Relevance-dependent modulation of tactile suppression during active, passive and pantomime reach-to-grasp movements

HIGHLIGHTSOur ability to detect tactile events on a moving limb is reduced.Active self and passive motor‐guided movements show similar tactile suppression.Movement‐related tactile suppression can be modulated in a task‐relevant manner. ABSTRACT When we move, our ability to detect tactile events on the moving limb is reduced (e.g., movement‐related tactile suppression). This process prevents unimportant sensory information from bombarding our central nervous system. This study investigated whether movement‐related suppression can be modulated according to task relevance, while introducing a novel motor‐driven complex upper limb movement. In three experiments, participants performed volitional self‐driven and passive motor‐driven reaching and grasping movements. Over the course of the movement, weak electrical stimulation was presented at task‐relevant (i.e., index finger) and irrelevant sites (i.e., forearm) on the moving limb. In Experiment 1, participants displayed reduced detectability during movement (90% resting detection). This was true for all locations on the moving limb irrespective of task‐relevance and during both self and motor‐driven movements. In Experiments 2 and 3 a range of stimulus amplitudes were presented to one task‐relevant location during both self and motor‐driven movements (Experiment 2A), to a task‐relevant and irrelevant site (Experiment 2B) and during a targeted and pantomime/no target reach (Experiment 3). This allowed us to estimate perceptual thresholds and assess the magnitude of movement‐related suppression. During both self and motor‐driven movements participants exhibited movement‐related suppression. Suppression was greater at the irrelevant site (forearm) than at the relevant site (index finger) of the limb. Further, the magnitude of suppression varied with task relevance such that pantomime movements elicited more suppression than targeted movements. Collectively, these experiments suggest that although tactile suppression may be a general consequence of movement, suppression can be modulated in a relevance‐dependent manner.

[1]  Roger Newport,et al.  Modulation of somatosensory perception by motor intention , 2011, Cognitive neuroscience.

[2]  J. Ferris,et al.  Task-relevancy effects on movement-related gating are modulated by continuous theta-burst stimulation of the dorsolateral prefrontal cortex and primary somatosensory cortex , 2014, Experimental Brain Research.

[3]  C. E. Chapman,et al.  Differential controls over tactile detection in humans by motor commands and peripheral reafference. , 2006, Journal of neurophysiology.

[4]  Daniel Goldreich,et al.  Tactile Spatial Acuity in Childhood: Effects of Age and Fingertip Size , 2013, PloS one.

[5]  R. Knight,et al.  Gating of somatosensory input by human prefrontal cortex , 1990, Brain Research.

[6]  R. Sainburg,et al.  The effect of target modality on visual and proprioceptive contributions to the control of movement distance , 2006, Experimental Brain Research.

[7]  D. Wolpert,et al.  Mere Expectation to Move Causes Attenuation of Sensory Signals , 2008, PloS one.

[8]  C E Chapman,et al.  Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. , 1994, Canadian journal of physiology and pharmacology.

[9]  H L TEUBER,et al.  Effect of Knowledge of Site of Stimulation on the Threshold for Pressure Sensitivity , 1963, Perceptual and motor skills.

[10]  Philip N. Sabes,et al.  Flexible strategies for sensory integration during motor planning , 2005, Nature Neuroscience.

[11]  Robert T. Knight,et al.  Prefrontal cortex gating of auditory transmission in humans , 1989, Brain Research.

[12]  Katja Fiehler,et al.  Enhancement and Suppression of Tactile Signals During Reaching , 2017, Journal of experimental psychology. Human perception and performance.

[13]  J. Rothwell,et al.  Gating of somatosensory evoked potentials during different kinds of movement in man. , 1981, Brain : a journal of neurology.

[14]  C. E. Chapman,et al.  Time course and magnitude of movement-related gating of tactile detection in humans. II. Effects of stimulus intensity. , 2000, Journal of neurophysiology.

[15]  Heiner Deubel,et al.  Attention and suppression affect tactile perception in reach-to-grasp movements. , 2011, Acta psychologica.

[16]  Gavin Buckingham,et al.  Tactile gating in a reaching and grasping task , 2014, Physiological reports.

[17]  C. Ghez,et al.  Inhibition of afferent transmission in cuneate nucleus during voluntary movement in the cat. , 1972, Brain research.

[18]  Katja Fiehler,et al.  Reach-relevant somatosensory signals modulate tactile suppression. , 2017, Journal of neurophysiology.

[19]  G. Gescheider Psychophysics: The Fundamentals , 1997 .

[20]  Felix Wichmann,et al.  The psychometric function: I , 2001 .

[21]  C. E. Chapman,et al.  Time course and magnitude of movement-related gating of tactile detection in humans. III. Effect of motor tasks. , 2002, Journal of neurophysiology.

[22]  Sandra E. Black,et al.  Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System , 2002, NeuroImage.

[23]  Gavin Buckingham,et al.  Gating of vibrotactile detection during visually guided bimanual reaches , 2010, Experimental Brain Research.

[24]  Amy Parkinson,et al.  Effects of motor intention on the perception of somatosensory events: A behavioural and functional magnetic resonance imaging study , 2011, Quarterly journal of experimental psychology.

[25]  D. Wolpert,et al.  Sensorimotor attenuation by central motor command signals in the absence of movement , 2006, Nature Neuroscience.

[26]  C. Spence,et al.  Changes in tactile sensitivity over the time-course of a goal-directed movement , 2010, Behavioural Brain Research.

[27]  Kazuhiko Seki,et al.  Gating of Sensory Input at Spinal and Cortical Levels during Preparation and Execution of Voluntary Movement , 2012, The Journal of Neuroscience.

[28]  S. Jones,et al.  An 'interference" approach to the study of somatosensory evoked potentials in man. , 1981, Electroencephalography and clinical neurophysiology.

[29]  E. Fetz,et al.  Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement , 2003, Nature Neuroscience.

[30]  W. McIlroy,et al.  Task‐relevant selective modulation of somatosensory afferent paths from the lower limb , 2000, Neuroreport.

[31]  S J Bolanowski,et al.  Vibrotactile masking: effects of stimulus onset asynchrony and stimulus frequency. , 1989, The Journal of the Acoustical Society of America.

[32]  J. Botwinick,et al.  Premotor and motor components of reaction time. , 1966, Journal of experimental psychology.

[33]  C. E. Chapman,et al.  Time course and magnitude of movement-related gating of tactile detection in humans. I. Importance of stimulus location. , 1998, Journal of neurophysiology.

[34]  Francisco L Colino,et al.  Time Course of Tactile Gating in a Reach-to-Grasp and Lift Task , 2016, Journal of motor behavior.

[35]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[36]  L. Cohen,et al.  Localization, timing and specificity of gating of somatosensory evoked potentials during active movement in man. , 1987, Brain : a journal of neurology.