Unsupervised quantification of whisking and head movement in freely moving rodents.

The rodent whisker system has become the leading experimental paradigm for the study of active sensing. Thanks to more sophisticated behavioral paradigms, progressively better neurophysiological methods, and improved video hardware/software, there is now the prospect of defining the precise connection between the sensory apparatus and brain activity in awake, exploring animals. Achieving this ambitious goal requires quantitative, objective characterization of head and whisker kinematics. This study presents the methodology and potential uses of a new automated motion analysis routine. The program provides full quantification of head orientation and translation, as well as the angle, frequency, amplitude, and bilateral symmetry of whisking. The system operates without any need for manual tracing by the user. Quantitative comparison to whisker detection by expert humans indicates that the program's correct detection rate is at >95% even on animals with all whiskers intact. Particular attention has been paid to obtaining reliable performance under nonoptimal lighting or video conditions and at frame rates as low as 100. Variation of the zoom across time is compensated for without user intervention. The program adapts automatically to the size and shape of different species. The outcome of our testing indicates that the program can be a valuable tool in quantifying rodent sensorimotor behavior.

[1]  Joseph H. Solomon,et al.  Biomechanics: Robotic whiskers used to sense features , 2006, Nature.

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

[3]  B. Sakmann,et al.  Unsupervised whisker tracking in unrestrained behaving animals. , 2008, Journal of neurophysiology.

[4]  Rafael C. González,et al.  Local Determination of a Moving Contrast Edge , 1985, IEEE Transactions on Pattern Analysis and Machine Intelligence.

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

[6]  Michael Brecht,et al.  Behavioral Neuroscience , 2022 .

[7]  D. Kleinfeld,et al.  'Where' and 'what' in the whisker sensorimotor system , 2008, Nature Reviews Neuroscience.

[8]  R. E. Kalman,et al.  New Results in Linear Filtering and Prediction Theory , 1961 .

[9]  Per Magne Knutsen,et al.  Haptic Object Localization in the Vibrissal System: Behavior and Performance , 2006, The Journal of Neuroscience.

[10]  Michael Isard,et al.  Active Contours: The Application of Techniques from Graphics, Vision, Control Theory and Statistics to Visual Tracking of Shapes in Motion , 2000 .

[11]  Dori Derdikman,et al.  Tracking whisker and head movements in unrestrained behaving rodents. , 2005, Journal of neurophysiology.

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

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

[14]  Vincent Hayward,et al.  Force can overcome object geometry in the perception of shape through active touch , 2001, Nature.

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

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

[17]  Pierre Vandergheynst,et al.  Multiresolution segmentation of natural images: from linear to nonlinear scale-space representations , 2004, IEEE Transactions on Image Processing.

[18]  Mathew E Diamond,et al.  Whisking and whisker kinematics during a texture classification task , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[19]  Nathan G. Clack,et al.  Vibrissa-Based Object Localization in Head-Fixed Mice , 2010, The Journal of Neuroscience.

[20]  M. Diamond,et al.  Deciphering the Spike Train of a Sensory Neuron: Counts and Temporal Patterns in the Rat Whisker Pathway , 2006, The Journal of Neuroscience.

[21]  Susan J. Lederman,et al.  Extracting object properties through haptic exploration. , 1993, Acta psychologica.

[22]  T. Krahe,et al.  Neocortical plasticity deficits in fetal alcohol spectrum disorders: Lessons from barrel and visual cortex , 2008, Journal of neuroscience research.

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

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

[25]  D. Kleinfeld,et al.  Goal-directed whisking increases phase-locking between vibrissa movement and electrical activity in primary sensory cortex in rat. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[26]  T. Prescott,et al.  An Algorithm for Automatic Tracking of Rat Whiskers , 2010 .

[27]  R. Bajcsy.  Active perception , 1988 .

[28]  David Kleinfeld,et al.  Active sensation: insights from the rodent vibrissa sensorimotor system , 2006, Current Opinion in Neurobiology.

[29]  E. Ahissar,et al.  Encoding of Vibrissal Active Touch , 2003, Neuron.

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

[31]  A. Savitzky,et al.  Smoothing and Differentiation of Data by Simplified Least Squares Procedures. , 1964 .

[32]  Farzin Mokhtarian,et al.  A Theory of Multiscale, Curvature-Based Shape Representation for Planar Curves , 1992, IEEE Trans. Pattern Anal. Mach. Intell..

[33]  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.

[34]  M. Diamond,et al.  Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination , 2007, PLoS biology.

[35]  R. Azouz,et al.  Dynamic translation of surface coarseness into whisker vibrations. , 2008, Journal of neurophysiology.

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

[37]  M. Diamond,et al.  Whisker-Mediated Texture Discrimination , 2008, PLoS biology.

[38]  Gloria Cristalli,et al.  A new ethyladenine antagonist of adenosine A2A receptors: Behavioral and biochemical characterization as an antiparkinsonian drug , 2010, Neuropharmacology.

[39]  Jose M. Carmena,et al.  A System for Neural Recording and Closed-Loop Intracortical Microstimulation in Awake Rodents , 2009, IEEE Transactions on Biomedical Engineering.

[40]  Michael Isard,et al.  Shape-space models , 1998 .

[41]  Mathew E. Diamond,et al.  Hippocampal Representation of Touch-Guided Behavior in Rats: Persistent and Independent Traces of Stimulus and Reward Location , 2011, PloS one.

[42]  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.