Reassessing referral of touch following peripheral deafferentation: The role of contextual bias.

Some amputees have been famously reported to perceive facial touch as arising from their phantom hand. These referred sensations have since been replicated across multiple neurological disorders and were classically interpreted as a perceptual correlate of cortical plasticity. Common to all these and related studies is that participants might have been influenced in their self-reports by the experimental design or related contextual biases. Here, we investigated whether referred sensations reports might be confounded by demand characteristics (e.g., compliance, expectation, suggestion). Unilateral upper-limb amputees (N = 18), congenital one-handers (N = 19), and two-handers (N = 22) were repeatedly stimulated with computer-controlled vibrations on 10 body-parts and asked to report the occurrence of any concurrent sensations on their hand(s). To further manipulate expectations, we gave participants the suggestion that some of these vibrations had a higher probability to evoke referred sensations. We also assessed similarity between (phantom) hand and face representation in primary somatosensory cortex (S1), using functional Magnetic Resonance Imaging (fMRI) multivariate representational similarity analysis. We replicated robust reports of referred sensations in amputees towards their phantom hand; however, the frequency and distribution of reported referred sensations were similar across groups. Moreover, referred sensations were evoked by stimulation of multiple body-parts and similarly reported on both the intact and phantom hand in amputees. Face-to-phantom-hand representational similarity was not different in amputees' missing hand region, compared with controls. These findings weaken the interpretation of referred sensations as a perceptual correlate of S1 plasticity and reveal the need to account for contextual biases when evaluating anomalous perceptual phenomena.

Complex pattern of facial remapping in somatosensory cortex following congenital but not acquired hand loss.

Cortical remapping after hand loss in the primary somatosensory cortex (S1) is thought to be predominantly dictated by cortical proximity, with adjacent body parts remapping into the deprived area. Traditionally, this remapping has been characterised by changes in the lip representation, which is assumed to be the immediate neighbour of the hand based on electrophysiological research in non-human primates. However, the orientation of facial somatotopy in humans is debated, with contrasting work reporting both an inverted and upright topography. We aimed to fill this gap in the S1 homunculus by investigating the topographic organisation of the face. Using both univariate and multivariate approaches we examined the extent of face-to-hand remapping in individuals with a congenital and acquired missing hand (hereafter one-handers and amputees, respectively), relative to two-handed controls. Participants were asked to move different facial parts (forehead, nose, lips, tongue) during functional MRI (fMRI) scanning. We first confirmed an upright face organisation in all three groups, with the upper-face and not the lips bordering the hand area. We further found little evidence for remapping of both forehead and lips in amputees, with no significant relationship to the chronicity of their phantom limb pain (PLP). In contrast, we found converging evidence for a complex pattern of face remapping in congenital one-handers across multiple facial parts, where relative to controls, the location of the cortical neighbour - the forehead - is shown to shift away from the deprived hand area, which is subsequently more activated by the lips and the tongue. Together, our findings demonstrate that the face representation in humans is highly plastic, but that this plasticity is restricted by the developmental stage of input deprivation, rather than cortical proximity.

Beyond body maps: Information content of specific body parts is distributed across the somatosensory homunculus.

The homunculus in primary somatosensory cortex (S1) is famous for its body part selectivity, but this dominant feature may eclipse other representational features, e.g., information content, also relevant for S1 organization. Using multivariate fMRI analysis, we ask whether body part information content can be identified in S1 beyond its primary region. Throughout S1, we identify significant representational dissimilarities between body parts but also subparts in distant non-primary regions (e.g., between the hand and the lips in the foot region and between different face parts in the foot region). Two movements performed by one body part (e.g., the hand) could also be dissociated well beyond its primary region (e.g., in the foot and face regions), even within Brodmann area 3b. Our results demonstrate that information content is more distributed across S1 than selectivity maps suggest. This finding reveals underlying information contents in S1 that could be harnessed for rehabilitation and brain-machine interfaces.

A neural surveyor to map touch on the body.

Perhaps the most recognizable sensory map in all of neuroscience is the somatosensory homunculus. Although it seems straightforward, this simple representation belies the complex link between an activation in a somatotopic map and the associated touch location on the body. Any isolated activation is spatially ambiguous without a neural decoder that can read its position within the entire map, but how this is computed by neural networks is unknown. We propose that the somatosensory system implements multilateration, a common computation used by surveying and global positioning systems to localize objects. Specifically, to decode touch location on the body, multilateration estimates the relative distance between the afferent input and the boundaries of a body part (e.g., the joints of a limb). We show that a simple feedforward neural network, which captures several fundamental receptive field properties of cortical somatosensory neurons, can implement a Bayes-optimal multilateral computation. Simulations demonstrated that this decoder produced a pattern of localization variability between two boundaries that was unique to multilateration. Finally, we identify this computational signature of multilateration in actual psychophysical experiments, suggesting that it is a candidate computational mechanism underlying tactile localization.

The homeostatic homunculus: rethinking deprivation-triggered reorganisation.

While amputation was considered a prominent model for cortical reorganisation, recent evidence highlights persistent representation of the missing hand. We offer a new perspective on the literature of amputation-triggered sensorimotor plasticity, by emphasising the need for homeostasis and emerging evidence of latent activity distributed across the homunculus. We argue that deprivation uncovers pre-existing latent activity, which can manifest as remapping, but that since this activity was already there, remapping could in some instances correspond to functional stability of the system rather than reorganisation. Adaptive behaviour and Hebbian-like plasticity may also play crucial roles in maintaining the functional organisation of the homunculus when deprivation occurs in adulthood or in early development. Collectively, we suggest that the brain's need for stability may underlie several key phenotypes for brain remapping, previously interpreted as consequential to reorganisation. Nevertheless, reorganisation may still be possible, especially when cortical changes contribute to the stability of the system.

Tactile learning transfer from the hand to the face but not to the forearm implies a special hand-face relationship.

In the primary somatosensory cortex, large-scale cortical and perceptual changes have been demonstrated following input deprivation. Recently, we found that the cortical and perceptual changes induced by repetitive somatosensory stimulation (RSS) at a finger transfer to the face. However, whether such cross-border changes are specific to the face remains elusive. Here, we investigated whether RSS-induced acuity changes at the finger can also transfer to the forearm, which is the body part represented on the other side of the hand representation. Our results confirmed the transfer of tactile learning from the stimulated finger to the lip, but no significant changes were observed at the forearm. A second experiment revealed that the same regions on the forearm exhibited improved tactile acuity when RSS was applied there, excluding the possibility of low plastic ability at the arm representation. This provides also the first evidence that RSS can be efficient on body parts other than the hand. These results suggest that RSS-induced tactile learning transfers preferentially from the hand to the face rather than to the forearm. This specificity could arise from a stronger functional connectivity between the cortical hand and face representations, reflecting a fundamental coupling between these body parts.

Neuromagnetic correlates of adaptive plasticity across the hand-face border in human primary somatosensory cortex.

It is well established that permanent or transient reduction of somatosensory inputs, following hand deafferentation or anesthesia, induces plastic changes across the hand-face border, supposedly responsible for some altered perceptual phenomena such as tactile sensations being referred from the face to the phantom hand. It is also known that transient increase of hand somatosensory inputs, via repetitive somatosensory stimulation (RSS) at a fingertip, induces local somatosensory discriminative improvement accompanied by cortical representational changes in the primary somatosensory cortex (SI). We recently demonstrated that RSS at the tip of the right index finger induces similar training-independent perceptual learning across the hand-face border, improving somatosensory perception at the lips (Muret D, Dinse HR, Macchione S, Urquizar C, Farnè A, Reilly KT.Curr Biol24: R736-R737, 2014). Whether neural plastic changes across the hand-face border accompany such remote and adaptive perceptual plasticity remains unknown. Here we used magnetoencephalography to investigate the electrophysiological correlates underlying RSS-induced behavioral changes across the hand-face border. The results highlight significant changes in dipole location after RSS both for the stimulated finger and for the lips. These findings reveal plastic changes that cross the hand-face border after an increase, instead of a decrease, in somatosensory inputs.