Impaired body-centred sensorimotor transformations in congenitally deaf people

Abstract

Congenital deafness modifies an individual’s daily interaction with the environment and alters the fundamental perception of the external world. How congenital deafness shapes the interface between the internal and external worlds remains poorly understood. To interact efficiently with the external world, visuospatial representations of external target objects need to be effectively transformed into sensorimotor representations with reference to the body. Here, we tested the hypothesis that egocentric body-centered sensorimotor transformation is impaired in congenital deafness. Consistent with this hypothesis, we found that congenital deafness induced impairments in egocentric judgments needed to associate the external objects with the internal body. These impairments were due to deficient body-centered sensorimotor transformation per se, rather than the reduced fidelity of the visuospatial representations of the egocentric positions. At the neural level, we first replicated the previously well-documented critical involvement of the fronto-parietal network in egocentric processing, in both congenitally deaf participants and hearing controls. However, both the strength of neural activity and the intra-network connectivity within the fronto-parietal network alone could not account for egocentric performance variance. Instead, the inter-network connectivity between the task-positive fronto-parietal network and the task-negative default-mode network was significantly correlated with egocentric performance: the more cross-talking between them, the worse the egocentric judgment. Accordingly, the impaired egocentric performance in the deaf group was related to increased inter-network connectivity between the fronto-parietal network and the default-mode network and decreased intra-network connectivity within the default-mode network. The altered neural network dynamics in congenital deafness were observed for both evoked neural activity during egocentric processing and intrinsic neural activity during rest. Our findings thus not only demonstrate the optimal network configurations between the task-positive and -negative neural networks underlying coherent body-centered sensorimotor transformations but also unravel a critical cause (i.e., impaired body-centered sensorimotor transformation) of a variety of hitherto unexplained difficulties in sensory-guided movements the deaf population experiences in their daily life.

Crossmodal reorganization in deaf auditory cortices compensates for the impaired body-centered visuomotor transformation after early deafness

“…All participants had a normal or corrected-to-normal vision, no color vision impairment, and no psychiatric or neurological diseases. More information about both groups was provided in our previous study (Li et al, 2022). Each participant had signed informed consent following the Helsinki Declaration before the experiment and got paid afterward.…”

“…Previous evidence consistently shows that the egocentric reference frame is impaired after early auditory deprivation (Zhang et al, 2014), associated with a hyper-crosstalk between the FPN and the default-mode network (DMN) during body-centered egocentric judgments in the deaf brain (Li et al, 2022). The DMN is generally deactivated during various externally directed tasks to suppress task-irrelevant distractions and achieve successful task performance (Anticevic et al, 2012).…”

“…Accordingly, the increased connectivity between the task-critical neural network and the DMN impairs task performance (Weisz et al, 2014;Sadaghiani et al, 2015;Li et al, 2022).…”

“…If the cross-modal reorganization in the deaf STG compensates for the impaired visuomotor transformation after early deafness, we predict that: (1) the deaf STG should show enhanced between-module connectivity with the task-critical DAN and FPN, specifically during the egocentric task, compared to the hearing controls; and more importantly (2) the potentially enhanced STG-frontoparietal connectivity should be associated with improved egocentric performance in the deaf people. Moreover, suppose the deaf STG is reorganized to functionally resemble the frontoparietal regions underlying the egocentric task since the impaired visuomotor transformation after early deafness is associated with abnormal hyper-connectivity between the task-critical frontoparietal regions and the DMN (Li et al, 2022). In that case, the deaf STG should also show increased connectivity with the DMN.…”

“…At the neural level, the dorsal attention network (DAN) is commonly involved in coding the general visuospatial representations underlying both the egocentric and allocentric reference frames (Committeri et al, 2004; Chen et al, 2012, 2014; Gomez et al, 2014), while the frontoparietal network (FPN) is specifically involved in body-centered visuomotor transformation during the egocentric task (Galati et al, 2000; Neggers et al, 2006; Chen et al, 2012, 2014). Previous evidence consistently shows that the egocentric reference frame is impaired after early auditory deprivation (Zhang et al, 2014), associated with a hyper-crosstalk between the FPN and the default-mode network (DMN) during body-centered egocentric judgments in the deaf brain (Li et al, 2022). The DMN is generally deactivated during various externally directed tasks to suppress task-irrelevant distractions and achieve successful task performance (Anticevic et al, 2012).…”