Fast and accurate edge orientation processing during object manipulation

Quickly and accurately extracting information about a touched object’s orientation is a critical aspect of dexterous object manipulation. However, the speed and acuity of tactile edge orientation processing with respect to the fingertips as reported in previous perceptual studies appear inadequate in these respects. Here we directly establish the tactile system’s capacity to process edge-orientation information during dexterous manipulation. Participants extracted tactile information about edge orientation very quickly, using it within 200 ms of first touching the object. Participants were also strikingly accurate. With edges spanning the entire fingertip, edge-orientation resolution was better than 3° in our object manipulation task, which is several times better than reported in previous perceptual studies. Performance remained impressive even with edges as short as 2 mm, consistent with our ability to precisely manipulate very small objects. Taken together, our results radically redefine the spatial processing capacity of the tactile system.

[1]  A. Canedo PRIMARY MOTOR CORTEX INFLUENCES ON THE DESCENDING AND ASCENDING SYSTEMS , 1997, Progress in Neurobiology.

[2]  R. Johansson Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. , 1978, The Journal of physiology.

[3]  E. Friedman,et al.  Temporal processing. , 1991, Journal of learning disabilities.

[4]  Claudio Brozzoli,et al.  Peripersonal space : a multisensory interface for body-objects interactions , 2009 .

[5]  S. Manita,et al.  A Top-Down Cortical Circuit for Accurate Sensory Perception , 2015, Neuron.

[6]  A. Goodwin,et al.  Tactile resolution: peripheral neural mechanisms underlying the human capacity to determine positions of objects contacting the fingerpad , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Daniel Goldreich,et al.  Tactile orientation perception: an ideal observer analysis of human psychophysical performance in relation to macaque area 3b receptive fields. , 2015, Journal of neurophysiology.

[8]  H. Sompolinsky,et al.  Compressed sensing, sparsity, and dimensionality in neuronal information processing and data analysis. , 2012, Annual review of neuroscience.

[9]  Bruce Bridgeman,et al.  Interactions between Vision for Perception and Vision for Behavior , 2000 .

[10]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[11]  J. Phillips,et al.  Responses of human mechanoreceptive afferents to embossed dot arrays scanned across fingerpad skin , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  N. Cauna,et al.  Nerve supply and nerve endings in Meissner's corpuscles. , 1956, The American journal of anatomy.

[13]  E P Gardner,et al.  Simulation of motion on the skin. I. Receptive fields and temporal frequency coding by cutaneous mechanoreceptors of OPTACON pulses delivered to the hand. , 1989, Journal of neurophysiology.

[14]  G. Orban,et al.  Human orientation discrimination tested with long stimuli , 1984, Vision Research.

[15]  Maria Nolano,et al.  Quantification of myelinated endings and mechanoreceptors in human digital skin , 2003, Annals of neurology.

[16]  J. Loomis,et al.  Sensitivity to shifts of a point stimulus: An instance of tactile hyperacuity , 1978, Perception & psychophysics.

[17]  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.

[18]  D. Wolpert,et al.  Perception of the Consequences of Self-Action Is Temporally Tuned and Event Driven , 2005, Current Biology.

[19]  David Cai,et al.  Sparsity and Compressed Coding in Sensory Systems , 2014, PLoS Comput. Biol..

[20]  M. D. Goldfinger,et al.  Random-sequence stimulation of the G1 hair afferent unit. , 1990, Somatosensory & motor research.

[21]  Response of cat cutaneous mechanoreceptors to punctate and grating stimuli. , 1986, Journal of neurophysiology.

[22]  Karl J. Friston,et al.  Predictions not commands: active inference in the motor system , 2012, Brain Structure and Function.

[23]  A. Iggo,et al.  A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit , 1967, The Journal of physiology.

[24]  R. Johansson,et al.  Spatial properties of the population of mechanoreceptive units in the glabrous skin of the human hand , 1980, Brain Research.

[25]  E. Lechelt,et al.  Tactile spatial anisotropy with static stimulation , 1992 .

[26]  M. Sommer,et al.  Corollary discharge across the animal kingdom , 2008, Nature Reviews Neuroscience.

[27]  Aneesha K. Suresh,et al.  Edge orientation signals in tactile afferents of macaques. , 2016, Journal of neurophysiology.

[28]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[29]  E. Candès,et al.  Stable signal recovery from incomplete and inaccurate measurements , 2005, math/0503066.

[30]  J. A. Pruszynski,et al.  Edge-orientation processing in first-order tactile neurons , 2014, Nature Neuroscience.

[31]  H. Burton,et al.  Discrimination of vibrotactile frequencies in a delayed pair comparison task , 1996, Perception & psychophysics.

[32]  Joshua M Rosenow,et al.  Methodological considerations for a chronic neural interface with the cuneate nucleus of macaques. , 2017, Journal of neurophysiology.

[33]  G. Stanley Reading and writing the neural code , 2013, Nature Neuroscience.

[34]  Robert M Friedman,et al.  Neural Coding of the Location and Direction of a Moving Object by a Spatially Distributed Population of Mechanoreceptors , 2002, The Journal of Neuroscience.

[35]  Emilio Salinas,et al.  Transformation of the neural code for tactile detection from thalamus to cortex , 2013, Proceedings of the National Academy of Sciences.

[36]  D. Simons,et al.  Motor modulation of afferent somatosensory circuits , 2008, Nature Neuroscience.

[37]  R. Johansson,et al.  Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. , 1984, Human neurobiology.

[38]  W. Usrey The role of spike timing for thalamocortical processing , 2002, Current Opinion in Neurobiology.

[39]  Peter Lakatos,et al.  Dynamics of Active Sensing and perceptual selection , 2010, Current Opinion in Neurobiology.

[40]  A. E. Casale,et al.  Motor Cortex Feedback Influences Sensory Processing by Modulating Network State , 2013, Neuron.

[41]  Benoit P. Delhaye,et al.  Simulating tactile signals from the whole hand with millisecond precision , 2017, Proceedings of the National Academy of Sciences.

[42]  V. Hayward,et al.  Segregation of Tactile Input Features in Neurons of the Cuneate Nucleus , 2014, Neuron.

[43]  E.J. Candes,et al.  An Introduction To Compressive Sampling , 2008, IEEE Signal Processing Magazine.

[44]  M. Paré,et al.  Distribution and terminal arborizations of cutaneous mechanoreceptors in the glabrous finger pads of the monkey , 2002, The Journal of comparative neurology.

[45]  J Andrew Pruszynski,et al.  Neural network models of the tactile system develop first-order units with spatially complex receptive fields , 2017, bioRxiv.

[46]  N. Cauna,et al.  The mode of termination of the sensory nerves and its significance , 1959, The Journal of comparative neurology.

[47]  A B Vallbo,et al.  Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. , 1995, The Journal of physiology.

[48]  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.

[49]  D. Pins,et al.  On the relation between stimulus intensity and processing time: Piéron’s law and choice reaction time , 1996, Perception & psychophysics.

[50]  D. Tapper,et al.  Integration of impulse activity in a peripheral sensory unit. , 1966, Experimental neurology.

[51]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[52]  J. Randall Flanagan,et al.  A Rapid Tactile-Motor Reflex Automatically Guides Reaching toward Handheld Objects , 2016, Current Biology.

[53]  A. Goodwin,et al.  Peripheral Neural Mechanisms Determining the Orientation of Cylinders Grasped by the Digits , 1998, The Journal of Neuroscience.

[54]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[55]  L. Weiskrantz Blindsight revisited , 1996, Current Opinion in Neurobiology.

[56]  BlakemoreSarah-J.,et al.  Spatio-Temporal Prediction Modulates the Perception of Self-Produced Stimuli , 1999 .

[57]  M. Goodale,et al.  The visual brain in action , 1995 .

[58]  T. Sejnowski,et al.  Temporal Processing in the Olfactory System: Can We See a Smell? , 2013, Neuron.

[59]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[60]  A. Nobre,et al.  Top-down modulation: bridging selective attention and working memory , 2012, Trends in Cognitive Sciences.

[61]  W. Singer,et al.  Integrator or coincidence detector? The role of the cortical neuron revisited , 1996, Trends in Neurosciences.

[62]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[63]  E. Moberg,et al.  Objective methods for determining the functional value of sensibility in the hand. , 1958, The Journal of bone and joint surgery. British volume.

[64]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[65]  Scott T. Grafton,et al.  Forward modeling allows feedback control for fast reaching movements , 2000, Trends in Cognitive Sciences.

[66]  L. Dahlin,et al.  Consequences and adaptation in daily life – patients’ experiences three decades after a nerve injury sustained in adolescence , 2013, BMC Musculoskeletal Disorders.

[67]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[68]  J M Loomis,et al.  An investigation of tactile hyperacuity. , 1979, Sensory processes.

[69]  Yves Rossetti,et al.  Beyond dissociation : interaction between dissociated implicit and explicit processing , 2000 .

[70]  Yoshichika Baba,et al.  Computation identifies structural features that govern neuronal firing properties in slowly adapting touch receptors , 2014, eLife.

[71]  R. Johansson,et al.  Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip , 2004, Experimental Brain Research.

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

[73]  D. Wolpert,et al.  Spatio-Temporal Prediction Modulates the Perception of Self-Produced Stimuli , 1999, Journal of Cognitive Neuroscience.

[74]  M. Srinivasan,et al.  Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors. , 1998, Journal of neurophysiology.

[75]  Charles Spence,et al.  The cognitive and neural correlates of tactile memory. , 2009, Psychological bulletin.

[76]  E. G. Jones,et al.  Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. , 2000, Annual review of neuroscience.

[77]  M. Diamond,et al.  The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex , 2001, Neuron.

[78]  Gerald Westheimer,et al.  Optical superresolution and visual hyperacuity , 2012, Progress in Retinal and Eye Research.

[79]  J C Craig,et al.  The tactile perception of stimulus orientation , 2008, Somatosensory & motor research.