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.

Category-Selective Visual Regions Have Distinctive Signatures of Connectivity in Neonates

“…However, for both tools and places, we found no effect of the time between scan and birth ("experience age") suggesting that either there was little development in this early time period in neonates, or that there are substantial individual differences that mask age effects in across-subjects analyses, but not within-subject longitudinal studies. These results extend those from fMRI 35 and functional connectivity 12 in infants and structural connectivity in adults 14 to reveal a proto-organization of category-selective regions in the ventral visual stream. The early maturity and specificity of the structural networks is further reflected in the connections identified by the classifiers.…”

“…The fusiform face area (FFA) 4 , for example, receives stronger visual input from the fovea and lower spatial frequencies 11 , leading to the acquisition of representations that are particularly suited for processing faces. Recently, it was found that this proto-organization is present at 6-27 days, as a face-selective region had stronger functional connectivity with foveal V1 than peripheral V1; while the reverse was seen for a scene region 12 .…”

“…It could be that it reflects experience, through the statistical learning of associations. According to this model, for example, in the first stage of learning face selectivity might mature in a bottom-up way through biased input 6,11,12,24 . The auditory system might be maturing from its own proto-organization, perhaps due to selectivity to temporal modulations, to develop voice-selective regions 25 .…”

Visual object categorization in infancy

“…There is initial evidence for signatures, or precursors, of neural specialization to object categories (faces, bodies, animals and scenes), in the visual cortex of newborns or young infants, using electroencephalography [25][26][27][28] or fMRI 29,30 .…”

“…There is initial evidence for signatures, or precursors, of neural specialization to object categories (faces, bodies, animals and scenes), in the visual cortex of newborns or young infants, using electroencephalography 25–28 or fMRI 29,30 . Behavioral counterparts of those neural effects include early preference for faces or face-like stimuli over inverted faces 31–33 , for biological, over non-biological motion 34,35 , and for canonical, over distorted bodies 36–38 .…”