Peripersonal space representation develops independently from visual experience

Our daily-life actions are typically driven by vision. When acting upon an object, we need to represent its visual features (e.g. shape, orientation, etc.) and to map them into our own peripersonal space. But what happens with people who have never had any visual experience? How can they map object features into their own peripersonal space? Do they do it differently from sighted agents? To tackle these questions, we carried out a series of behavioral experiments in sighted and congenitally blind subjects. We took advantage of a spatial alignment effect paradigm, which typically refers to a decrease of reaction times when subjects perform an action (e.g., a reach-to-grasp pantomime) congruent with that afforded by a presented object. To systematically examine peripersonal space mapping, we presented visual or auditory affording objects both within and outside subjects’ reach. The results showed that sighted and congenitally blind subjects did not differ in mapping objects into their own peripersonal space. Strikingly, this mapping occurred also when objects were presented outside subjects’ reach, but within the peripersonal space of another agent. This suggests that (the lack of) visual experience does not significantly affect the development of both one’s own and others’ peripersonal space representation.

[1]  Giacomo Rizzolatti,et al.  The mirror mechanism: a basic principle of brain function , 2016, Nature Reviews Neuroscience.

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

[3]  P. Pietrini,et al.  Spatial imagery relies on a sensory independent, though sensory sensitive, functional organization within the parietal cortex: A fMRI study of angle discrimination in sighted and congenitally blind individuals , 2015, Neuropsychologia.

[4]  Hiroaki Ishida,et al.  Shared Mapping of Own and Others' Bodies in Visuotactile Bimodal Area of Monkey Parietal Cortex , 2010, Journal of Cognitive Neuroscience.

[5]  D. Bub,et al.  Grasping beer mugs: on the dynamics of alignment effects induced by handled objects. , 2010, Journal of experimental psychology. Human perception and performance.

[6]  Emiliano Ricciardi,et al.  Are Supramodality and Cross-Modal Plasticity the Yin and Yang of Brain Development? From Blindness to Rehabilitation , 2016, Front. Syst. Neurosci..

[7]  Gaetano Tieri,et al.  Where does an object trigger an action? An investigation about affordances in space , 2010, Experimental Brain Research.

[8]  Jason W. Osborne,et al.  The power of outliers (and why researchers should ALWAYS check for them) , 2004 .

[9]  M. Proulx,et al.  Visual experience facilitates allocentric spatial representation , 2013, Behavioural Brain Research.

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

[11]  Elizabeth J. Saccone,et al.  Explicit spatial compatibility is not critical to the object handle effect. , 2016, Journal of experimental psychology. Human perception and performance.

[12]  Maurizio Ferrarin,et al.  Bisecting Lines with Different Tools in Right Brain Damaged Patients: The Role of Action Programming and Sensory Feedback in Modulating Spatial Remapping , 2007, Cortex.

[13]  C. Thinus-Blanc,et al.  Representation of space in blind persons: vision as a spatial sense? , 1997, Psychological bulletin.

[14]  Luigi Cattaneo,et al.  Broken affordances, broken objects: A TMS study , 2009, Neuropsychologia.

[15]  Y. Rossetti,et al.  Coding of Visual Space during Motor Preparation: Approaching Objects Rapidly Modulate Corticospinal Excitability in Hand-Centered Coordinates , 2009, The Journal of Neuroscience.

[16]  M. Costantini,et al.  The space of affordances: A TMS study , 2011, Neuropsychologia.

[17]  Olivier Collignon,et al.  Embodied Space in Early Blind Individuals , 2012, Front. Psychology.

[18]  C. Spence,et al.  Developmental vision determines the reference frame for the multisensory control of action , 2007, Proceedings of the National Academy of Sciences.

[19]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[20]  G. Sandini,et al.  Impairment of auditory spatial localization in congenitally blind human subjects , 2013, Brain : a journal of neurology.

[21]  P. Pietrini,et al.  Mind the blind brain to understand the sighted one! Is there a supramodal cortical functional architecture? , 2014, Neuroscience & Biobehavioral Reviews.

[22]  V. Gallese,et al.  When a laser pen becomes a stick: remapping of space by tool-use observation in hemispatial neglect , 2014, Experimental Brain Research.

[23]  G. Pellegrino,et al.  Peripersonal space in the brain , 2015, Neuropsychologia.

[24]  Andrea Serino,et al.  Suppression of premotor cortex disrupts motor coding of peripersonal space , 2012, NeuroImage.

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

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

[27]  A. Kappers,et al.  Differences between Early-Blind, Late-Blind, and Blindfolded-Sighted People in Haptic Spatial-Configuration Learning and Resulting Memory Traces , 2007, Perception.

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

[29]  Glyn W Humphreys,et al.  Widening the Sphere of Influence: Using a Tool to Extend Extrapersonal Visual Space in a Patient with Severe Neglect , 2002, Neurocase.

[30]  A. Serino,et al.  Motor Properties of Peripersonal Space in Humans , 2009, PloS one.

[31]  T Landis,et al.  So near yet so far: Neglect in far or near space depends on tool use , 2001, Annals of neurology.

[32]  Comparative study of simple auditory reaction time in blind and blindfolded sighted individuals , 2017 .

[33]  C. Spence,et al.  Tool-use changes multimodal spatial interactions between vision and touch in normal humans , 2002, Cognition.

[34]  L. Rönnqvist,et al.  Early influence of auditory stimuli on upper-limb movements in young human infants: an overview , 2014, Front. Psychol..

[35]  R J Ilmoniemi,et al.  Electrophysiological evidence for cross-modal plasticity in humans with early- and late-onset blindness. , 1997, Psychophysiology.

[36]  Monica Gori,et al.  Intercepting a sound without vision , 2017, PloS one.

[37]  Á. Pascual-Leone,et al.  Spatial biases in peripersonal space in sighted and blind individuals revealed by a haptic line bisection paradigm. , 2011, Journal of experimental psychology. Human perception and performance.

[38]  Yale E. Cohen,et al.  A common reference frame for movement plans in the posterior parietal cortex , 2002, Nature Reviews Neuroscience.

[39]  Alfonso Caramazza,et al.  Cross-modal plasticity preserves functional specialization in posterior parietal cortex. , 2014, Cerebral cortex.

[40]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[41]  Matthijs L. Noordzij,et al.  The influence of visual experience on the ability to form spatial mental models based on route and survey descriptions , 2006, Cognition.

[42]  A. Iriki,et al.  Acquisition and development of monkey tool-use: behavioral and kinematic analyses. , 2000, Canadian journal of physiology and pharmacology.

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

[44]  M. Bassolino,et al.  PSYCHOLOGICAL SCIENCE Research Article Extended Multisensory Space in Blind Cane Users , 2022 .

[45]  F. Rösler,et al.  The human dorsal action control system develops in the absence of vision. , 2009, Cerebral cortex.

[46]  V. Gallese,et al.  Tool-use observation makes far objects ready-to-hand , 2011, Neuropsychologia.

[47]  Andrea Serino,et al.  Moving sounds within the peripersonal space modulate the motor system , 2015, Neuropsychologia.

[48]  Alessandro Livi,et al.  Ventral Premotor Neurons Encoding Representations of Action during Self and Others’ Inaction , 2014, Current Biology.

[49]  M. Lassonde,et al.  Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects , 2008, Experimental Brain Research.

[50]  L. Fogassi,et al.  Functional properties of grasping-related neurons in the ventral premotor area F5 of the macaque monkey. , 2006, Journal of neurophysiology.

[51]  P. Pietrini,et al.  New light from the dark: what blindness can teach us about brain function. , 2011, Current opinion in neurology.

[52]  Giorgia Committeri,et al.  Ready Both to Your and to My Hands: Mapping the Action Space of Others , 2011, PloS one.

[53]  Luciano Fadiga,et al.  Beyond Motor Scheme: A Supramodal Distributed Representation in the Action-Observation Network , 2013, PloS one.

[54]  O. Collignon,et al.  Further evidence that congenitally blind participants react faster to auditory and tactile spatial targets. , 2009, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[55]  Luciano Fadiga,et al.  Do We Really Need Vision? How Blind People “See” the Actions of Others , 2009, The Journal of Neuroscience.

[56]  A. Berti,et al.  When Far Becomes Near: Remapping of Space by Tool Use , 2000, Journal of Cognitive Neuroscience.

[57]  Emiliano Ricciardi,et al.  The blind brain: How (lack of) vision shapes the morphological and functional architecture of the human brain , 2014, Experimental biology and medicine.

[58]  Marcello Costantini,et al.  Grasping affordances with the other's hand: a TMS study. , 2013, Social cognitive and affective neuroscience.

[59]  P. Pietrini,et al.  Imagery and spatial processes in blindness and visual impairment , 2008, Neuroscience & Biobehavioral Reviews.