Integration of Visual and Proprioceptive Limb Position Information in Human Posterior Parietal, Premotor, and Extrastriate Cortex

The brain constructs a flexible representation of the body from multisensory information. Previous work on monkeys suggests that the posterior parietal cortex (PPC) and ventral premotor cortex (PMv) represent the position of the upper limbs based on visual and proprioceptive information. Human experiments on the rubber hand illusion implicate similar regions, but since such experiments rely on additional visuo-tactile interactions, they cannot isolate visuo-proprioceptive integration. Here, we independently manipulated the position (palm or back facing) of passive human participants' unseen arm and of a photorealistic virtual 3D arm. Functional magnetic resonance imaging (fMRI) revealed that matching visual and proprioceptive information about arm position engaged the PPC, PMv, and the body-selective extrastriate body area (EBA); activity in the PMv moreover reflected interindividual differences in congruent arm ownership. Further, the PPC, PMv, and EBA increased their coupling with the primary visual cortex during congruent visuo-proprioceptive position information. These results suggest that human PPC, PMv, and EBA evaluate visual and proprioceptive position information and, under sufficient cross-modal congruence, integrate it into a multisensory representation of the upper limb in space. SIGNIFICANCE STATEMENT The position of our limbs in space constantly changes, yet the brain manages to represent limb position accurately by combining information from vision and proprioception. Electrophysiological recordings in monkeys have revealed neurons in the posterior parietal and premotor cortices that seem to implement and update such a multisensory limb representation, but this has been difficult to demonstrate in humans. Our fMRI experiment shows that human posterior parietal, premotor, and body-selective visual brain areas respond preferentially to a virtual arm seen in a position corresponding to one's unseen hidden arm, while increasing their communication with regions conveying visual information. These brain areas thus likely integrate visual and proprioceptive information into a flexible multisensory body representation.

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

[2]  J. Hyvärinen Posterior parietal lobe of the primate brain. , 1982, Physiological reviews.

[3]  C. Gross,et al.  Coding of visual space by premotor neurons. , 1994, Science.

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

[5]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[6]  C. Galletti,et al.  Arm Movement‐related Neurons in the Visual Area V6A of the Macaque Superior Parietal Lobule , 1997, The European journal of neuroscience.

[7]  R. E. Passingham,et al.  Parietal cortex and movement II. Spatial representation , 1997, Experimental Brain Research.

[8]  G. Rizzolatti,et al.  Parietal cortex: from sight to action , 1997, Current Opinion in Neurobiology.

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

[10]  D. Wolpert,et al.  Maintaining internal representations: the role of the human superior parietal lobe , 1998, Nature Neuroscience.

[11]  R. J. van Beers,et al.  Integration of proprioceptive and visual position-information: An experimentally supported model. , 1999, Journal of neurophysiology.

[12]  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.

[13]  A P Batista,et al.  Reach plans in eye-centered coordinates. , 1999, Science.

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

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

[16]  N. Kanwisher,et al.  The Human Body , 2001 .

[17]  R. Passingham,et al.  The Attentional Role of the Left Parietal Cortex: The Distinct Lateralization and Localization of Motor Attention in the Human Brain , 2001, Journal of Cognitive Neuroscience.

[18]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

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

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

[21]  Nicholas P. Holmes,et al.  The body schema and multisensory representation(s) of peripersonal space , 2004, Cognitive Processing.

[22]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[23]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[24]  Nicholas P. Holmes,et al.  Visual bias of unseen hand position with a mirror: spatial and temporal factors , 2005, Experimental Brain Research.

[25]  Paul S. Morgan,et al.  Parietal updating of limb posture: An event-related fMRI study , 2006, Neuropsychologia.

[26]  Murray Grossman,et al.  Left Inferior Parietal Representations for Skilled Hand-Object Interactions: Evidence from Stroke and Corticobasal Degeneration , 2007, Cortex.

[27]  E. Macaluso,et al.  Processing of multisensory spatial congruency can be dissociated from working memory and visuo‐spatial attention , 2007, The European journal of neuroscience.

[28]  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.

[29]  P. Downing,et al.  The neural basis of visual body perception , 2007, Nature Reviews Neuroscience.

[30]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[31]  H. C. Dijkerman,et al.  Somatosensory processes subserving perception and action , 2007, Behavioral and Brain Sciences.

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

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

[34]  Patrizia Fattori,et al.  Hand Orientation during Reach-to-Grasp Movements Modulates Neuronal Activity in the Medial Posterior Parietal Area V6A , 2009, The Journal of Neuroscience.

[35]  Jonathan D. Nelson,et al.  Multiple Parietal Reach Regions in Humans: Cortical Representations for Visual and Proprioceptive Feedback during On-Line Reaching , 2009, The Journal of Neuroscience.

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

[37]  P. Downing,et al.  The role of occipitotemporal body-selective regions in person perception , 2011, Cognitive neuroscience.

[38]  Kalanit Grill-Spector,et al.  Not one extrastriate body area: Using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex , 2011, NeuroImage.

[39]  Jody C Culham,et al.  Functional magnetic resonance adaptation reveals the involvement of the dorsomedial stream in hand orientation for grasping. , 2011, Journal of neurophysiology.

[40]  F. D. de Lange,et al.  Motor planning is facilitated by adopting an action's goal posture: an fMRI study. , 2012, Cerebral cortex.

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

[42]  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.

[43]  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.

[44]  Henrik Walter,et al.  Proprioceptive drift in the rubber hand illusion is intensified following 1 Hz TMS of the left EBA , 2014, Front. Hum. Neurosci..

[45]  Deborah A Barany,et al.  Feature Interactions Enable Decoding of Sensorimotor Transformations for Goal-Directed Movement , 2014, The Journal of Neuroscience.

[46]  P. Downing,et al.  The lateral occipitotemporal cortex in action , 2015, Trends in Cognitive Sciences.

[47]  Felix Blankenburg,et al.  Network activity underlying the illusory self‐attribution of a dummy arm , 2015, Human brain mapping.

[48]  Karl J. Friston,et al.  Sensory Processing and the Rubber Hand Illusion—An Evoked Potentials Study , 2015, Journal of Cognitive Neuroscience.

[49]  Felix Blankenburg,et al.  That's not quite me: limb ownership encoding in the brain. , 2016, Social cognitive and affective neuroscience.

[50]  J Randall Flanagan,et al.  Planning Ahead: Object-Directed Sequential Actions Decoded from Human Frontoparietal and Occipitotemporal Networks. , 2015, Cerebral cortex.