Remapping nociceptive stimuli into a peripersonal reference frame is spatially locked to the stimulated limb

ABSTRACT The localization of harmful stimuli approaching our body is essential for survival. Here we investigated whether the mapping of nociceptive stimuli is based on a spatial representation that is anchored to the stimulated limb. In three experiments, we measured the effect of unilateral visual stimuli on the perceived temporal order of nociceptive stimuli, applied to each hand. Crucially, the position of the hands and the visual stimuli was manipulated, so that visual and nociceptive stimuli occurred in an adjacent or non‐adjacent spatial position. Temporal order judgments of nociceptive stimuli were biased in favor of the stimulus applied to the hand most adjacent to the visual stimulus, irrespective to their positions in space. This suggests that the ability to determine the position of a nociceptive stimulus on a specific body area is based on a peripersonal representation of the stimulated limb following it during limb displacement. HIGHLIGHTSThree temporal order judgment tasks with visual cues and nociceptive targets were conducted.Both the position of the visual stimuli and the position of the nociceptive stimuli was manipulated.Visual and nociceptive stimuli occurred in an adjacent or non‐adjacent spatial position.Judgments were biased towards the stimulus applied to the hand most adjacent to the visual stimulus.Nociceptive stimuli are mapped in a reference frame spatially locked to a specific body area.

[1]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[2]  C. Maier,et al.  Severity and specificity of neglect-like symptoms in patients with complex regional pain syndrome (CRPS) compared to chronic limb pain of other origins , 2006, Pain.

[3]  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.

[4]  A. Mouraux,et al.  Low intensity intra-epidermal electrical stimulation can activate Aδ-nociceptors selectively , 2010, PAIN.

[5]  C. Gross,et al.  From eye to hand , 1995 .

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

[7]  Giuseppe di Pellegrino,et al.  Neuropsychological Evidence of an Integrated Visuotactile Representation of Peripersonal Space in Humans , 1998, Journal of Cognitive Neuroscience.

[8]  R. Allan Reese,et al.  Linear Mixed Models: a Practical Guide using Statistical Software , 2008 .

[9]  Alessandro Farnè,et al.  Neuropsychological evidence of modular organization of the near peripersonal space , 2005, Neurology.

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

[11]  Charles Spence,et al.  Space-based, but not arm-based, shift in tactile processing in complex regional pain syndrome and its relationship to cooling of the affected limb. , 2009, Brain : a journal of neurology.

[12]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

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

[14]  M. Kenward,et al.  Small sample inference for fixed effects from restricted maximum likelihood. , 1997, Biometrics.

[15]  G. Crombez,et al.  When you dislike patients, pain is taken less seriously , 2011, PAIN®.

[16]  V. Legrain,et al.  Using temporal order judgments to investigate attention bias toward pain and threat-related information. Methodological and theoretical issues , 2016, Consciousness and Cognition.

[17]  Andrea Serino,et al.  Dynamic Size-Change of Peri-Hand Space Following Tool-Use: Determinants and Spatial Characteristics Revealed Through Cross-Modal Extinction , 2007, Cortex.

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

[19]  C. Spence,et al.  Mapping nociceptive stimuli in a peripersonal frame of reference: Evidence from a temporal order judgment task , 2014, Neuropsychologia.

[20]  C. Spence,et al.  Multisensory integration and the body schema: close to hand and within reach , 2003, Current Biology.

[21]  V. Legrain,et al.  Cognitive psychology and neuropsychology of nociception and pain , 2015 .

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

[23]  Jon Driver,et al.  Attentional competition between modalities: extinction between touch and vision after right hemisphere damage , 1997, Neuropsychologia.

[24]  Gian Domenico Iannetti,et al.  Spatially defined modulation of skin temperature and hand ownership of both hands in patients with unilateral complex regional pain syndrome. , 2012, Brain : a journal of neurology.

[25]  Y. Rossetti,et al.  Pain, body, and space: What do patients with complex regional pain syndrome really neglect? , 2012, PAIN®.

[26]  Nadia Bolognini,et al.  Dynamic expansion of alert responses to incoming painful stimuli following tool use , 2015, Neuropsychologia.

[27]  H. Vertommen,et al.  The McGill Pain Questionnaire constructed for the Dutch language (MPQ-DV). Preliminary data concerning reliability and validity , 1987, Pain.

[28]  André Mouraux,et al.  Thermal Detection Thresholds of Aδ- and C-Fibre Afferents Activated by Brief CO2 Laser Pulses Applied onto the Human Hairy Skin , 2012, PloS one.

[29]  Alessandro Farnè,et al.  Peripersonal Space and Body Schema: Two Labels for the Same Concept? , 2009, Brain Topography.

[30]  R. Rafal,et al.  Derangement of body representation in complex regional pain syndrome: report of a case treated with mirror and prisms , 2009, Experimental Brain Research.

[31]  P. Haggard,et al.  Spatial Sensory Organization and Body Representation in Pain Perception , 2013, Current Biology.

[32]  C. Spence,et al.  Multisensory prior entry. , 2001, Journal of experimental psychology. General.

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

[34]  Koji Inui,et al.  Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans. , 2006, Cerebral cortex.

[35]  A. Aron,et al.  Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex , 2010, Proceedings of the National Academy of Sciences.

[36]  B. Galer,et al.  Case reports and hypothesis: a neglect-like syndrome may be responsible for the motor disturbance in reflex sympathetic dystrophy (Complex Regional Pain Syndrome-1). , 1995, Journal of pain and symptom management.

[37]  S. Miyauchi,et al.  Pathologic pain distorts visuospatial perception , 2007, Neurology.

[38]  G. Kitagawa,et al.  Akaike Information Criterion Statistics , 1988 .

[39]  E. Chudler,et al.  Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. , 1994, Journal of neurophysiology.

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

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

[42]  G. Crombez,et al.  From a Somatotopic to a Spatiotopic Frame of Reference for the Localization of Nociceptive Stimuli , 2015, PloS one.

[43]  G. Kitagawa,et al.  Akaike Information Criterion Statistics , 1988 .

[44]  C. Spence,et al.  Spatial constraints on visual-tactile cross-modal distractor congruency effects , 2004, Cognitive, affective & behavioral neuroscience.

[45]  C. McCabe,et al.  Body perception disturbance: A contribution to pain in complex regional pain syndrome (CRPS) , 2007, PAIN®.

[46]  C. Spence,et al.  Does the sight of physical threat induce a tactile processing bias? Modality-specific attentional facilitation induced by viewing threatening pictures , 2009, Brain Research.

[47]  André Mouraux,et al.  Short trains of intra-epidermal electrical stimulation to elicit reliable behavioral and electrophysiological responses to the selective activation of nociceptors in humans , 2014, Neuroscience Letters.