Global Tactile Coding in Rat Barrel Cortex in the Absence of Local Cues

Although whisker-related perception is based predominantly on local, near-instantaneous coding, global, intensive coding, which integrates the vibrotactile signal over time, has also been shown to play a role given appropriate behavioral conditions. Here, we study global coding in isolation by studying head-fixed rats that identified pulsatile stimuli differing in pulse frequency but not in pulse waveforms, thus abolishing perception based on local coding. We quantified time locking and spike counts as likely variables underpinning the 2 coding schemes. Both neurometric variables contained substantial stimulus information, carried even by spikes of single barrel cortex neurons. To elucidate which type of information is actually used by the rats, we systematically compared psychometric with neurometric sensitivity based on the 2 coding schemes. Neurometric performance was calculated by using a population-encoding model incorporating the properties of our recorded neuron sample. We found that sensitivity calculated from spike counts sampled over long periods (>1 s) matched the performance of rats better than the one carried by spikes time-locked to the stimulus. We conclude that spike counts are more relevant to tactile perception when instantaneous kinematic parameters are not available.

[1]  Paul R. Schrater,et al.  Auditory Frequency and Intensity Discrimination Explained Using a Cortical Population Rate Code , 2013, PLoS Comput. Biol..

[2]  Anders Dale,et al.  Band-pass response properties of rat SI neurons. , 2003, Journal of neurophysiology.

[3]  W. Schiff,et al.  Tactual Perception: A Source Book , 1983 .

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

[5]  Frank Jäkel,et al.  Mapping Spikes to Sensations , 2011, Front. Neurosci..

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

[7]  Cornelius Schwarz,et al.  The Slip Hypothesis: Tactile Perception and its Neuronal Bases , 2016, Trends in Neurosciences.

[8]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

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

[10]  Maik C. Stüttgen,et al.  The Head-fixed Behaving Rat—Procedures and Pitfalls , 2010, Somatosensory & motor research.

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

[12]  H. Barlow Vision: A computational investigation into the human representation and processing of visual information: David Marr. San Francisco: W. H. Freeman, 1982. pp. xvi + 397 , 1983 .

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

[14]  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.

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

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

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

[18]  M. Diamond,et al.  Encoding of Whisker Vibration by Rat Barrel Cortex Neurons: Implications for Texture Discrimination , 2003, The Journal of Neuroscience.

[19]  W S Rhode Cochlear mechanics. , 1984, Annual review of physiology.

[20]  D J Simons,et al.  Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. , 2004, Journal of neurophysiology.

[21]  G. Madden,et al.  Impulsive choice and pre-exposure to delays: III. Four-month test-retest outcomes in male wistar rats , 2016, Behavioural Processes.

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

[23]  M. Diamond,et al.  Complementary Contributions of Spike Timing and Spike Rate to Perceptual Decisions in Rat S1 and S2 Cortex , 2015, Current Biology.

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

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

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

[27]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. Deschenes,et al.  The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway , 2003, The Journal of Neuroscience.

[29]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[30]  B. Heller Circular Statistics in Biology, Edward Batschelet. Academic Press, London & New York (1981), 371, Price $69.50 , 1983 .

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

[32]  C. Schwarz,et al.  Functional unity of the ponto-cerebellum: evidence that intrapontine communication is mediated by a reciprocal loop with the cerebellar nuclei. , 2006, Journal of neurophysiology.

[33]  Gert Cauwenberghs,et al.  Neuromorphic Silicon Neuron Circuits , 2011, Front. Neurosci.

[34]  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.

[35]  H Stanislaw,et al.  Calculation of signal detection theory measures , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

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

[37]  David P Jarmolowicz,et al.  Changing delay discounting in the light of the competing neurobehavioral decision systems theory: a review. , 2013, Journal of the experimental analysis of behavior.

[38]  Ned Jenkinson,et al.  Stimulus Frequency Processing in Awake Rat Barrel Cortex , 2006, The Journal of Neuroscience.

[39]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

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

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

[42]  M. Goldberg,et al.  Memory-Guided Saccade to a Distractor Flashed During the Delay Period of a Response of Neurons in the Lateral Intraparietal Area , 2015 .

[43]  M. Abeles Quantification, smoothing, and confidence limits for single-units' histograms , 1982, Journal of Neuroscience Methods.

[44]  F. Haiss,et al.  A miniaturized chronic microelectrode drive for awake behaving head restrained mice and rats , 2010, Journal of Neuroscience Methods.

[45]  Refractor Vision , 2000, The Lancet.

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

[47]  Maik C. Stüttgen,et al.  Two Psychophysical Channels of Whisker Deflection in Rats Align with Two Neuronal Classes of Primary Afferents , 2006, The Journal of Neuroscience.

[48]  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.

[49]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

[50]  Nicholas I. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

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

[52]  J. Goldberg,et al.  Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. , 1968, Journal of neurophysiology.

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

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

[55]  Gregory Telian,et al.  Short Time-Scale Sensory Coding in S1 during Discrimination of Whisker Vibrotactile Sequences , 2016, PLoS biology.

[56]  Justin A. Harris,et al.  Factors Affecting Frequency Discrimination of Vibrotactile Stimuli: Implications for Cortical Encoding , 2006, PloS one.

[57]  Martin Bogdan,et al.  Employing ICA and SOM for spike sorting of multielectrode recordings from CNS , 2004, Journal of Physiology-Paris.

[58]  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.

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

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

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