Individual variation in the functional lateralization of human ventral temporal cortex: Local competition and long-range coupling

Abstract

AbstractThe ventral temporal cortex (VTC) of the human cerebrum is critically engaged in high-level vision. One intriguing aspect of this region is its functional lateralization, with neural responses to words being stronger in the left hemisphere, and neural responses to faces being stronger in the right hemisphere; such patterns can be summarized with a signed laterality index (LI), positive for leftward laterality. Converging evidence has suggested that word laterality emerges to couple efficiently with left-lateralized frontotemporal language regions, but evidence is more mixed regarding the sources of the right-lateralization for face perception. Here, we use individual differences as a tool to test three theories of VTC organization arising from: 1) local competition between words and faces driven by long-range coupling between words and language processes, 2) local competition between faces and other categories, 3) long-range coupling with VTC and temporal areas exhibiting local competition between language and social processing. First, in an in-house functional MRI experiment, we did not obtain a negative correlation in the LIs of word and face selectivity relative to object responses, but did find a positive correlation when using selectivity relative to a fixation baseline, challenging ideas of local competition between words and faces driving rightward face lateralization. We next examined broader local LI interactions with faces using the large-scale Human Connectome Project (HCP) dataset. Face and tool LIs were significantly anti-correlated, while face and body LIs were positively correlated, consistent with the idea that generic local representational competition and cooperation may shape face lateralization. Last, we assessed the role of long-range coupling in the development of VTC lateralization. Within our in-house experiment, substantial positive correlation was evident between VTC text LI and that of several other nodes of a distributed text-processing circuit. In the HCP data, VTC face LI was both negatively correlated with language LI and positively correlated with social processing in different subregions of the posterior temporal lobe (PSL and STSp, respectively). In summary, we find no evidence of local face-word competition in VTC; instead, more generic local interactions shape multiple lateralities within VTC, including face laterality. Moreover, face laterality is also influenced by long-range coupling with social processing in the posterior temporal lobe, where social processing may become right-lateralized due to local competition with language.