The Morphology of the Rat Vibrissal Array: A Model for Quantifying Spatiotemporal Patterns of Whisker-Object Contact

In all sensory modalities, the data acquired by the nervous system is shaped by the biomechanics, material properties, and the morphology of the peripheral sensory organs. The rat vibrissal (whisker) system is one of the premier models in neuroscience to study the relationship between physical embodiment of the sensor array and the neural circuits underlying perception. To date, however, the three-dimensional morphology of the vibrissal array has not been characterized. Quantifying array morphology is important because it directly constrains the mechanosensory inputs that will be generated during behavior. These inputs in turn shape all subsequent neural processing in the vibrissal-trigeminal system, from the trigeminal ganglion to primary somatosensory (“barrel”) cortex. Here we develop a set of equations for the morphology of the vibrissal array that accurately describes the location of every point on every whisker to within ±5% of the whisker length. Given only a whisker's identity (row and column location within the array), the equations establish the whisker's two-dimensional (2D) shape as well as three-dimensional (3D) position and orientation. The equations were developed via parameterization of 2D and 3D scans of six rat vibrissal arrays, and the parameters were specifically chosen to be consistent with those commonly measured in behavioral studies. The final morphological model was used to simulate the contact patterns that would be generated as a rat uses its whiskers to tactually explore objects with varying curvatures. The simulations demonstrate that altering the morphology of the array changes the relationship between the sensory signals acquired and the curvature of the object. The morphology of the vibrissal array thus directly constrains the nature of the neural computations that can be associated with extraction of a particular object feature. These results illustrate the key role that the physical embodiment of the sensor array plays in the sensing process.

[1]  E. Guic-Robles,et al.  Rats can learn a roughness discrimination using only their vibrissal system , 1989, Behavioural Brain Research.

[2]  P. D. Polly,et al.  Geometric morphometrics: recent applications to the study of evolution and development , 2010 .

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

[4]  E. Salinas How Behavioral Constraints May Determine Optimal Sensory Representations , 2006, PLoS biology.

[5]  Takashi R Sato,et al.  Divergent movement of adjacent whiskers. , 2002, Journal of neurophysiology.

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

[7]  R. German,et al.  Pelvic growth: Ontogeny of size and shape sexual dimorphism in rat pelves , 2007, Journal of morphology.

[8]  M. Hartmann,et al.  Right–Left Asymmetries in the Whisking Behavior of Rats Anticipate Head Movements , 2006, The Journal of Neuroscience.

[9]  H. Philip Zeigler,et al.  Trigeminal orosensory deafferentation disrupts feeding and drinking mechanisms in the rat , 1982, Brain Research.

[10]  Joseph H. Solomon,et al.  Variability in velocity profiles during free-air whisking behavior of unrestrained rats. , 2008, Journal of neurophysiology.

[11]  E Ahissar,et al.  Size gradients of barreloids in the rat thalamus , 2001, The Journal of comparative neurology.

[12]  M. Nicolelis,et al.  Behavioral Properties of the Trigeminal Somatosensory System in Rats Performing Whisker-Dependent Tactile Discriminations , 2001, The Journal of Neuroscience.

[13]  P David Polly,et al.  PHYLOGENETIC AND ENVIRONMENTAL COMPONENTS OF MORPHOLOGICAL VARIATION: SKULL, MANDIBLE, AND MOLAR SHAPE IN MARMOTS (MARMOTA, RODENTIA) , 2005, Evolution; international journal of organic evolution.

[14]  R J Full,et al.  How animals move: an integrative view. , 2000, Science.

[15]  H. Zeigler,et al.  Topography of rodent whisking--I. Two-dimensional monitoring of whisker movements , 2002, Somatosensory & motor research.

[16]  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.

[17]  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.

[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]  J. Dörfl The musculature of the mystacial vibrissae of the white mouse. , 1982, Journal of anatomy.

[20]  A. Ahl The role of vibrissae in behavior: A status review , 1986, Veterinary Research Communications.

[21]  John G. Griffiths,et al.  Least squares ellipsoid specific fitting , 2004, Geometric Modeling and Processing, 2004. Proceedings.

[22]  E. Ahissar,et al.  Vibrissal Kinematics in 3D: Tight Coupling of Azimuth, Elevation, and Torsion across Different Whisking Modes , 2008, Neuron.

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

[24]  S. B. Vincent The function of the vibrissae in the behavior of the white rat , 1912 .

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

[26]  Hillel J. Chiel,et al.  The Brain in Its Body: Motor Control and Sensing in a Biomechanical Context , 2009, The Journal of Neuroscience.

[27]  R Bermejo,et al.  Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks. , 2001, Somatosensory & motor research.

[28]  Patrick J Drew,et al.  Representation of moving wavefronts of whisker deflection in rat somatosensory cortex. , 2007, Journal of neurophysiology.

[29]  R Bermejo,et al.  Topography of whisking II: Interaction of whisker and pad , 2005, Somatosensory & motor research.

[30]  Ben Mitchinson,et al.  Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact , 2007, Proceedings of the Royal Society B: Biological Sciences.

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