A somatotopic map of vibrissa motion direction within a barrel column

Most mammals possess high-resolution visual perception, with primary visual cortices containing fine-scale, inter-related feature representations (for example, orientation and ocular dominance). Rats lack precise vision, but their vibrissa sensory system provides a precise tactile modality, including vibrissa-related 'barrel' columns in primary somatosensory cortex. Here, we examined the subcolumnar organization of direction preference and somatotopy using a new omni-directional, multi-vibrissa stimulator. We discovered a direction map that was systematically linked to somatotopy, such that neurons were tuned for motion toward their preferred surround vibrissa. This sub-barrel column direction map demonstrated an emergent refinement from layer IV to layer II/III. These data suggest that joint processing of multiple sensory features is a common property of high-resolution sensory systems.

[1]  H. Head STUDIES IN NEUROLOGY , 1921 .

[2]  T. Woolsey,et al.  The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. , 1970, Brain research.

[3]  T. Woolsey,et al.  The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex , 1970 .

[4]  D. Hubel,et al.  Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. , 1976, Cold Spring Harbor symposia on quantitative biology.

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

[6]  L. Wineski Facial morphology and vibrissal movement in the golden hamster , 1985, Journal of morphology.

[7]  M. Armstrong‐James,et al.  Spatiotemporal convergence and divergence in the rat S1 “Barrel” cortex , 1987, The Journal of comparative neurology.

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

[9]  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.

[10]  M. Armstrong‐James,et al.  Flow of excitation within rat barrel cortex on striking a single vibrissa. , 1992, Journal of neurophysiology.

[11]  G. Blasdel,et al.  Orientation selectivity, preference, and continuity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  M. Jacquin,et al.  Dual innervation of the rat vibrissa: Responses of trigeminal ganglion cells projecting through deep or superficial nerves , 1992, The Journal of comparative neurology.

[13]  F. Ebner,et al.  Laminar comparison of somatosensory cortical plasticity. , 1994, Science.

[14]  Denise Brown,et al.  Taming the beast , 1995 .

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

[16]  M. Stryker,et al.  The Role of Activity in the Development of Long-Range Horizontal Connections in Area 17 of the Ferret , 1996, The Journal of Neuroscience.

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

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

[19]  W. Singer,et al.  Development of Orientation Preference Maps in Area 18 of Kitten Visual Cortex , 1997, The European journal of neuroscience.

[20]  A. Grinvald,et al.  Spatial Relationships among Three Columnar Systems in Cat Area 17 , 1997, The Journal of Neuroscience.

[21]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[22]  F. Ebner,et al.  Contribution of supragranular layers to sensory processing and plasticity in adult rat barrel cortex. , 1998, Journal of neurophysiology.

[23]  R. Lund,et al.  Receptive field properties of single neurons in rat primary visual cortex. , 1999, Journal of neurophysiology.

[24]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[25]  R. Douglas,et al.  Behavioral assessment of visual acuity in mice and rats , 2000, Vision Research.

[26]  Ehud Ahissar,et al.  Figuring Space by Time , 2001, Neuron.

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

[28]  K. Svoboda,et al.  Rapid Development and Plasticity of Layer 2/3 Maps in Rat Barrel Cortex In Vivo , 2001, Neuron.

[29]  Receptive-field construction in cortical inhibitory interneurons , 2002, Nature Neuroscience.

[30]  Randy M Bruno,et al.  Feedforward Mechanisms of Excitatory and Inhibitory Cortical Receptive Fields , 2002, The Journal of Neuroscience.

[31]  D. Feldman,et al.  Long-term depression induced by sensory deprivation during cortical map plasticity in vivo , 2003, Nature Neuroscience.

[32]  M. A. Neimark,et al.  Vibrissa Resonance as a Transduction Mechanism for Tactile Encoding , 2003, The Journal of Neuroscience.

[33]  Terrence J Sejnowski,et al.  Communication in Neuronal Networks , 2003, Science.

[34]  B. Sakmann,et al.  Dynamic Receptive Fields of Reconstructed Pyramidal Cells in Layers 3 and 2 of Rat Somatosensory Barrel Cortex , 2003, The Journal of physiology.

[35]  M. Deschenes,et al.  A Map of Angular Tuning Preference in Thalamic Barreloids , 2003, The Journal of Neuroscience.

[36]  D. Simons,et al.  Thalamocortical Angular Tuning Domains within Individual Barrels of Rat Somatosensory Cortex , 2003, The Journal of Neuroscience.

[37]  Daniel E Feldman,et al.  Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex , 2003, The Journal of Neuroscience.

[38]  M. Hartmann,et al.  Mechanical Characteristics of Rat Vibrissae: Resonant Frequencies and Damping in Isolated Whiskers and in the Awake Behaving Animal , 2003, The Journal of Neuroscience.

[39]  Dmitri B Chklovskii,et al.  Synaptic Connectivity and Neuronal Morphology Two Sides of the Same Coin , 2004, Neuron.

[40]  R. Frostig,et al.  Naturalistic experience transforms sensory maps in the adult cortex of caged animals , 2004 .

[41]  D. Simons,et al.  Angular tuning and velocity sensitivity in different neuron classes within layer 4 of rat barrel cortex. , 2004, Journal of neurophysiology.

[42]  M. A. Neimark,et al.  Neural Correlates of Vibrissa Resonance Band-Pass and Somatotopic Representation of High-Frequency Stimuli , 2004, Neuron.

[43]  M. A. Carreira-Perpiñán,et al.  Influence of lateral connections on the structure of cortical maps. , 2004, Journal of neurophysiology.

[44]  Christopher I. Moore,et al.  Title the Vibrissa Resonance Hypothesis the Vibrissa Resonance Hypothesis , 2004 .

[45]  D. Contreras,et al.  Stimulus-Dependent Changes in Spike Threshold Enhance Feature Selectivity in Rat Barrel Cortex Neurons , 2005, The Journal of Neuroscience.

[46]  P. Land,et al.  Subbarrel domains in rat somatosensory (S1) cortex , 2005, The Journal of comparative neurology.

[47]  Sooyoung Chung,et al.  Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex , 2005, Nature.

[48]  R. Frostig,et al.  Whisker-based discrimination of object orientation determined with a rapid training paradigm , 2005, Neurobiology of Learning and Memory.

[49]  Dezhe Z. Jin,et al.  The Coordinated Mapping of Visual Space and Response Features in Visual Cortex , 2005, Neuron.

[50]  Alexander M. Benison,et al.  Temporal patterns of field potentials in vibrissa/barrel cortex reveal stimulus orientation and shape. , 2006, Journal of neurophysiology.

[51]  Maja Loncar,et al.  Taming of the BEAST , 2007 .

[52]  R. K. Simpson Nature Neuroscience , 2022 .