Functional selectivity for face processing in the temporal voice area of early deaf individuals

Abstract

Brain systems supporting face and voice processing both contribute to the extraction of important information for social interaction (e.g., person identity). How does the brain reorganize when one of these channels is absent? Here, we explore this question by combining behavioral and multimodal neuroimaging measures (magnetoencephalography and functional imaging) in a group of early deaf humans. We show enhanced selective neural response for faces and for individual face coding in a specific region of the auditory cortex that is typically specialized for voice perception in hearing individuals. In this region, selectivity to face signals emerges early in the visual processing hierarchy, shortly after typical face-selective responses in the ventral visual pathway. Functional and effective connectivity analyses suggest reorganization in long-range connections from early visual areas to the face-selective temporal area in individuals with early and profound deafness. Altogether, these observations demonstrate that regions that typically specialize for voice processing in the hearing brain preferentially reorganize for face processing in borndeaf people. Our results support the idea that cross-modal plasticity in the case of early sensory deprivation relates to the original functional specialization of the reorganized brain regions.cross-modal plasticity | deafness | modularity | ventral stream | identity processing T he human brain is endowed with the fundamental ability to adapt its neural circuits in response to experience. Sensory deprivation has long been championed as a model to test how experience interacts with intrinsic constraints to shape functional brain organization. In particular, decades of neuroscientific research have gathered compelling evidence that blindness and deafness are associated with cross-modal recruitment of the sensory-deprived cortices (1). For instance, in early deaf individuals, visual and tactile stimuli induce responses in regions of the cerebral cortex that are sensitive primarily to sounds in the typical hearing brain (2, 3).Animal models of congenital and early deafness suggest that specific visual functions are relocated to discrete regions of the reorganized cortex and that this functional preference in crossmodal recruitment supports superior visual performance. For instance, superior visual motion detection is selectively altered in deaf cats when a portion of the dorsal auditory cortex, specialized for auditory motion processing in the hearing cat, is transiently deactivated (4). These results suggest that cross-modal plasticity associated with early auditory deprivation follows organizational principles that maintain the functional specialization of the colonized brain regions. In humans, however, there is only limited evidence that specific nonauditory inputs are differentially localized to discrete portions of the auditory-deprived cortices. For example, Bola et al. have recently reported, in deaf individuals, cross-modal activations for visual rhythm discrimination in t...

White matter connectivity between occipital and temporal regions involved in face and voice processing in hearing and early deaf individuals.

“…Early integration between facial and vocal information during the processing of speech may be supported by these direct connections between occipital and temporal regions (van connections as disclosed in our study. The high probability of detecting direct structural connectivity between V2/3 and TVA in the right hemisphere fits well with our previous observation of significant effective connectivity between these regions during face processing in deaf individuals, supporting our hypothesis that this heteromodal connection might be primarily involved in visual cross-modal reorganization of the deaf TVA (Benetti et al 2017).…”

White matter connectivity between occipital and temporal regions involved in face and voice processing in hearing and early deaf individuals

“…For instance, Lomber and colleagues have reported that, in deaf cats, superior visual motion detection is selectively impaired if a specific region in the dorsal auditory cortex, which processes auditory motion in hearing cats, is transiently suppressed (Lomber et al 2010). In deaf humans, supporting evidence has recently been provided by a study showing rhythm-specific visual activations in posterior-lateral and associative auditory regions (Bola et al 2017) and, further, by our observation of preferential responses to faces and face discrimination in the human temporal voice sensitive area (TVA) as a consequence of early auditory deprivation (Benetti et al 2017).…”

Stimulus arousal drives amygdalar responses to emotional expressions across sensory modalities

“…A recent study by Lin and colleagues (2016) 5 showed that stimulus arousal strongly impacts activation of the posterior STS in response to facial expressions. Several researchers proposed that the posterior STS is involved in the representation of facial information, particularly the representation of emotional expressions 67,68 , and demonstrated coupling with other face processing areas such as the fusiform gyrus 69,70 . Moreover, parts of the STS have been suggested to be the vocal analogue of the fusiform face processing area 9,71,72 , representing vocal features of varying complexity dependent on their emotional significance 8,9,71,73 .…”