The brain dynamics of congenitally blind people seeing faces with sound

Abstract

Sensory substitution devices (SSDs) convert images to sounds to equip blind individuals with nominally visual functions, like face or letter sensitivity. Prior studies showed that image-to-sound SSDs engage cortices ordinarily specialised for visual functions. However, the brain dynamics of SSD-supported perception remains unknown. Either visual cortices are the first locus of discrimination of SSD percepts, or their activation is a byproduct of perceptual processes unfurling elsewhere, such as in auditory cortices. Resolving this uncertainty is critical for understanding the contribution of visual cortices to mechanisms subserving SSD-induced perceptions in the blind. Using electrical neuroimaging of EEG data from congenitally blind adults, we show for the first time that visual cortices are the earliest site of face and letter sensitivity when conveyed via SSDs, though with distinct temporal dynamics and spatial localizations. In the case of faces versus scrambled faces, differences first manifested at 460ms post-stimulus onset as topographic EEG modulations that were in turn localized to a network of right-hemisphere regions, including the fusiform face area (FFA) as well as lateral occipital cortices. In the case of discerning vertically versus horizontally oriented letter shapes, differences first manifested at 370ms post-stimulus onset as topographic EEG modulations that were localized to a network of left-hemisphere regions, including the occipital pole and the occipito-temporal junction extending into the angular gyrus. Notably, early-latency auditory evoked potentials did not differ based on visual properties of the soundscapes. These collective data support the proposition that responses to soundscapes are routed to brain circuits ordinarily specialized for processing visual information and that these circuits are the loci of the initial discriminant processes. By providing the temporal dynamics of SSD perception, our findings provide unique evidence for the theory that cortices are characterised by task-contingent functional organisation. HighlightsO_LISensory substitution devices (SSDs) provide the blind access to visual information C_LIO_LIBrain dynamics in visual cortices to SSD-conveyed object images are unknown C_LIO_LIEarly EEG sensitivity for faces and letters was localized to the visual cortex C_LIO_LIThe blind visual cortex takes part in early SSD processing for visual categories C_LI eTOC blurbWe characterise for the first time the brain dynamics of the blind using soundscapes for face and letter discrimination. Faces recruited the FFA at 460ms post-stimulus onset, whereas letters recruited the occipital pole, occipito-temporal junction, and angular gyrus at 370ms post-stimulus onset. Our findings of the temporal dynamics of SSD perception uniquely support the theory that cortices are characterised by task-selective sensory-independent functional organisation.