Cortical network differences in the sighted versus early blind for recognition of human‐produced action sounds

Abstract

Both sighted and blind individuals can readily interpret meaning behind everyday real-world sounds. In sighted listeners, we previously reported that regions along the bilateral posterior superior temporal sulci (pSTS) and middle temporal gyri (pMTG) are preferentially activated when presented with recognizable action sounds. These regions have generally been hypothesized to represent primary loci for complex motion processing, including visual biological motion processing and audio-visual integration. However, it remained unclear whether, or to what degree, life-long visual experience might impact functions related to hearing perception or memory of sound-source actions. Using functional magnetic resonance imaging (fMRI), we compared brain regions activated in congenitally blind versus sighted listeners in response to hearing a wide range of recognizable human-produced action sounds (excluding vocalizations) versus unrecognized, backward-played versions of those sounds. Here we show that recognized human action sounds commonly evoked activity in both groups along most of the left pSTS/pMTG complex, though with relatively greater activity in the right pSTS/pMTG by the blind group. These results indicate that portions of the postero-lateral temporal cortices contain domain-specific hubs for biological and/or complex motion processing independent of sensory-modality experience. Contrasting the two groups, the sighted listeners preferentially activated bilateral parietal plus medial and lateral frontal networks, while the blind listeners preferentially activated left anterior insula plus bilateral anterior calcarine and medial occipital regions, including what would otherwise have been visual-related cortex. These global-level network differences suggest that blind and sighted listeners may preferentially use different memory retrieval strategies when attempting to recognize action sounds.

Making Sense of the Chemical Senses

“…These findings contrast sharply with corresponding imaging studies on olfaction ( Fig. 3A; Kupers et al,201 lb), audition (Gougoux et al, 2009;Lewis et al, 2011) and touch (Amedi et al, 2010;Ptito et al, 2005), all of which have highlighted the recruitment of the deprived visual cortex of the blind in processing informa tion arising from another modality. This can be excluded for the case for taste since blind people do not manifest superior tasting abilities, and do not recruit their visual cortex in response to tastants.…”

“…So far, only one imaging study has investigated the neural correlates of (orthonasal) olfactory processing in blindness (Kupers et al, 2011b), and data on retronasal olfaction are currently missing. Simi larly to cases of audition (Gougoux et al, 2009;Lewis et al, 2011) and touch (Amedi et al, 2010), orthonasal olfactory processing recruits more strongly the occipital cortex in the blind, compared to blindfolded sighted participants ( Fig. 3A; Kupers et al, 2011b).…”

Autism, social cognition and superior temporal sulcus

“…For example, Bidet-Caulet and colleagues reported activity in the STS as participants heard footsteps. Other studies have shown greater STS activity associated with hearing of human actions, such as yawning or chewing, compared to hearing other environmental or mechanical actions [52].…”

Auditory object perception: A neurobiological model and prospective review

“…From the perspective of grounded cognition theories, a couple studies sought to assess whether a cortical organization respecting a living versus non-living boundary would hold true of real-world sounds (Engel et al, 2009; Lewis et al, 2011b). However, because vocalizations are acoustically characterized and distinguished by strong harmonic content, to facilitate data interpretation (addressed in Section 2.1) the sound stimuli used were restricted to those devoid of any vocal content.…”

“…However, individuals who have never had visual experience (early blind listeners) are clearly fully capable of recognizing and identifying action sounds. Examining brain responses of congenitally blind listeners (Lewis et al, 2011b), human action sounds deemed as recognized, in contrast to backward played version that were not recognized, also recruited the pSTS/pMTG complex in addition to portions of occipital cortices associated with visual processing (Fig. 3, yellow outlines).…”