Elementary motion sequence detectors in whisker somatosensory cortex

How the somatosensory cortex (S1) encodes complex patterns of touch, such as those that occur during tactile exploration, is poorly understood. In the mouse whisker S1, temporally dense stimulation of local whisker pairs revealed that most neurons are not classical single-whisker feature detectors, but instead are strongly tuned to two-whisker sequences that involve the columnar whisker (CW) and one specific surround whisker (SW), usually in a SW-leading-CW order. Tuning was spatiotemporally precise and diverse across cells, generating a rate code for local motion vectors defined by SW–CW combinations. Spatially asymmetric, sublinear suppression for suboptimal combinations and near-linearity for preferred combinations sharpened combination tuning relative to linearly predicted tuning. This resembles computation of motion direction selectivity in vision. SW-tuned neurons, misplaced in the classical whisker map, had the strongest combination tuning. Thus, each S1 column contains a rate code for local motion sequences involving the CW, thus providing a basis for higher-order feature extraction.Laboy-Juárez et al. show that barrel cortex neurons in mice are tuned for elementary multi-whisker sequences that represent tactile motion, using a computation similar to motion direction selectivity in vision. These findings provide a novel view of columnar organization.

[1]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[2]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. , 1986, Journal of neurophysiology.

[3]  B. Sakmann,et al.  Depletion of calcium in the synaptic cleft of a calyx‐type synapse in the rat brainstem , 1999, The Journal of physiology.

[4]  J. Poulet,et al.  Synaptic Mechanisms Underlying Sparse Coding of Active Touch , 2011, Neuron.

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

[6]  Partha P. Mitra,et al.  Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability , 1996, Journal of Neuroscience Methods.

[7]  M A Nicolelis,et al.  Nonlinear processing of tactile information in the thalamocortical loop. , 1997, Journal of neurophysiology.

[8]  D. Shulz,et al.  Spatial structure of multiwhisker receptive fields in the barrel cortex is stimulus dependent. , 2011, Journal of neurophysiology.

[9]  Houman Safaai,et al.  Coordinated Population Activity Underlying Texture Discrimination in Rat Barrel Cortex , 2013, The Journal of Neuroscience.

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

[11]  Dan D. Stettler,et al.  Representations of Odor in the Piriform Cortex , 2009, Neuron.

[12]  M. Diamond,et al.  Integration of multiple-whisker inputs in rat somatosensory cortex. , 2001, Cerebral cortex.

[13]  C. Welker Receptive fields of barrels in the somatosensory neocortex of the rat , 1976, The Journal of comparative neurology.

[14]  Nicholas J. Priebe,et al.  Mechanisms of Neuronal Computation in Mammalian Visual Cortex , 2012, Neuron.

[15]  Alexander Borst,et al.  Visual Circuits for Direction Selectivity. , 2017, Annual review of neuroscience.

[16]  Daniel N. Hill,et al.  Biomechanics of the Vibrissa Motor Plant in Rat: Rhythmic Whisking Consists of Triphasic Neuromuscular Activity , 2008, The Journal of Neuroscience.

[17]  S. Nelson,et al.  Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. , 1998, Journal of neurophysiology.

[18]  S. Shimegi,et al.  Physiological and Anatomical Organization of Multiwhisker Response Interactions in the Barrel Cortex of Rats , 2000, The Journal of Neuroscience.

[19]  Sami El Boustani,et al.  Correlated input reveals coexisting coding schemes in a sensory cortex , 2012, Nature Neuroscience.

[20]  F. Ebner,et al.  Temporal organization of multi-whisker contact in rats. , 2001, Somatosensory & motor research.

[21]  Liam Paninski,et al.  Spatiotemporal receptive fields of barrel cortex revealed by reverse correlation of synaptic input , 2014, Nature Neuroscience.

[22]  D. Simons,et al.  Thalamocortical response transformation in the rat vibrissa/barrel system. , 1989, Journal of neurophysiology.

[23]  Michael B. Reiser,et al.  Simple integration of fast excitation and offset, delayed inhibition computes directional selectivity in Drosophila , 2017, Nature Neuroscience.

[24]  Alison L. Barth,et al.  Experimental evidence for sparse firing in the neocortex , 2012, Trends in Neurosciences.

[25]  V. Ego-Stengel,et al.  Representation of Tactile Scenes in the Rodent Barrel Cortex , 2018, Neuroscience.

[26]  D J Simons,et al.  Spatial gradients and inhibitory summation in the rat whisker barrel system. , 1996, Journal of neurophysiology.

[27]  J. Poulet,et al.  Synaptic Mechanisms Underlying Sparse Coding of Active Touch , 2011, Neuron.

[28]  D. Feldman,et al.  Increased Excitation-Inhibition Ratio Stabilizes Synapse and Circuit Excitability in Four Autism Mouse Models , 2018, Neuron.

[29]  J. Schiller,et al.  NMDA spikes in basal dendrites of cortical pyramidal neurons , 2000, Nature.

[30]  Philipp Schnepel,et al.  Structure of a Single Whisker Representation in Layer 2 of Mouse Somatosensory Cortex , 2015, The Journal of Neuroscience.

[31]  D. Simons Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[32]  V. Ego-Stengel,et al.  Coding of Apparent Motion in the Thalamic Nucleus of the Rat Vibrissal Somatosensory System , 2012, The Journal of Neuroscience.

[33]  H. Sato,et al.  Temporal Characteristics of Response Integration Evoked by Multiple Whisker Stimulations in the Barrel Cortex of Rats , 1999, The Journal of Neuroscience.

[34]  Vincent Jacob,et al.  Emergent Properties of Tactile Scenes Selectively Activate Barrel Cortex Neurons , 2008, Neuron.

[35]  S. Grün,et al.  Analysis Of Parallel Spike Trains (Series: Springer Series In Computational Neuroscience, Preliminary Entry 106) , 2010 .

[36]  B. Willmore,et al.  Sparse coding in striate and extrastriate visual cortex. , 2011, Journal of neurophysiology.

[37]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.

[38]  M. Carandini,et al.  Normalization as a canonical neural computation , 2011, Nature Reviews Neuroscience.

[39]  Jackie Schiller,et al.  Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo , 2012, Nature.

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

[41]  S. Bensmaia,et al.  The neural basis of tactile motion perception. , 2014, Journal of neurophysiology.

[42]  Vincent Jacob,et al.  Spatiotemporal characteristics of neuronal sensory integration in the barrel cortex of the rat. , 2005, Journal of neurophysiology.

[43]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001 .

[44]  Robert N. S. Sachdev, Heike Sellien, Ford Ebner Temporal organization of multi-whisker contact in rats , 2001 .

[45]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[46]  Garrett B Stanley,et al.  The Dynamics of Spatiotemporal Response Integration in the Somatosensory Cortex of the Vibrissa System , 2006, The Journal of Neuroscience.

[47]  Shigeru Shinomoto,et al.  Estimating the Firing Rate , 2010 .

[48]  Matteo Carandini,et al.  Somatosensory Integration Controlled by Dynamic Thalamocortical Feed-Forward Inhibition , 2005, Neuron.

[49]  M. Hartmann,et al.  Spatiotemporal Patterns of Contact Across the Rat Vibrissal Array During Exploratory Behavior , 2016, Front. Behav. Neurosci..

[50]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[51]  T. Prescott,et al.  Active touch sensing in the rat: anticipatory and regulatory control of whisker movements during surface exploration. , 2009, Journal of neurophysiology.

[52]  Daniel E. Feldman,et al.  Slip-Based Coding of Local Shape and Texture in Mouse S1 , 2018, Neuron.

[53]  Beau Dabbs,et al.  Summary and discussion of : “ Controlling the False Discovery Rate : A Practical and Powerful Approach to Multiple Testing , 2014 .

[54]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[55]  D. Simons Temporal and spatial integration in the rat SI vibrissa cortex. , 1985, Journal of neurophysiology.

[56]  Luc Estebanez,et al.  Supra-barrel Distribution of Directional Tuning for Global Motion in the Mouse Somatosensory Cortex. , 2018, Cell reports.

[57]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[58]  Kip A Ludwig,et al.  Using a common average reference to improve cortical neuron recordings from microelectrode arrays. , 2009, Journal of neurophysiology.

[59]  Keven J. Laboy-Juárez,et al.  A normalized template matching method for improving spike detection in extracellular voltage recordings , 2018, bioRxiv.

[60]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.

[61]  Srivatsun Sadagopan,et al.  Nonlinear Spectrotemporal Interactions Underlying Selectivity for Complex Sounds in Auditory Cortex , 2009, The Journal of Neuroscience.

[62]  Zachary F. Mainen,et al.  The Functional Microarchitecture of the Mouse Barrel Cortex , 2007, PLoS Biology.