Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation

Abstract

The role of cortical activity in generating and abolishing chronic pain is increasingly emphasized in the clinical community. Perhaps the most striking example of this is the maladaptive plasticity theory, according to which phantom pain arises from remapping of cortically neighbouring representations (lower face) into the territory of the missing hand following amputation. This theory has been extended to a wide range of chronic pain conditions, such as complex regional pain syndrome. Yet, despite its growing popularity, the evidence to support the maladaptive plasticity theory is largely based on correlations between pain ratings and oftentimes crude measurements of cortical reorganization, with little consideration of potential contributions of other clinical factors, such as adaptive behaviour, in driving the identified brain plasticity. Here, we used a physiologically meaningful measurement of cortical reorganization to reassess its relationship to phantom pain in upper limb amputees. We identified small yet consistent shifts in lip representation contralateral to the missing hand towards, but not invading, the hand area. However, we were unable to identify any statistical relationship between cortical reorganization and phantom sensations or pain either with this measurement or with the traditional Euclidian distance measurement. Instead, we demonstrate that other factors may contribute to the observed remapping. Further research that reassesses more broadly the relationship between cortical reorganization and chronic pain is warranted.

Keywords: amputees; functional MRI; pain; phantom pain; plasticity.

The brain’s ability to reorganise itself is key to our recovery from injuries, but the subsequent mismatch between old and new organisation may lead to pain. Makin et al. argue against this ‘maladaptive plasticity’ theory by showing that phantom pain in upper limb amputees is independent of cortical remapping.

Figure 1

Shifted lip representation in amputees. (A) An illustration of the human sensorimotor homunculus, projected on a cortical surface map. Coloured contours delineate the boundaries of clusters activated during execution of movements using the feet (green), arms (blue), hands (white), and lips (pink) in controls. The hand representation is located approximately half way between the feet (medial) and lips (lateral). The yellow line indicates the central sulcus. The image was adapted from Makin et al. (2013a). (B and C) CoG of surface-based lip (B) and feet (C) representation for amputees (red) and controls (purple) in the central sulcus contralateral to the missing (amputees) or non-dominant hand (controls), projected on an averaged brain. While the amputees’ lip representations showed a medial displacement compared with the controls, the feet representation was largely overlapping (D) means (± SEM) of amputees (red) and controls (purple) lip-to-feet distance for each hemisphere, using the surface-based approaches (top) and the traditional (Euclidian distance in the folded brain, bottom). The dotted line shows the position of the hand (in the controls’ non-dominant hemisphere) along the homunculus. The surface-based approach showed a clear cortical shift in the lip representation along the deprived homunculus in amputees. However, note that the lip representation did not invade the hand area. Significance of planned comparisons (two-tailed t-tests) are denoted as follows: *P < 0.05; **P < 0.01. n.s. = non-significant (P > 0.05).