Visual experience shapes the neural networks remapping touch into external space

Abstract

Localizing touch relies on the activation of skin-based and externally defined spatial frames of references. Psychophysical studies have demonstrated that early visual deprivation prevents the automatic remapping of touch into external space. We used fMRI to characterize how visual experience impacts on the brain circuits dedicated to the spatial processing of touch. Sighted and congenitally blind humans (male and female) performed a tactile temporal order judgment (TOJ) task, either with the hands uncrossed or crossed over the body midline. Behavioral data confirmed that crossing the hands has a detrimental effect on TOJ judgments in sighted but not in blind. Crucially, the crossed hand posture elicited more activity in a fronto-parietal network in the sighted group only. Psychophysiological interaction analysis revealed that the congenitally blind showed enhanced functional connectivity between parietal and frontal regions in the crossed versus uncrossed hand postures. Our results demonstrate that visual experience scaffolds the neural implementation of touch perception.Significance statementAlthough we seamlessly localize tactile events in our daily life, it is not a trivial operation because the hands move constantly within the peripersonal space. To process touch correctly, the brain has therefore to take the current position of the limbs into account and remap them to their location in the external world. In sighted, parietal and premotor areas support this process. However, while visual experience has been suggested to support the implementation of the automatic external remapping of touch, no studies so far have investigated how early visual deprivation alters the brain network supporting touch localization. Examining this question is therefore crucial to conclusively determine the intrinsic role vision plays in scaffolding the neural implementation of touch perception.

No Evidence for an Effect of the Distance Between the Hands on Tactile Temporal Order Judgments

“…Previous experiments reported decreased performances in judging the order of appearance of two tactile stimuli when the hands are positioned close together when compared with when they are placed farther away, as indexed by higher JND values in the close posture (Gallace & Spence, 2005; Roberts et al., 2003; Shore et al., 2005). These studies confirm that spatial processing of somatosensory inputs integrates information about the relative posture of the body limbs in external space, in line with the results from the studies having tested tactile TOJ performance with the hands in a crossed posture (e.g., Crollen, Lazzouni, et al., 2017; Crollen et al., 2019; Heed & Azañón, 2014; Röder et al., 2004; Shore et al., 2002; Yamamoto & Kitazawa, 2001). It was also suggested that these effects might be mostly driven by the actual vision of the limbs position (Cadieux & Shore, 2013; Gallace & Spence, 2005).…”

“…The ability to code somatosensory (tactile or nociceptive) information according to spatiotopic reference has been assessed, among others, using temporal order judgment (TOJ) tasks (Badde et al., 2014, 2015; Crollen, Albouy, et al., 2017; Crollen, Lazzouni, et al., 2017; Crollen et al., 2019; De Paepe et al., 2015; Heed & Azañón, 2014; Röder et al., 2004; Sambo et al., 2013; Shore et al., 2002; Vanderclausen, Bourgois, et al., 2020; Vanderclausen, Manfron, et al., 2020; Yamamoto & Kitazawa, 2001). In these tasks, participants judge the temporal order of two successive somatosensory stimuli, one applied to each hand, separated by different temporal delays.…”

General Enhancement of Spatial Hearing in Congenitally Blind People

“…Second, spatial-bisection tasks require a metric representation of external space (Vercillo et al, 2018). Indeed, early-blind people have qualitative alterations in their perception of external space (Crollen et al, 2017), which may explain their specific difficulties in resolving spatial-bisection tasks independently of their intrinsic spatial-hearing abilities (Collignon et al, 2009). Supporting this view, one recent study found that severe deficits of early-blind participants in localizing brief auditory stimuli with respect to external acoustic landmarks (using a spatial-bisection task) were simply alleviated when participants had to localize the exact same sounds with respect to their own hand (using a body-centered reference frame; Vercillo et al, 2018).…”

Dynamic spatial coding in parietal cortex mediates tactile-motor transformation

“…However, it is inconsistent with the widely held idea that each hemisphere of PPC represents mainly the contralateral side of space, and findings that both putative human LIP and hVIP#1 are bilateral regions 21,32,47,71,73 . FMRI responses related to tactile remapping in PPC were stronger in the right hemisphere in one study 87 , but in the left hemisphere in another study 88 . TMS studies on tactile remapping have often targeted only the right hemisphere, making it unclear whether their findings would generalize to the left hemisphere 12,13,84 , however one study that stimulated both the left and right hemisphere found similar effects for both hemispheres 14 .…”