Academic journal article Cognitive, Affective and Behavioral Neuroscience

Enhanced Corticospinal Response to Observed Pain in Pain Synesthetes

Academic journal article Cognitive, Affective and Behavioral Neuroscience

Enhanced Corticospinal Response to Observed Pain in Pain Synesthetes

Article excerpt

Published online: 27 December 2011

© Psychonomic Society, Inc. 2011

Abstract Observing noxious injury to another's hand is known to induce corticospinal inhibition that can be measured in the observer's corresponding muscle. Here, we investigated whether acquired pain synesthetes, individuals who experience actual pain when observing injury to another, demonstrate less corticospinal inhibition than do controls during pain observation, as a potential mechanism for the experience of vicarious pain. We recorded motor-evoked potentials (MEPs) induced at two time points through transcranial magnetic stimulation while participants observed videos of a hand at rest, a hypodermic needle penetrating the skin, a Q-tip touching the skin, and a hypodermic needle penetrating an apple. We compared MEPs in three groups: 7 amputees who experience pain synesthesia, 11 nonsynesthete amputees who experience phantom limb pain, and 10 healthy controls. Results indicated that the pain synesthete group demonstrated significantly enhanced MEP response to the needle penetrating the hand, relative to the needle not having yet penetrated the hand, as compared with controls. This effect was not observed exclusively in the same muscle where noxious stimulation was applied. We speculate that our findings reflect a generalized response to pain observation arising from hyperactivity of motor mirror neurons not involved in direct one-to-one simulation but, rather, in the representation of another's experience.

Keywords Synesthesia . Synesthetic pain . Phantom limb pain . Empathy for pain . Transcranial magnetic stimulation

Introduction

The perception of noxious stimulation to another can induce a personal experience of pain. This phenomenon is known as synesthetic pain, an experience that has been described seemingly from birth (congenital; Osborn & Derbyshire, 2010) and following pain-related trauma (acquired; Fitzgibbon, Enticott, et al., 2010; Giummarra & Bradshaw, 2008). Early incidence reports of synesthetic pain have suggested that around 30% of a healthy population experience congenital synesthetic pain and around 16% of an amputee group report synesthetic pain acquired following amputation (Fitzgibbon, Enticott, et al., 2010). Besides onset, there are key differences between congenital and acquired pain synesthetes: Congenital pain synesthetes experience pain in the same location that they observe injury in another, at an intensity of no more than 3.7/10, and demonstrate higher levels of empathy than do nonsynesthete controls (Osborn & Derbyshire, 2010). In contrast, acquired pain synesthetes experience high-intensity pain at the site of previous trauma (e.g., the phantom limb; Fitzgibbon, Enticott, et al., 2010) and, according to studies so far, do not demonstrate higher levels of empathy, as compared with nonsynesthete controls (Fitzgibbon et al., 2011; Giummarra et al., 2010). The neurobiological mechanisms that underpin synesthetic pain and its variants are currently unknown.

One explanatory model suggests that synesthetic pain may be induced through hyperactivity of vicarious neural circuits, involved in experiencing actual pain and observing noxious stimulation to another (Fitzgibbon, Giummarra, Georgiou-Karistianis, Enticott, & Bradshaw, 2010b). Vicarious neural activity may occur through mirror neurons, neurons that were first found in the ventral premotor cortex (F5) and the parietal area (PF) of the macaque brain and are active during both action observation and action execution (di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992). Although these areas have become known as the classical mirror neuron areas (for a review, see Rizzolatti & Craighero, 2004), areas of the brain with mirror properties, mirror systems, have since been identified in humans for action (for a review, see Rizzolatti & Craighero, 2004), as well as for emotions (e.g., Carr, Iacoboni, Dubeau, Mazziotta, & Lenzi, 2003; Enticott, Johnston, Herring, Hoy, & Fitzgerald, 2008; Wicker et al. …

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