Abstract
The human brain contains multiple hand-selective areas, in both the sensorimotor and visual systems. Could our brain repurpose neural resources, originally developed for supporting hand function, to represent and control artificial limbs? We studied individuals with congenital or acquired hand-loss (hereafter one-handers) using functional MRI. We show that the more one-handers use an artificial limb (prosthesis) in their everyday life, the stronger visual hand-selective areas in the lateral occipitotemporal cortex respond to prosthesis images. This was found even when one-handers were presented with images of active prostheses that share the functionality of the hand but not necessarily its visual features (e.g. a 'hook' prosthesis). Further, we show that daily prosthesis usage determines large-scale inter-network communication across hand-selective areas. This was demonstrated by increased resting state functional connectivity between visual and sensorimotor hand-selective areas, proportional to the intensiveness of everyday prosthesis usage. Further analysis revealed a 3-fold coupling between prosthesis activity, visuomotor connectivity and usage, suggesting a possible role for the motor system in shaping use-dependent representation in visual hand-selective areas, and/or vice versa. Moreover, able-bodied control participants who routinely observe prosthesis usage (albeit less intensively than the prosthesis users) showed significantly weaker associations between degree of prosthesis observation and visual cortex activity or connectivity. Together, our findings suggest that altered daily motor behaviour facilitates prosthesis-related visual processing and shapes communication across hand-selective areas. This neurophysiological substrate for prosthesis embodiment may inspire rehabilitation approaches to improve usage of existing substitutionary devices and aid implementation of future assistive and augmentative technologies.
Highlights
Our hands are the primary tool of the brain, and the loss of a hand leads to profound changes in individuals’ abilities to interact with their environment (Makin et al, 2013a; Hahamy et al, 2017)
Activity tended to be stronger for the cosmetic prostheses compared to active prostheses [F(1,106) = 3.5, P = 0.066], the interaction term was not significant [F(1,106) = 0.4, P = 0.538], indicating that this trend is likely driven by the visual features of the cosmetic prosthesis, which strongly resembles a hand
We show that prosthetic limbs, used to substitute the missing hand, can recruit brain resources normally devoted for body representation
Summary
Our hands are the primary tool of the brain, and the loss of a hand leads to profound changes in individuals’ abilities to interact with their environment (Makin et al, 2013a; Hahamy et al, 2017). It has recently been suggested that the profound reorganization observed following hand loss possibly occurs to accommodate changes in individuals’ abilities to interact with their environment in daily life (Makin et al, 2013a; Hahamy et al, 2015, 2017). A key strategy for adapting to hand loss is using an artificial limb (hereafter ‘prosthesis’). Prosthesis usage strongly depends on both motor control and visual information, considering the limited somatosensory inputs from the artificial limb
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