Rapid Recalibration of Peri-Personal Space: Psychophysical, Electrophysiological, and Neural Network Modeling Evidence

Abstract Interactions between individuals and the environment occur within the peri-personal space (PPS). The encoding of this space plastically adapts to bodily constraints and stimuli features. However, these remapping effects have not been demonstrated on an adaptive time-scale, trial-to-trial. Here, we test this idea first via a visuo-tactile reaction time (RT) paradigm in augmented reality where participants are asked to respond as fast as possible to touch, as visual objects approach them. Results demonstrate that RTs to touch are facilitated as a function of visual proximity, and the sigmoidal function describing this facilitation shifts closer to the body if the immediately precedent trial had indexed a smaller visuo-tactile disparity. Next, we derive the electroencephalographic correlates of PPS and demonstrate that this multisensory measure is equally shaped by recent sensory history. Finally, we demonstrate that a validated neural network model of PPS is able to account for the present results via a simple Hebbian plasticity rule. The present findings suggest that PPS encoding remaps on a very rapid time-scale and, more generally, that it is sensitive to sensory history, a key feature for any process contextualizing subsequent incoming sensory information (e.g., a Bayesian prior).

[1]  A Farnè,et al.  Dynamic size‐change of hand peripersonal space following tool use , 2000, Neuroreport.

[2]  P. Bertelson,et al.  Recalibration of temporal order perception by exposure to audio-visual asynchrony. , 2004, Brain research. Cognitive brain research.

[3]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[4]  G Rizzolatti,et al.  The Space Around Us , 1997, Science.

[5]  D. Whitney,et al.  Serial dependence in visual perception , 2011, Nature Neuroscience.

[6]  G. Verni,et al.  Amputation and prosthesis implantation shape body and peripersonal space representations , 2013, Scientific Reports.

[7]  Jon Driver,et al.  Active Tool Use with the Contralesional Hand Can Reduce Cross-modal Extinction of Touch on that Hand , 2002, Neurocase.

[8]  Olaf Blanke,et al.  Audio-Tactile and Peripersonal Space Processing Around the Trunk in Human Parietal and Temporal Cortex: An Intracranial EEG Study , 2018, bioRxiv.

[9]  Andrea Serino,et al.  Peripersonal space (PPS) as a multisensory interface between the individual and the environment, defining the space of the self , 2019, Neuroscience & Biobehavioral Reviews.

[10]  A. Arnsten,et al.  Dynamic Network Connectivity: A new form of neuroplasticity , 2010, Trends in Cognitive Sciences.

[11]  A. Serino,et al.  Dynamic Sounds Capture the Boundaries of Peripersonal Space Representation in Humans , 2012, PloS one.

[12]  Andrea Serino,et al.  High Action Values Occur Near Our Body , 2019, Trends in Cognitive Sciences.

[13]  W. Wildman,et al.  Theoretical Neuroscience , 2014 .

[14]  H. C. Dijkerman,et al.  On the contribution of overt tactile expectations to visuo-tactile interactions within the peripersonal space , 2017, Experimental Brain Research.

[15]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[16]  Mauro Ursino,et al.  Visuotactile Representation of Peripersonal Space: A Neural Network Study , 2010, Neural Computation.

[17]  Bruno Herbelin,et al.  Peripersonal Space: An Index of Multisensory Body–Environment Interactions in Real, Virtual, and Mixed Realities , 2018, Front. ICT.

[18]  S. Fernberger Interdependence of judgments within the series for the method of constant stimuli. , 1920 .

[19]  O. Blanke,et al.  Full body action remapping of peripersonal space: The case of walking , 2015, Neuropsychologia.

[20]  Hugo Zeberg,et al.  Tool Use Changes the Spatial Extension of the Magnetic Touch Illusion , 2018, Journal of experimental psychology. General.

[21]  Justine Cléry,et al.  Cortical networks for encoding near and far space in the non-human primate , 2018, NeuroImage.

[22]  D. O. Hebb,et al.  The organization of behavior , 1988 .

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

[24]  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.

[25]  Volker Dürr,et al.  Transfer of Spatial Contact Information Among Limbs and the Notion of Peripersonal Space in Insects , 2018, Front. Comput. Neurosci..

[26]  Francesco Pavani,et al.  Action Planning Modulates Peripersonal Space , 2019, Journal of Cognitive Neuroscience.

[27]  Francesco Pavani,et al.  Grasping actions remap peripersonal space , 2009, Neuroreport.

[28]  Alessandro Farnè,et al.  Mind the Depth: Visual Perception of Shapes Is Better in Peripersonal Space , 2018, Psychological science.

[29]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[30]  M. Wallace,et al.  Event Related Potentials Index Rapid Recalibration to Audiovisual Temporal Asynchrony , 2017, Front. Integr. Neurosci..

[31]  B. Stein,et al.  Spatial determinants of multisensory integration in cat superior colliculus neurons. , 1996, Journal of neurophysiology.

[32]  D. Lehmann,et al.  Principles of spatial analysis , 1987 .

[33]  Randolph Blake,et al.  Probing Electrophysiological Indices of Perceptual Awareness across Unisensory and Multisensory Modalities , 2018, Journal of Cognitive Neuroscience.

[34]  Harold Bekkering,et al.  Sensorimotor integration , 2000 .

[35]  Weiwei Zhang,et al.  Familiarity Speeds Up Visual Short-term Memory Consolidation: Electrophysiological Evidence from Contralateral Delay Activities , 2018, Journal of Cognitive Neuroscience.

[36]  Denis Brunet,et al.  Topographic ERP Analyses: A Step-by-Step Tutorial Review , 2008, Brain Topography.

[37]  Olaf Blanke,et al.  Audio-visual sensory deprivation degrades visuo-tactile peri-personal space , 2018, Consciousness and Cognition.

[38]  Matthew A. De Niear,et al.  Atypical rapid audio‐visual temporal recalibration in autism spectrum disorders , 2017, Autism research : official journal of the International Society for Autism Research.

[39]  Andrea Serino,et al.  Everyday use of the computer mouse extends peripersonal space representation , 2010, Neuropsychologia.

[40]  Tobias Bonhoeffer,et al.  Area-specific mapping of binocular disparity across mouse visual cortex , 2019 .

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

[42]  Elisabetta Làdavas,et al.  Seeing where your hands are , 1997, Nature.

[43]  Tobias Bonhoeffer,et al.  Area-Specific Mapping of Binocular Disparity across Mouse Visual Cortex , 2019, Current Biology.

[44]  O. Blanke,et al.  Peripersonal space as the space of the bodily self , 2015, Cognition.

[45]  H. Ehrsson,et al.  Multisensory Representation of the Space Near the Hand , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[46]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[47]  D. Alais,et al.  True and Perceived Synchrony are Preferentially Associated With Particular Sensory Pairings , 2015, Scientific Reports.

[48]  Jean-Paul Noel,et al.  Audiovisual integration in depth: multisensory binding and gain as a function of distance , 2018, Experimental Brain Research.

[49]  Olaf Blanke,et al.  Neural adaptation accounts for the dynamic resizing of peripersonal space: evidence from a psychophysical-computational approach , 2018, Journal of neurophysiology.

[50]  J. Bizley The Neural Bases of Multisensory Processes , 2011 .

[51]  Gregor Thut,et al.  Auditory–Visual Multisensory Interactions in Humans: Timing, Topography, Directionality, and Sources , 2010, The Journal of Neuroscience.

[52]  S. Sterbing-D’Angelo,et al.  Behavioral/systems/cognitive Multisensory Space Representations in the Macaque Ventral Intraparietal Area , 2022 .

[53]  Mark T. Wallace,et al.  Increased Neural Strength and Reliability to Audiovisual Stimuli at the Boundary of Peripersonal Space , 2019, Journal of Cognitive Neuroscience.

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

[55]  Elisa Magosso,et al.  Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach , 2015, Front. Behav. Neurosci..

[56]  S. Nishida,et al.  Recalibration of audiovisual simultaneity , 2004, Nature Neuroscience.

[57]  Olaf Blanke,et al.  Vestibular modulation of peripersonal space boundaries , 2018, The European journal of neuroscience.

[58]  Isabelle Viaud-Delmon,et al.  Capturing the dynamics of peripersonal space by integrating expectancy effects and sound propagation properties , 2019, Journal of Neuroscience Methods.

[59]  Micah M. Murray,et al.  The Behavioral Relevance of Multisensory Neural Response Interactions , 2009, Frontiers in neuroscience.

[60]  S. Ichinose,et al.  Extension of Corticocortical Afferents into the Anterior Bank of the Intraparietal Sulcus by Tool-use Training in Adult Monkeys , 2005 .

[61]  José del R. Millán,et al.  Peri-personal space encoding in patients with disorders of consciousness and cognitive-motor dissociation , 2019, NeuroImage: Clinical.

[62]  Suliann Ben Hamed,et al.  The Prediction of Impact of a Looming Stimulus onto the Body Is Subserved by Multisensory Integration Mechanisms , 2017, The Journal of Neuroscience.

[63]  B. Herbelin,et al.  Social perception of others shapes one's own multisensory peripersonal space , 2017, Cortex.

[64]  F. Pavani,et al.  Action-specific remapping of peripersonal space , 2010, Neuropsychologia.

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

[66]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[67]  C. Gross,et al.  A neuronal representation of the location of nearby sounds , 1999, Nature.

[68]  Jonathan D. Cohen,et al.  Sequential effects: Superstition or rational behavior? , 2008, NIPS.

[69]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[70]  Matthew A. De Niear,et al.  Audiovisual Simultaneity Judgment and Rapid Recalibration throughout the Lifespan , 2016, PloS one.

[71]  Thomas Metzinger,et al.  Unconscious integration of multisensory bodily inputs in the peripersonal space shapes bodily self-consciousness , 2016, Cognition.

[72]  D. Alais,et al.  Rapid Recalibration to Audiovisual Asynchrony , 2013, The Journal of Neuroscience.

[73]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[74]  Suliann Ben Hamed,et al.  Impact Prediction by Looming Visual Stimuli Enhances Tactile Detection , 2015, The Journal of Neuroscience.

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

[76]  Tristan A. Chaplin,et al.  Cortical circuits for integration of self-motion and visual-motion signals , 2019, Current Opinion in Neurobiology.

[77]  Bettina Forster,et al.  An ERP Investigation on Visuotactile Interactions in Peripersonal and Extrapersonal Space: Evidence for the Spatial Rule , 2009, Journal of Cognitive Neuroscience.

[78]  Gian Domenico Iannetti,et al.  An Action Field Theory of Peripersonal Space , 2018, Trends in Cognitive Sciences.

[79]  Dylan F. Cooke,et al.  Sensorimotor integration in the precentral gyrus: polysensory neurons and defensive movements. , 2004, Journal of neurophysiology.

[80]  K. Yu,et al.  Rhizosphere-Associated Pseudomonas Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH , 2019, Current Biology.

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

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

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

[84]  Mauro Ursino,et al.  Neural bases of peri-hand space plasticity through tool-use: Insights from a combined computational–experimental approach , 2010, Neuropsychologia.

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

[86]  N. Van der Stoep,et al.  Audiovisual integration in near and far space: effects of changes in distance and stimulus effectiveness , 2015, Experimental Brain Research.

[87]  John J. Foxe,et al.  Multisensory contributions to low-level, ‘unisensory’ processing , 2005, Current Opinion in Neurobiology.

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

[89]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[90]  David Alais,et al.  Audiovisual temporal recalibration occurs independently at two different time scales , 2015, Scientific Reports.

[91]  Patrick Marmaroli,et al.  Body part-centered and full body-centered peripersonal space representations , 2015, Scientific Reports.

[92]  Andrew J. Doxon,et al.  Peri-personal space as a prior in coupling visual and proprioceptive signals , 2018, Scientific Reports.