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Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation

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  • Ref Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation

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    Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation
    Tamar R. Makin, Jan Scholz, David Henderson Slater, Heidi Johansen-Berg, Irene Tracey

    Brain (2015)

    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.

    Introduction

    Brain reorganization is a key mechanism that enables adjustment to novel situations and injuries, but it had also been suggested to have maladaptive consequences (Flor et al., 2006). Amputation is a striking driver of plasticity, as it induces both sensory deprivation and altered behaviour. In monkeys, arm deafferentation drives massive cortical reorganization in the primary somatosensory cortex (SI), where the lower face representation takes over the cortical territory of the missing hand (Pons et al., 1991; Jain et al., 2008) (see Devor and Wall, 1978; Florence and Kaas, 1995; Kambi et al., 2014 for reorganization in subcortical structures). In humans, remapping of lower face representation was shown to correlate with phantom limb pain (Flor et al., 1995; Lotze et al., 2001; Foell et al., 2013). Subsequently, SI reorganization is increasingly assumed to play a key role in other syndromes of chronic pain (Maihöfner et al., 2003; Nava and Röder, 2011; Gustin et al., 2012), with important potential implications for designing clinical treatments (Moseley and Flor, 2012).

    We recently reported that activity levels in the missing hands’ territory of amputees is not increased during lip movements (Makin et al., 2013b). Instead, we found that phantom pain is associated with maintained structure and function during phantom hand movements. Nevertheless, this approach was not suitable for studying reorganization along the sensorimotor homunculus outside the missing hand territory. Sensorimotor reorganization in humans is typically measured as the Euclidian distance between the centre of gravity (CoG), or peak, in activity associated with facial touch (Flor et al., 1995), or more recently lip movements (Lotze et al., 2001; Foell et al., 2013), and an ‘anchor’ (e.g. the mirror projection of the intact hand representation; Flor et al., 1995). However, these measurements are taken across a folded cortical volume, and therefore do not respect anatomical barriers (e.g. white matter), or take into account the unique cortical morphology of individuals. As such, the physiological relevance of these measurements for cortical reorganization is potentially limited.

    Here, we assessed remapping of sensorimotor lip representations using an unfolded model of the cortex, allowing us to measure surface-based cortical distances while considering individual cortical folding patterns (Maeda et al., 2014) in 17 unilateral upper limb amputees and 21 intact controls. We found consistent shifts in lip representation along the homunculus contralateral to the missing hand in amputees (hereafter ‘deprived homunculus’) towards the hand area. However, this shift didn’t reflect full invasion of the lips into the hand territory as previously described, but rather a small local shift in the centre of gravity of the lips. This remapping was statistically independent of phantom pain ratings.


    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.
    Marcel

    "Evolution is a tinkerer not an engineer" F.Jacob
    "Without imperfection neither you nor I would exist" Stephen Hawking
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