When Right Feels Left: Referral of Touch and Ownership between the Hands

Feeling touch on a body part is paradigmatically considered to require stimulation of tactile afferents from the body part in question, at least in healthy non-synaesthetic individuals. In contrast to this view, we report a perceptual illusion where people experience “phantom touches” on a right rubber hand when they see it brushed simultaneously with brushes applied to their left hand. Such illusory duplication and transfer of touch from the left to the right hand was only elicited when a homologous (i.e., left and right) pair of hands was brushed in synchrony for an extended period of time. This stimulation caused the majority of our participants to perceive the right rubber hand as their own and to sense two distinct touches – one located on the right rubber hand and the other on their left (stimulated) hand. This effect was supported by quantitative subjective reports in the form of questionnaires, behavioral data from a task in which participants pointed to the felt location of their right hand, and physiological evidence obtained by skin conductance responses when threatening the model hand. Our findings suggest that visual information augments subthreshold somatosensory responses in the ipsilateral hemisphere, thus producing a tactile experience from the non-stimulated body part. This finding is important because it reveals a new bilateral multisensory mechanism for tactile perception and limb ownership.

[1]  C. Sherrick,et al.  EFFECTS OF DOUBLE SIMULTANEOUS STIMULATION OF THE SKIN. , 1964, The American journal of psychology.

[2]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[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]  C. Gross,et al.  Visuospatial properties of ventral premotor cortex. , 1997, Journal of neurophysiology.

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

[6]  Anna W. Roe,et al.  Optical Imaging of a Tactile Illusion in Area 3b of the Primary Somatosensory Cortex , 2003, Science.

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

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

[9]  R. Lemon,et al.  Cortical afferents and efferents of monkey postarcuate area: an anatomical and electrophysiological study , 2004, Experimental Brain Research.

[10]  T. P. S. Powell,et al.  The cortico-cortical connections of area 7b, PF, in the parietal lobe of the monkey , 1987, Brain Research.

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

[12]  Matthew Botvinick,et al.  Neuroscience. Probing the neural basis of body ownership. , 2004, Science.

[13]  A. Iriki,et al.  Book Review: Bilateral Activity and Callosal Connections in the Somatosensory Cortex , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[14]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[15]  P. Haggard,et al.  Noninformative vision improves the spatial resolution of touch in humans , 2001, Current Biology.

[16]  M. Graziano.  Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Hari,et al.  Relationship between Responses to Contra- and Ipsilateral Stimuli in the Human Second Somatosensory Cortex SII , 1999, NeuroImage.

[18]  A Villringer,et al.  Somatotopic organization of human secondary somatosensory cortex. , 2001, Cerebral cortex.

[19]  K D Alloway,et al.  Cross-correlation analysis reveals laminar differences in thalamocortical interactions in the somatosensory system. , 1996, Journal of neurophysiology.

[20]  David R. Wozny,et al.  Human trimodal perception follows optimal statistical inference. , 2008, Journal of vision.

[21]  M. Dawson,et al.  The electrodermal system , 2007 .

[22]  H. Ehrsson,et al.  How Many Arms Make a Pair? Perceptual Illusion of Having an Additional Limb , 2009, Perception.

[23]  P. Haggard,et al.  Visual enhancement of touch in spatial body representation , 2003, Experimental Brain Research.

[24]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[25]  G. Rizzolatti,et al.  Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses , 1981, Behavioural Brain Research.

[26]  I ROCK,et al.  Vision and Touch: An Experimentally Created Conflict between the Two Senses , 1964, Science.

[27]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

[28]  G. Rizzolatti,et al.  Afferent and efferent projections of the inferior area 6 in the macaque monkey , 1986, The Journal of comparative neurology.

[29]  Juhani Hyva¨rinen.  Regional distribution of functions in parietal association area 7 of the monkey , 1981, Brain Research.

[30]  Riitta Hari,et al.  Transient Suppression of Ipsilateral Primary Somatosensory Cortex during Tactile Finger Stimulation , 2006, The Journal of Neuroscience.

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

[32]  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.

[33]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[34]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

[35]  J. Duhamel,et al.  Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey , 2007, The Journal of Neuroscience.

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

[37]  Y. Iwamura,et al.  Bilateral receptive field neurons and callosal connections in the somatosensory cortex. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  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.

[39]  P. Halligan,et al.  Simulating sensory-motor incongruence in healthy volunteers: implications for a cortical model of pain. , 2005, Rheumatology.

[40]  V. Ramachandran,et al.  Synaesthesia in phantom limbs induced with mirrors , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  S. Shimojo,et al.  Illusions: What you see is what you hear , 2000, Nature.

[42]  H. Ehrsson,et al.  Referral of sensation to an advanced humanoid robotic hand prosthesis , 2009, Scandinavian journal of plastic and reconstructive surgery and hand surgery.

[43]  H. Ehrsson,et al.  Upper limb amputees can be induced to experience a rubber hand as their own , 2008, Brain : a journal of neurology.

[44]  R. Dolan,et al.  Threatening a rubber hand that you feel is yours elicits a cortical anxiety response , 2007, Proceedings of the National Academy of Sciences.

[45]  E P Gardner,et al.  Spatial integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. , 1980, Journal of Neurophysiology.

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

[47]  Takeo Ishigaki,et al.  Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation—an fMRI study , 2005, Clinical Neurophysiology.

[48]  S. Tipper,et al.  Vision influences tactile perception at body sites that cannot be viewed directly , 2001, Experimental Brain Research.

[49]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.

[50]  John C. Marshall,et al.  When seeing is feeling: Acquired synaesthesia or phantom touch? , 1996 .

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

[52]  C. Robinson,et al.  Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis , 1980, The Journal of comparative neurology.

[53]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[54]  Geraint Rees,et al.  The Cutaneous Rabbit Illusion Affects Human Primary Sensory Cortex Somatotopically , 2006, PLoS biology.

[55]  H Burton,et al.  Somatotopographic organization in the second somatosensory area of M. fascicularis , 1980, The Journal of comparative neurology.

[56]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[57]  F. Bremmer,et al.  Spatial invariance of visual receptive fields in parietal cortex neurons , 1997, Nature.

[58]  K. Sathian,et al.  Intermanual referral of sensation to anesthetic hands , 2000, Neurology.

[59]  S. Shimojo,et al.  Sensory modalities are not separate modalities: plasticity and interactions , 2001, Current Opinion in Neurobiology.

[60]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[61]  P. Roland,et al.  Somatosensory Activations of the Parietal Operculum of Man. A PET Study , 1995, The European journal of neuroscience.

[62]  M. Tanaka,et al.  Processing of tactile and kinesthetic signals from bilateral sides of the body in the postcentral gyrus of awake monkeys , 2002, Behavioural Brain Research.

[63]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[64]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[65]  S. Lederman,et al.  Texture perception: studies of intersensory organization using a discrepancy paradigm, and visual versus tactual psychophysics. , 1981, Journal of experimental psychology. Human perception and performance.

[66]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[67]  M. Raichle,et al.  Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. , 1993, Somatosensory & motor research.

[68]  F. A. Geldard,et al.  The Cutaneous "Rabbit": A Perceptual Illusion , 1972, Science.

[69]  V. Ramachandran,et al.  Touching the phantom limb , 1995, Nature.

[70]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[71]  C. Colby,et al.  Heterogeneity of extrastriate visual areas and multiple parietal areas in the Macaque monkey , 1991, Neuropsychologia.

[72]  U Salvolini,et al.  Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients , 1999, The European journal of neuroscience.

[73]  J Hyvärinen,et al.  Regional distribution of functions in parietal association area 7 of the monkey. , 1981, Brain research.

[74]  P. Haggard,et al.  Viewing the body modulates tactile receptive fields , 2007, Experimental Brain Research.