The Slip Hypothesis: Tactile Perception and its Neuronal Bases

The slip hypothesis of epicritic tactile perception interprets actively moving sensor and touched objects as a frictional system, known to lead to jerky relative movements called 'slips'. These slips depend on object geometry, forces, material properties, and environmental factors, and, thus, have the power to incorporate coding of the perceptual target, as well as perceptual strategies (sensor movement). Tactile information as transferred by slips will be encoded discontinuously in space and time, because slips sometimes engage only parts of the touching surfaces and appear as discrete and rare events in time. This discontinuity may have forced tactile systems of vibrissae and fingertips to evolve special ways to convert touch signals to a tactile percept.

[1]  Garrett B. Stanley,et al.  Thalamic Synchrony and the Adaptive Gating of Information Flow to Cortex , 2010, Nature Neuroscience.

[2]  Jim Woodhouse,et al.  The Bowed String As We Know It Today , 2004 .

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

[4]  Maik C. Stüttgen,et al.  Integration of Vibrotactile Signals for Whisker-Related Perception in Rats Is Governed by Short Time Constants: Comparison of Neurometric and Psychometric Detection Performance , 2010, The Journal of Neuroscience.

[5]  M. Srinivasan,et al.  Tactile detection of slip: surface microgeometry and peripheral neural codes. , 1990, Journal of neurophysiology.

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

[7]  Robin A A Ince,et al.  Low-Dimensional Sensory Feature Representation by Trigeminal Primary Afferents , 2013, The Journal of Neuroscience.

[8]  A. M. Smith,et al.  Scopolamine increases prehensile force during object manipulation by reducing palmar sweating and decreasing skin friction , 1997, Experimental Brain Research.

[9]  A. Chateauminois,et al.  Slip dynamics at a patterned rubber/glass interface during stick-slip motions , 2012, The European Physical Journal E.

[10]  Hannes P. Saal,et al.  Millisecond Precision Spike Timing Shapes Tactile Perception , 2012, The Journal of Neuroscience.

[11]  Asaf Keller,et al.  Robust Temporal Coding in the Trigeminal System , 2004, Science.

[12]  G. Debrégeas,et al.  Effect of fingerprints orientation on skin vibrations during tactile exploration of textured surfaces , 2009, Communicative & integrative biology.

[13]  H. Witte,et al.  Structural Characterization of the Whisker System of the Rat , 2012, IEEE Sensors Journal.

[14]  K Sathian,et al.  Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Ari J. Tuononen,et al.  Digital image correlation to analyse stick-slip behaviour of tyre tread block , 2014 .

[16]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[17]  M. Hollins,et al.  The vibrations of texture , 2003, Somatosensory & motor research.

[18]  M. M. Taylor,et al.  Tactile roughness of grooved surfaces: A model and the effect of friction , 1975 .

[19]  K. O. Johnson,et al.  Monkey cutaneous SAI and RA responses to raised and depressed scanned patterns: effects of width, height, orientation, and a raised surround. , 1997, Journal of neurophysiology.

[20]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[22]  A. Volokitin,et al.  Rubber friction on smooth surfaces , 2006, The European physical journal. E, Soft matter.

[23]  Christoph Kayser,et al.  Texture signals in whisker vibrations. , 2006, Journal of neurophysiology.

[24]  W. Welker Analysis of Sniffing of the Albino Rat 1) , 1964 .

[25]  Dominik Brugger,et al.  Support for the slip hypothesis from whisker-related tactile perception of rats in a noisy environment , 2015, Front. Integr. Neurosci..

[26]  Vincent Hayward,et al.  Roughness of simulated surfaces examined with a haptic tool: effects of spatial period, friction, and resistance amplitude , 2010, Experimental Brain Research.

[27]  V. Mountcastle,et al.  Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. , 1975, Journal of neurophysiology.

[28]  Matthias Bethge,et al.  Functional analysis of ultra high information rates conveyed by rat vibrissal primary afferents , 2013, Front. Neural Circuits.

[29]  B. Berglund,et al.  Feeling Small: Exploring the Tactile Perception Limits , 2013, Scientific Reports.

[30]  Jason Wolfe,et al.  Sparse temporal coding of elementary tactile features during active whisker sensation , 2009, Nature Neuroscience.

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

[32]  Alan M. Wing,et al.  Internal models of the motor system that explain predictive grip force control , 2004 .

[33]  R. Romo,et al.  Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  Bernd Nilius,et al.  Sensing pressure with ion channels , 2012, Trends in Neurosciences.

[35]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[36]  R. Johansson,et al.  Tactile detection thresholds for a single asperity on an otherwise smooth surface. , 1983, Somatosensory research.

[37]  V. Hayward,et al.  Finger pad friction and its role in grip and touch , 2013, Journal of The Royal Society Interface.

[38]  M. Brecht,et al.  Spiking Irregularity and Frequency Modulate the Behavioral Report of Single-Neuron Stimulation , 2014, Neuron.

[39]  S J Bolanowski,et al.  Subjective magnitude of tactile roughness. , 1999, Somatosensory & motor research.

[40]  G. J. Gerling,et al.  Fingerprint lines may not directly affect SA-I mechanoreceptor response , 2008, Somatosensory & motor research.

[41]  M. Diamond,et al.  Behavioral study of whisker-mediated vibration sensation in rats , 2012, Proceedings of the National Academy of Sciences.

[42]  S. Lederman Tactile roughness of grooved surfaces: The touching process and effects of macro- and microsurface structure , 1974 .

[43]  Jean-Louis Thonnard,et al.  The cutaneous contribution to adaptive precision grip , 2004, Trends in Neurosciences.

[44]  Mark Hollins,et al.  The coding of roughness. , 2007, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[45]  Dominik Brugger,et al.  Are spatial frequency cues used for whisker-based active discrimination? , 2014, Front. Behav. Neurosci..

[46]  J. Fineberg,et al.  Visualizing stick–slip: experimental observations of processes governing the nucleation of frictional sliding , 2009 .

[47]  Ellen A Lumpkin,et al.  Mammalian touch catches up , 2015, Current Opinion in Neurobiology.

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

[49]  Maik C. Stüttgen,et al.  Psychophysical and neurometric detection performance under stimulus uncertainty , 2008, Nature Neuroscience.

[50]  A. Fairhall,et al.  Shifts in Coding Properties and Maintenance of Information Transmission during Adaptation in Barrel Cortex , 2007, PLoS biology.

[51]  Maiju Aikala,et al.  Tactile perception : Finger friction, surface roughness and perceived coarseness , 2011 .

[52]  J. Fineberg,et al.  Slip-stick and the evolution of frictional strength , 2010, Nature.

[53]  M. Hollins,et al.  Evidence for the duplex theory of tactile texture perception , 2000, Perception & psychophysics.

[54]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[55]  E. Ahissar,et al.  Temporal and Spatial Characteristics of Vibrissa Responses to Motor Commands , 2010, The Journal of Neuroscience.

[56]  D. Feldman,et al.  Texture coding in the whisker system , 2010, Current Opinion in Neurobiology.

[57]  Garrett B. Stanley,et al.  The Adaptive Trade-Off between Detection and Discrimination in Cortical Representations and Behavior , 2014, Neuron.

[58]  Daniel N. Hill,et al.  Texture Coding in the Rat Whisker System: Slip-Stick Versus Differential Resonance , 2008, PLoS biology.

[59]  J. Gibson Observations on active touch. , 1962, Psychological review.

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

[61]  A. Engel,et al.  High-Frequency Whisker Vibration Is Encoded by Phase-Locked Responses of Neurons in the Rat's Barrel Cortex , 2008, The Journal of Neuroscience.

[62]  M. Diamond,et al.  Neuronal Encoding of Texture in the Whisker Sensory Pathway , 2005, PLoS biology.

[63]  M. Brecht,et al.  Sparse and powerful cortical spikes , 2010, Current Opinion in Neurobiology.

[64]  M. Andermann,et al.  Embodied Information Processing: Vibrissa Mechanics and Texture Features Shape Micromotions in Actively Sensing Rats , 2008, Neuron.

[65]  David Golomb,et al.  Tapered whiskers are required for active tactile sensation , 2013, eLife.

[66]  Ehud Ahissar,et al.  Importance of Temporal Cues for Tactile Spatial- Frequency Discrimination , 2001, The Journal of Neuroscience.

[67]  Roland Bennewitz,et al.  Dynamic strain measurements in a sliding microstructured contact , 2008 .

[68]  D. Katz Der Aufbau der Tastwelt , 1925 .

[69]  B. Bhushan,et al.  Introduction to Tribology , 2002 .

[70]  Philippe Lefèvre,et al.  Surface strain measurements of fingertip skin under shearing , 2016, Journal of The Royal Society Interface.

[71]  Vincent Hayward,et al.  Spatio-temporal skin strain distributions evoke low variability spike responses in cuneate neurons , 2014, Journal of The Royal Society Interface.

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

[73]  R. Romo,et al.  Neural codes for perceptual discrimination in primary somatosensory cortex , 2005, Nature Neuroscience.

[74]  S. Panzeri,et al.  Diverse and Temporally Precise Kinetic Feature Selectivity in the VPm Thalamic Nucleus , 2008, Neuron.

[75]  Hannes P. Saal,et al.  Spatial and temporal codes mediate the tactile perception of natural textures , 2014, 2014 IEEE Haptics Symposium (HAPTICS).

[76]  D. Simons,et al.  Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. , 1990, Somatosensory & motor research.

[77]  M. Brecht,et al.  Functional architecture of the mystacial vibrissae , 1997, Behavioural Brain Research.

[78]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[79]  C. E. Chapman,et al.  Role of friction and tangential force variation in the subjective scaling of tactile roughness , 2002, Experimental Brain Research.

[80]  R. Johansson,et al.  Tactile sensory coding in the glabrous skin of the human hand , 1983, Trends in Neurosciences.

[81]  Joseph H. Solomon,et al.  The Morphology of the Rat Vibrissal Array: A Model for Quantifying Spatiotemporal Patterns of Whisker-Object Contact , 2011, PLoS Comput. Biol..

[82]  Kenneth O. Johnson,et al.  Neural Coding Mechanisms Underlying Perceived Roughness of Finely Textured Surfaces , 2001, The Journal of Neuroscience.

[83]  Kenneth O. Johnson,et al.  Neural Mechanisms of Tactual form and Texture Perception , 1992 .

[84]  T. Gerdjikov,et al.  Discrimination of Vibrotactile Stimuli in the Rat Whisker System: Behavior and Neurometrics , 2010, Neuron.

[85]  G. Debrégeas,et al.  The Role of Fingerprints in the Coding of Tactile Information Probed with a Biomimetic Sensor , 2009, Science.

[86]  Dominik Brugger,et al.  Vibrotactile Discrimination in the Rat Whisker System is Based on Neuronal Coding of Instantaneous Kinematic Cues , 2013, Cerebral cortex.

[87]  Philippe Lefèvre,et al.  Dynamics of fingertip contact during the onset of tangential slip , 2014, Journal of The Royal Society Interface.

[88]  W. Brace,et al.  Stick-Slip as a Mechanism for Earthquakes , 1966, Science.

[89]  N. Cauna Nature and functions of the papillary ridges of the digital skin , 1954, The Anatomical record.