Cross-modal activation of auditory regions during visuo-spatial working memory in early deafness

Abstract

Early deafness can reshape deprived auditory regions to enable the processing of signals from the remaining intact sensory modalities. Cross-modal activation has been observed in auditory regions during non-auditory tasks in early deaf subjects. In hearing subjects, visual working memory can evoke activation of the visual cortex, which further contributes to behavioural performance. In early deaf subjects, however, whether and how auditory regions participate in visual working memory remains unclear. We hypothesized that auditory regions may be involved in visual working memory processing and activation of auditory regions may contribute to the superior behavioural performance of early deaf subjects. In this study, 41 early deaf subjects (22 females and 19 males, age range: 20-26 years, age of onset of deafness < 2 years) and 40 age- and gender-matched hearing controls underwent functional magnetic resonance imaging during a visuo-spatial delayed recognition task that consisted of encoding, maintenance and recognition stages. The early deaf subjects exhibited faster reaction times on the spatial working memory task than did the hearing controls. Compared with hearing controls, deaf subjects exhibited increased activation in the superior temporal gyrus bilaterally during the recognition stage. This increased activation amplitude predicted faster and more accurate working memory performance in deaf subjects. Deaf subjects also had increased activation in the superior temporal gyrus bilaterally during the maintenance stage and in the right superior temporal gyrus during the encoding stage. These increased activation amplitude also predicted faster reaction times on the spatial working memory task in deaf subjects. These findings suggest that cross-modal plasticity occurs in auditory association areas in early deaf subjects. These areas are involved in visuo-spatial working memory. Furthermore, amplitudes of cross-modal activation during the maintenance stage were positively correlated with the age of onset of hearing aid use and were negatively correlated with the percentage of lifetime hearing aid use in deaf subjects. These findings suggest that earlier and longer hearing aid use may inhibit cross-modal reorganization in early deaf subjects. Granger causality analysis revealed that, compared to the hearing controls, the deaf subjects had an enhanced net causal flow from the frontal eye field to the superior temporal gyrus. These findings indicate that a top-down mechanism may better account for the cross-modal activation of auditory regions in early deaf subjects.See MacSweeney and Cardin (doi:10/1093/awv197) for a scientific commentary on this article.

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

“…This view is consistent with recent evidence that cross-modal visual recruitment of the pSTS was associated with increased functional connectivity with the calcarine cortex in the deaf although the directionality of the effect was undetermined (40). The hypothesis that the auditory cortex participates in early sensory/perceptual processing after early auditory deprivation, in contrast with previous assumptions that such recruitment manifests only for late and higher level cognitive process (41,42), also finds support in our MEG finding that a face-selective response occurs at about 196 ms in the right dTFA. The finding that at least 150 ms of information accumulation is necessary for highlevel individuation of faces in the cortex (22) suggests that the faceselective response in the right dTFA occurs immediately after the initial perceptual encoding of face identity.…”

Visual deprivation selectively reshapes the intrinsic functional architecture of the anterior insula subregions

“…The present study provided additional evidence supporting strengthened functional links between the visual stream and the salient core hubs, which may partly interpret the compensatory changes in non-visual perceptual181920232425 and cognitive performance in blind individuals262728. This inference was supported by a recent serial study by Ding et al ., who reported cross-modal activation of auditory regions during visuospatial working memory in early deafness42; moreover, strengthened functional connectivity has been shown between these reshaped auditory regions and the AI in early deafness, and the strengthened functional connectivity is significantly associated with the working memory performance43. Because the present study did not acquire the behaviour information, the direct association between the visual-AI functional coupling and the non-visual functions requires future clarification.…”

“…Several studies have indicated the plastic potential of the AI in response to sensory deprivation. For example, early deaf individuals demonstrate stronger activation of the AI during visual short-term verbal memory task4142, as well as a strengthened functional connectivity (FC) between the AI and the superior temporal sulcus, where cross-modal processing of the visual spatial working memory have been identified compared with hearing subjects43. Compared with the sighted subjects, the congenitally blind (CB) individuals demonstrate decreased regional homogeneities of the AI44.…”

Cerebral blood perfusion changes in amputees with myoelectric hands after rehabilitation: a SPECT computer-aided analysis

“…The fMRI, PET and SPECT are the most commonly used techniques to evaluate the changes [22–24]. Blood oxygen level, regional cerebral blood flow or FDG uptakes are measured by these methods and can definitively reflect changes in the underlying neuronal activity.…”