Empathy or Ownership? Evidence from Corticospinal Excitability Modulation during Pain Observation

Recent studies show that motor responses similar to those present in one's own pain (freezing effect) occur as a result of observation of pain in others. This finding has been interpreted as the physiological basis of empathy. Alternatively, it can represent the physiological counterpart of an embodiment phenomenon related to the sense of body ownership. We compared the empathy and the ownership hypotheses by manipulating the perspective of the observed hand model receiving pain so that it could be a first-person perspective, the one in which embodiment occurs, or a third-person perspective, the one in which we usually perceive the others. Motor-evoked potentials (MEPs) by TMS over M1 were recorded from first dorsal interosseous muscle, whereas participants observed video clips showing (a) a needle penetrating or (b) a Q-tip touching a hand model, presented either in first-person or in third-person perspective. We found that a pain-specific inhibition of MEP amplitude (a significantly greater MEP reduction in the “pain” compared with the “touch” conditions) only pertains to the first-person perspective, and it is related to the strength of the self-reported embodiment. We interpreted this corticospinal modulation according to an “affective” conception of body ownership, suggesting that the body I feel as my own is the body I care more about.

[1]  Hiroaki Ishida,et al.  Shared Mapping of Own and Others' Bodies in Visuotactile Bimodal Area of Monkey Parietal Cortex , 2010, Journal of Cognitive Neuroscience.

[2]  Cristina Becchio,et al.  Timecourse of mirror and counter-mirror effects measured with transcranial magnetic stimulation , 2013, Social cognitive and affective neuroscience.

[3]  V. Ramachandran,et al.  Projecting sensations to external objects: evidence from skin conductance response , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  Maria V. Sanchez-Vives,et al.  Towards a Digital Body: The Virtual Arm Illusion , 2008, Frontiers in human neuroscience.

[5]  A. Sirigu,et al.  Racial Bias Reduces Empathic Sensorimotor Resonance with Other-Race Pain , 2010, Current Biology.

[6]  Salvatore Maria Aglioti,et al.  Somatotopic mapping of piano fingering errors in sensorimotor experts: TMS studies in pianists and visually trained musically naives. , 2014, Cerebral cortex.

[7]  James T. Enns,et al.  Mislocalizations of touch to a fake hand , 2004, Cognitive, affective & behavioral neuroscience.

[8]  Carlotta Fossataro,et al.  Embodiment of others’ hands elicits arousal responses similar to one’s own hands , 2014, Current Biology.

[9]  P. Mazzone,et al.  Comparison of descending volleys evoked by monophasic and biphasic magnetic stimulation of the motor cortex in conscious humans , 2001, Experimental Brain Research.

[10]  H. Topka,et al.  Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types , 2001, Clinical Neurophysiology.

[11]  Salvatore Maria Aglioti,et al.  The pain of a model in the personality of an onlooker: Influence of state-reactivity and personality traits on embodied empathy for pain , 2009, NeuroImage.

[12]  D. Lloyd.  Spatial limits on referred touch to an alien limb may reflect boundaries of visuo-tactile peripersonal space surrounding the hand , 2007, Brain and Cognition.

[13]  Cosimo Urgesi,et al.  Corticospinal facilitation during first and third person imagery , 2005, Experimental Brain Research.

[14]  Stefano Facchini,et al.  Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements , 2005, NeuroImage.

[15]  Francesca Garbarini,et al.  Embodiment of an alien hand interferes with intact-hand movements , 2013, Current Biology.

[16]  T. Singer,et al.  The empathic brain: how, when and why? , 2006, Trends in Cognitive Sciences.

[17]  H. Ehrsson,et al.  Behavioural Brain Research , 1999 .

[18]  R. Passingham,et al.  That's My Hand! Activity in Premotor Cortex Reflects Feeling of Ownership of a Limb , 2004, Science.

[19]  J. Decety,et al.  To what extent do we share the pain of others? Insight from the neural bases of pain empathy , 2006, Pain.

[20]  Nicholas P. Holmes,et al.  Effects of action observation on corticospinal excitability: Muscle specificity, direction, and timing of the mirror response , 2014, Neuropsychologia.

[21]  Massimiliano Valeriani,et al.  Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation , 2001, Neuroscience Letters.

[22]  F. Vignemont.  Body schema and body image—Pros and cons , 2010, Neuropsychologia.

[23]  Viviana Betti,et al.  Seeing the pain of others while being in pain: A laser-evoked potentials study , 2008, NeuroImage.

[24]  H. Ehrsson,et al.  Moving a Rubber Hand that Feels Like Your Own: A Dissociation of Ownership and Agency , 2012, Front. Hum. Neurosci..

[25]  V. Walsh,et al.  Motor empathy is a consequence of misattribution of sensory information in observers , 2014, Front. Hum. Neurosci..

[26]  P P Urban,et al.  Different short‐term modulation of cortical motor output to distal and proximal upper‐limb muscles during painful sensory nerve stimulation , 2004, Muscle & nerve.

[27]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[28]  Giovanni Gentile,et al.  A Shared Representation of the Space Near Oneself and Others in the Human Premotor Cortex , 2013, Current Biology.

[29]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[30]  Alessio Avenanti,et al.  Freezing or escaping? Opposite modulations of empathic reactivity to the pain of others , 2009, Cortex.

[31]  S. Rossi,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee , 2015, Clinical Neurophysiology.

[32]  Carlotta Fossataro,et al.  When your arm becomes mine: Pathological embodiment of alien limbs using tools modulates own body representation , 2015, Neuropsychologia.

[33]  Michel Magnin,et al.  Emotional Modulation of Pain: Is It the Sensation or What We Recall? , 2006, The Journal of Neuroscience.

[34]  Valeria I. Petkova,et al.  The Perspective Matters! Multisensory Integration in Ego-Centric Reference Frames Determines Full-Body Ownership , 2011, Front. Psychology.

[35]  Mark H. Davis.  Measuring individual differences in empathy: Evidence for a multidimensional approach. , 1983 .

[36]  L. Fogassi,et al.  A Touching Sight SII/PV Activation during the Observation and Experience of Touch , 2004, Neuron.

[37]  P. Haggard,et al.  Self and Other in the Human Motor System , 2006, Current Biology.

[38]  G. D. Iannetti,et al.  Interpersonal interactions and empathy modulate perception of threat and defensive responses , 2016, Scientific Reports.

[39]  H. Henrik Ehrsson,et al.  The Illusion of Owning a Third Arm , 2011, PloS one.

[40]  P. Haggard,et al.  The rubber hand illusion revisited: visuotactile integration and self-attribution. , 2005, Journal of experimental psychology. Human perception and performance.

[41]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[42]  Á. Pascual-Leone,et al.  Psychopathy and the mirror neuron system: Preliminary findings from a non-psychiatric sample , 2008, Psychiatry Research.

[43]  Lindsey J. Powell,et al.  My body or yours? The effect of visual perspective on cortical body representations. , 2006, Cerebral cortex.

[44]  Gaspare Galati,et al.  Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain , 2005, Nature Neuroscience.

[45]  Tania Singer,et al.  The painful side of empathy , 2005, Nature Neuroscience.

[46]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[47]  G. Rizzolatti,et al.  Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. , 2014, Physiological reviews.

[48]  Massimiliano Valeriani,et al.  Pain-related modulation of the human motor cortex , 2003, Neurological research.

[49]  V. Gallese.  The manifold nature of interpersonal relations: the quest for a common mechanism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  D. Saint-Amour,et al.  EEG and neuronavigated single-pulse TMS in the study of the observation/execution matching system: Are both techniques measuring the same process? , 2008, Journal of Neuroscience Methods.

[51]  Domenica Le Pera,et al.  Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain , 2001, Clinical Neurophysiology.

[52]  Paul T. Sowden,et al.  Your hand or mine? The extrastriate body area , 2008, NeuroImage.

[53]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[54]  Jonathan D. Cohen,et al.  Rubber hands ‘feel’ touch that eyes see , 1998, Nature.

[55]  F. Pavani,et al.  Left tactile extinction following visual stimulation of a rubber hand. , 2000, Brain : a journal of neurology.

[56]  M. Tsakiris.  My body in the brain: A neurocognitive model of body-ownership , 2010, Neuropsychologia.

[57]  A. Berti,et al.  Pain and Body Awareness: Evidence from Brain-Damaged Patients with Delusional Body Ownership , 2013, Front. Hum. Neurosci..

[58]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[59]  C. Spence,et al.  Visual Capture of Touch: Out-of-the-Body Experiences With Rubber Gloves , 2000, Psychological science.

[60]  V. Gazzola,et al.  Transcranial magnetic stimulation reveals two functionally distinct stages of motor cortex involvement during perception of emotional body language , 2014, Brain Structure and Function.

[61]  M. Hallett,et al.  Focal transcranial magnetic stimulation and response bias in a forced-choice task. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[62]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[63]  F. Vignemont,et al.  Pain and Bodily Care: Whose Body Matters? , 2015 .

[64]  M. Brass,et al.  Effects of Being Imitated on Motor Responses Evoked by Pain Observation: Exerting Control Determines Action Tendencies When Perceiving Pain in Others , 2014, The Journal of Neuroscience.

[65]  P. Haggard,et al.  The rubber hand illusion: Sensitivity and reference frame for body ownership , 2007, Consciousness and Cognition.

[66]  F. Garbarini,et al.  Bodily ownership modulation in defensive responses: physiological evidence in brain-damaged patients with pathological embodiment of other’s body parts , 2016, Scientific Reports.

[67]  Salvatore Maria Aglioti,et al.  Stimulus-driven modulation of motor-evoked potentials during observation of others' pain , 2006, NeuroImage.