Elsevier

Neuroscience

Volume 387, 1 September 2018, Pages 85-91
Neuroscience

Cortical plasticity as a basis of phantom limb pain: Fact or fiction?

https://doi.org/10.1016/j.neuroscience.2017.11.015Get rights and content

Highlights

  • Sensory and motor representations of the amputated limb are differentially affected by an amputation.

  • Cortical reorganization, preserved limb function and peripheral factors interact to create phantom limb pain.

  • Contextual factors such as body representation and psychological variables need to be considered in models of phantom pain.

  • Maladaptive reorganization and preserved plasticity might go hand in hand in determining phantom limb pain.

  • Longitudinal studies are needed to determine the formation of the phantom pain experience.

Abstract

Cortical reorganization has been proposed as a major factor involved in phantom pain with prior nociceptive input to the deafferented region and input from the non-deafferented cortex creating neuronal activity that is perceived as phantom pain. There is substantial evidence that these processes play a role in neuropathic pain, although causal evidence is lacking. Recently it has been suggested that a maintenance of the cortical representation of the former hand area is related to phantom pain. Although interesting, evidence for this process is so far scarce. In addition, peripheral factors have been proposed as important for phantom limb pain. Although often introduced as contradictory, we suggest that cortical reorganization, preserved limb function and peripheral factors interact to create the various painful and nonpainful aspects of the phantom limb experience. In addition, the type of task (sensory versus motor), the interaction of injury- and use-dependent plasticity, the type of data analysis, contextual factors such as the body representation and psychological variables determine the outcome and need to be considered in models of phantom limb pain. Longitudinal studies are needed to determine the formation of the phantom pain experience.

Introduction

There is considerable evidence that phantom limb pain is related to changes in the somatotopic map in primary sensory and motor cortex, although causal evidence is lacking and it has been debated whether maladaptive cortical plasticity or preserved function of the representation of the limb contribute to pain (cf., Flor et al., 2006, Flor et al., 2013, Makin et al., 2013a, Makin et al., 2015). In this review, we present evidence for the central changes related to phantom limb pain and discuss their interaction with peripheral factors. In addition, we evaluate the role of methodological aspects of assessing cortical reorganization, type of experimental task (sensory, motor or both) and the role of body perception and use-dependent plasticity. We also address the role of psychological factors and how they relate to phantom pain. A better understanding of how these factors interact could help to understand differences between studies and could advance the analysis of mechanisms of phantom limb pain. Finally, we review some training interventions for phantom limb pain, aiming at inducing changes in the perception of the phantom limb and we discuss their contribution to our current understanding of phantom pain.

Section snippets

Perspectives on the neural basis of phantom limb pain

Neural plasticity is generally viewed as an adaptive learning process enabling the cortex to redistribute computational resources to focus on brain regions containing behaviorally relevant information. For example, the cortical representation of the ventral body surface is expanded in nursing rats (Xerri et al., 1994). Map expansions also occur in humans following extensive sensory and sensorimotor training (e.g., Merzenich et al., 1990, Recanzone et al., 1992, Elbert et al., 1995, Molina-Luna

Context matters

It is important to emphasize conceptual differences across studies in assessing cortical reorganization following amputation. While some studies used various types of phantom movements (imagined, executed, or a combination), other studies used innocuous stimulation at body sites represented adjacent to the former hand area, movement of adjacent body parts such as the mouth or illusory movement, such as that related to mirrored movements.

For example, in a functional magnetic resonance imaging

Cortical plasticity and phantom limb pain: clinical implications

Several lines of evidence based on models of plasticity in the “affected” sensorimotor cortex suggest that reorganization processes occurring after amputation are reversible, offering potential for therapy. For instance, a recent study aimed to relieve phantom pain in brachial plexus avulsion patients by restoring functional integrity of the phantom limb representation in the sensorimotor cortex using a brain machine interface and real-time magnetoencephalography (MEG) (Yanagisawa et al., 2016

Conclusion

Different models have been proposed to explain the neural basis of phantom pain. We propose that topographic shifts and preserved representations are not necessarily mutually exclusive; however, clear causal evidence in support of either model of the neural basis of phantom pain is still lacking. Furthermore, the role of peripheral changes in the maintenance of phantom pain needs to be clarified also in light of computational models that suggest that central and peripheral changes are

Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft (SFB1158/B07) awarded to H.F. and J.A. and an Advanced Grant (230249) from the European Research Council awarded to H.F. The authors declare no conflict of interest.

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