Patterns of neural activity in the human ventral premotor cortex reflect a whole-body multisensory percept

Previous research has shown that the integration of multisensory signals from the body in fronto-parietal association areas underlies the perception of a body part as belonging to one's physical self. What are the neural mechanisms that enable the perception of one's entire body as a unified entity? In one behavioral and one fMRI multivoxel pattern analysis experiment, we used a full-body illusion to investigate how congruent visuo-tactile signals from a single body part facilitate the emergence of the sense of ownership of the entire body. To elicit this illusion, participants viewed the body of a mannequin from the first-person perspective via head-mounted displays while synchronous touches were applied to the hand, abdomen, or leg of the bodies of the participant and the mannequin; asynchronous visuo-tactile stimuli served as controls. The psychometric data indicated that the participants perceived ownership of the entire artificial body regardless of the body segment that received the synchronous visuo-tactile stimuli. Based on multivoxel pattern analysis, we found that the neural responses in the left ventral premotor cortex displayed illusion-specific activity patterns that generalized across all tested pairs of body parts. Crucially, a tripartite generalization analysis revealed the whole-body specificity of these premotor activity patterns. Finally, we also identified multivoxel patterns in the premotor, intraparietal, and lateral occipital cortices and in the putamen that reflected multisensory responses specific to individual body parts. Based on these results, we propose that the dynamic formation of a whole-body percept may be mediated by neuronal populations in the ventral premotor cortex that contain visuo-tactile receptive fields encompassing multiple body segments.

[1]  G. Rizzolatti,et al.  Coding of peripersonal space in inferior premotor cortex (area F4). , 1996, Journal of neurophysiology.

[2]  H. Henrik Ehrsson,et al.  When Right Feels Left: Referral of Touch and Ownership between the Hands , 2009, PloS one.

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

[4]  M. Sereno,et al.  A human parietal face area contains aligned head-centered visual and tactile maps , 2006, Nature Neuroscience.

[5]  H. Henrik Ehrsson,et al.  Being Barbie: The Size of One’s Own Body Determines the Perceived Size of the World , 2011, PloS one.

[6]  Maria V. Sanchez-Vives,et al.  Inducing Illusory Ownership of a Virtual Body , 2009, Front. Neurosci..

[7]  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.

[8]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[9]  J. Hyvärinen,et al.  Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. , 1974, Brain : a journal of neurology.

[10]  H. Ehrsson,et al.  Illusory Changes in Body Size Modulate Body Satisfaction in a Way That Is Related to Non-Clinical Eating Disorder Psychopathology , 2014, PloS one.

[11]  H. Ehrsson,et al.  Disintegration of Multisensory Signals from the Real Hand Reduces Default Limb Self-Attribution: An fMRI Study , 2013, The Journal of Neuroscience.

[12]  C. Gross,et al.  A bimodal map of space: somatosensory receptive fields in the macaque putamen with corresponding visual receptive fields , 1993, Experimental Brain Research.

[13]  Ana Tajadura-Jiménez,et al.  Plasticity in unimodal and multimodal brain areas reflects multisensory changes in self-face identification. , 2015, Cerebral cortex.

[14]  Atsushi Iriki,et al.  Bilateral receptive field neurons in the hindlimb region of the postcentral somatosensory cortex in awake macaque monkeys , 2000, Experimental Brain Research.

[15]  G. Rizzolatti,et al.  Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses , 1981, Behavioural Brain Research.

[16]  A. Pouget,et al.  Reference frames for representing visual and tactile locations in parietal cortex , 2005, Nature Neuroscience.

[17]  Robin Bekrater-Bodmann,et al.  The perceptual and neuronal stability of the rubber hand illusion across contexts and over time , 2012, Brain Research.

[18]  T. Metzinger,et al.  Video Ergo Sum: Manipulating Bodily Self-Consciousness , 2007, Science.

[19]  Tirin Moore,et al.  Complex movements evoked by microstimulation of the ventral intraparietal area , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[21]  O. Blanke Multisensory brain mechanisms of bodily self-consciousness , 2012, Nature Reviews Neuroscience.

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

[23]  T. Metzinger,et al.  Full-body illusions and minimal phenomenal selfhood , 2009, Trends in Cognitive Sciences.

[24]  Johan Wessberg,et al.  A Monte Carlo method for locally multivariate brain mapping , 2011, NeuroImage.

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

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

[27]  H. Ehrsson,et al.  That's Near My Hand! Parietal and Premotor Coding of Hand-Centered Space Contributes to Localization and Self-Attribution of the Hand , 2012, Journal of Neuroscience.

[28]  Giovanni Gentile,et al.  The Invisible Hand Illusion: Multisensory Integration Leads to the Embodiment of a Discrete Volume of Empty Space , 2013, Journal of Cognitive Neuroscience.

[29]  M. Sereno,et al.  Multisensory maps in parietal cortex☆ , 2014, Current Opinion in Neurobiology.

[30]  Adrian J. T. Smith Comment: Minimal conditions for the simplest form of self-consciousness , 2010 .

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

[32]  B. Stein The new handbook of multisensory processes , 2012 .

[33]  D H Hubel,et al.  Republication of The Journal of Physiology (1959) 148, 574-591: Receptive fields of single neurones in the cat's striate cortex. 1959. , 2009, The Journal of physiology.

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

[35]  M. Slater,et al.  The building blocks of the full body ownership illusion , 2013, Front. Hum. Neurosci..

[36]  M. Beauchamp,et al.  Neural Substrates of Reliability-Weighted Visual-Tactile Multisensory Integration , 2010, Front. Syst. Neurosci..

[37]  Justin M. Harris,et al.  If I Were You: Perceptual Illusion of Body Swapping , 2008, PloS one.

[38]  Y. Iwamura Hierarchical somatosensory processing , 1998, Current Opinion in Neurobiology.

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

[40]  Michael S Beauchamp,et al.  See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex , 2005, Current Opinion in Neurobiology.

[41]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[42]  T. Aflalo,et al.  Mapping Behavioral Repertoire onto the Cortex , 2007, Neuron.

[43]  Johan Wessberg,et al.  Somatotopic Organization of Gentle Touch Processing in the Posterior Insular Cortex , 2009, The Journal of Neuroscience.

[44]  Johan Wessberg,et al.  Clustered sampling improves random subspace brain mapping , 2012, Pattern Recognit..

[45]  O. Blanke,et al.  Multi-Sensory and Sensorimotor Foundation of Bodily Self-Consciousness – An Interdisciplinary Approach , 2011, Front. Psychology.

[46]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[47]  Valeria I. Petkova,et al.  From Part- to Whole-Body Ownership in the Multisensory Brain , 2011, Current Biology.

[48]  Ehud Zohary,et al.  Is That Near My Hand? Multisensory Representation of Peripersonal Space in Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[49]  M. Sereno,et al.  Mapping multisensory parietal face and body areas in humans , 2012, Proceedings of the National Academy of Sciences.

[50]  H. Ehrsson The Experimental Induction of Out-of-Body Experiences , 2007, Science.

[51]  B. Robertson A celebration of the 50th anniversary of David Hubel and Torsten Wiesel's Receptive fields of single neurones in the cat's striate cortex , 2009, The Journal of physiology.

[52]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[53]  Olaf Blanke,et al.  Full body illusion is associated with widespread skin temperature reduction , 2013, Front. Behav. Neurosci..

[54]  Mariela Rance,et al.  The Importance of Synchrony and Temporal Order of Visual and Tactile Input for Illusory Limb Ownership Experiences – An fMRI Study Applying Virtual Reality , 2014, PloS one.

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

[56]  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.

[57]  Olaf Blanke,et al.  The brain network reflecting bodily self-consciousness: a functional connectivity study. , 2014, Social cognitive and affective neuroscience.

[58]  P. Haggard,et al.  Neural signatures of body ownership: a sensory network for bodily self-consciousness. , 2007, Cerebral cortex.

[59]  M. Corbetta,et al.  Extrastriate body area in human occipital cortex responds to the performance of motor actions , 2004, Nature Neuroscience.

[60]  M. Graziano,et al.  Location of the polysensory zone in the precentral gyrus of anesthetized monkeys , 2000, Experimental Brain Research.

[61]  Gian Luca Romani,et al.  Viewing One's Own Face Being Touched Modulates Tactile Perception: An fMRI Study , 2011, Journal of Cognitive Neuroscience.

[62]  Maria V. Sanchez-Vives,et al.  First Person Experience of Body Transfer in Virtual Reality , 2010, PloS one.

[63]  E. Zohary,et al.  Topographic Representation of the Human Body in the Occipitotemporal Cortex , 2010, Neuron.

[64]  Dylan F. Cooke,et al.  Parieto-frontal interactions, personal space, and defensive behavior , 2006, Neuropsychologia.

[65]  Valeria I. Petkova,et al.  Integration of visual and tactile signals from the hand in the human brain: an FMRI study. , 2011, Journal of neurophysiology.

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

[67]  Hans-Jochen Heinze,et al.  Referral of Touch and Ownership between the Hands and the Role of the Somatosensory Cortices , 2013, PloS one.

[68]  Joan Llobera,et al.  The relationship between virtual body ownership and temperature sensitivity , 2013, Journal of The Royal Society Interface.

[69]  G. Rizzolatti,et al.  The Organization of the Frontal Motor Cortex. , 2000, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[70]  P. Roland,et al.  I Feel My Hand Moving A New Role of the Primary Motor Cortex in Somatic Perception of Limb Movement , 2002, Neuron.

[71]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[72]  O. Blanke,et al.  Multisensory Mechanisms in Temporo-Parietal Cortex Support Self-Location and First-Person Perspective , 2011, Neuron.

[73]  Alisa Mandrigin,et al.  Bodily ownership and self-location: Components of bodily self-consciousness , 2013, Consciousness and Cognition.