Reassessing referred sensations following peripheral deafferentation and the role of cortical reorganisation

Background and ObjectivesTactile sensations referred to body parts other than those stimulated have been repeatedly described across a wide range of deafferentation and neuropathic pain conditions, including amputation, complex regional pain syndrome, spinal cord injury, and brachial plexus avulsion. Common to all interpretations of referred sensations is the notion that they result from central nervous system (CNS) reorganisation. For example, in amputees, sensations referred to the phantom limb following touches on the face have been classically interpreted as the perceptual correlate of cortical remapping of the face into the neighbouring missing-hand territory in primary somatosensory cortex (S1). Here, using the prominent model of acquired upper-limb amputation, we investigated whether referred sensations reports are associated with cortical remapping or can instead be attributed to demand characteristics (e.g., compliance, expectation, and suggestion), which have been shown to greatly influence self-reports of bodily sensations and were uncontrolled in previous assessments. MethodsUnilateral upper-limb amputees (N=18), congenital one-handers (N=19), and two-handers (N=20) were repeatedly stimulated with PC-controlled vibrations on ten body-parts and asked to report on each trial 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. To evaluate remapping, we analysed fMRI data in S1 from two tasks involving movement of facial and whole-body parts, using univariate and multivariate approaches. ResultsThe frequency and distribution of reported referred sensations were similar across groups, with higher frequencies in the high expectancy condition. In amputees, referred sensations were evoked by stimulation of multiple body-parts and reported in both the intact and phantom hand. The group profiles for referred sensations reports were not consistent with the observed patterns of S1 remapping. DiscussionThese findings weaken the interpretation of referred sensations as a perceptual consequence of post-deafferentation CNS reorganisation and reveal the need to account for demand characteristics when evaluating self-reports of anomalous perceptual phenomena for both research and clinical assessments purposes.