveal V1 and scene regions to peripheral V1) than between eccentricity (i.e., face regions to peripheral V1 or scene regions to foveal V1). Eccentricity-biased functional connectivity is not found in noise data designed to simulate distance effects (Methods). (B) Functional connectivity between each face (OFA and FFA) and place (PPA and RSC) region and the three portions of V1, representing foveal (“fov”), middle (“mid”), and peripheral (“per”) V1. (C) Greater functional connectivity within eccentricity than between eccentricity is found even in the between-hemisphere data, ensuring that effects are not driven by local spread of the fMRI signal. Furthermore, domain-specific functional connectivity is not found in noise data designed to simulate distance effects (Methods). Error bars indicate SEM.