Threatening a rubber hand that you feel is yours elicits a cortical anxiety response

The feeling of body ownership is a fundamental aspect of self-consciousness. The underlying neural mechanisms can be studied by using the illusion where a person is made to feel that a rubber hand is his or her own hand by brushing the person's hidden real hand and synchronously brushing the artificial hand that is in full view. Here we show that threat to the rubber hand can induce a similar level of activity in the brain areas associated with anxiety and interoceptive awareness (insula and anterior cingulate cortex) as when the person's real hand is threatened. We further show that the stronger the feeling of ownership of the artificial hand, the stronger the threat-evoked neuronal responses in the areas reflecting anxiety. Furthermore, across subjects, activity in multisensory areas reflecting ownership predicted the activity in the interoceptive system when the hand was under threat. Finally, we show that there is activity in medial wall motor areas, reflecting an urge to withdraw the artificial hand when it is under threat. These findings suggest that artificial limbs can evoke the same feelings as real limbs and provide objective neurophysiological evidence that the rubber hand is fully incorporated into the body. These findings are of fundamental importance because they suggest that the feeling of body ownership is associated with changes in the interoceptive systems.

[1]  C. Darwin The Expression of the Emotions in Man and Animals , .

[2]  J. Gibson The Senses Considered As Perceptual Systems , 1967 .

[3]  J. Winn,et al.  Brain , 1878, The Lancet.

[4]  J. Tanji,et al.  Neuronal activity in the cortical supplementary motor area related with distal and proximal forelimb movements , 1979, Neuroscience Letters.

[5]  G. McCarthy,et al.  Functional organization of human supplementary motor cortex studied by electrical stimulation , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  E. Cabanis,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy and Mri , 1991 .

[7]  M Ingvar,et al.  Urge to scratch represented in the human cerebral cortex during itch. , 1994, Journal of neurophysiology.

[8]  M. Tanaka,et al.  Coding of modified body schema during tool use by macaque postcentral neurones. , 1996, Neuroreport.

[9]  S. Stone-Elander,et al.  Traumatic nociceptive pain activates the hypothalamus and the periaqueductal gray: a positron emission tomography study , 1996, Pain.

[10]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[11]  H. Ellis stroke , 1997, The Lancet.

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

[13]  J. Tanji,et al.  Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. , 1998, Journal of neurophysiology.

[14]  The science of haptics gets in touch with prosthetics , 1999, The Lancet.

[15]  K. Chang,et al.  Subregions within the Supplementary Motor Area Activated at Different Stages of Movement Preparation and Execution , 1999, NeuroImage.

[16]  Ravi S. Menon,et al.  Dissociating pain from its anticipation in the human brain. , 1999, Science.

[17]  C. L. Kwan,et al.  An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli , 2000, Pain.

[18]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[19]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

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

[21]  William Craelius,et al.  The bionic man: restoring mobility. , 2002, Science.

[22]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[23]  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.

[24]  C. Spence,et al.  Multisensory integration and the body schema: close to hand and within reach , 2003, Current Biology.

[25]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

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

[27]  Peter Svensson,et al.  Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation , 2003, European journal of pain.

[28]  Antonio Damasio,et al.  Mental self: The person within , 2003, Nature.

[29]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces to restore motor function and probe neural circuits , 2003, Nature Reviews Neuroscience.

[30]  Dylan F. Cooke,et al.  Defensive movements evoked by air puff in monkeys. , 2003, Journal of neurophysiology.

[31]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[32]  M. Botvinick Probing the Neural Basis of Body Ownership , 2004, Science.

[33]  J. Donoghue,et al.  Brain–Machine and Brain–Computer Interfaces , 2004, Stroke.

[34]  Edward E. Smith,et al.  Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain , 2004, Science.

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

[36]  C. Spence,et al.  Extending or projecting peripersonal space with tools? Multisensory interactions highlight only the distal and proximal ends of tools , 2004, Neuroscience Letters.

[37]  R. Passingham,et al.  Attention to Intention , 2004, Science.

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

[39]  H. Kornhuber,et al.  Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements , 2004, Experimental Brain Research.

[40]  A. Maravita,et al.  Tools for the body (schema) , 2004, Trends in Cognitive Sciences.

[41]  Ewald Moser,et al.  Premovement activity of the pre-supplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI. , 2005, Human movement science.

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

[43]  Raymond J. Dolan,et al.  Anxiety Reduction through Detachment: Subjective, Physiological, and Neural Effects , 2005, Journal of Cognitive Neuroscience.

[44]  J. Maunsell,et al.  Touching a Rubber Hand: Feeling of Body Ownership Is Associated with Activity in Multisensory Brain Areas , 2005, The Journal of Neuroscience.

[45]  Atsushi Iriki,et al.  Shaping multisensory action–space with tools: evidence from patients with cross-modal extinction , 2005, Neuropsychologia.

[46]  Angela R Laird,et al.  Brain activity associated with painfully hot stimuli applied to the upper limb: A meta‐analysis , 2005, Human brain mapping.

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

[48]  S. Kitazawa,et al.  Referral of tactile sensation to the tips of L-shaped sticks. , 2005, Journal of neurophysiology.

[49]  Raymond J. Dolan,et al.  Levels of appraisal: A medial prefrontal role in high-level appraisal of emotional material , 2006, NeuroImage.

[50]  Kathleen R. Gibson The use of tools by human and non-human primates , 2007, International Journal of Primatology.

[51]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[52]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1956 .