Vibrissa Resonance as a Transduction Mechanism for Tactile Encoding

We present evidence that resonance properties of rat vibrissae differentially amplify high-frequency and complex tactile signals. Consistent with a model of vibrissa mechanics, optical measurements of vibrissae revealed that their first mechanical resonance frequencies systematically varied from low (60-100 Hz) in longer, posterior vibrissae to high (∼750 Hz) in shorter, anterior vibrissae. Resonance amplification of tactile input was observed in vivo and ex vivo, and in a variety of boundary conditions that are likely to occur during perception, including stimulation of the vibrissa with moving complex natural stimuli such as sandpaper. Vibrissae were underdamped, allowing for sharp tuning to resonance frequencies. Vibrissa resonance constitutes a potentially useful mechanism for perception of high-frequency and complex tactile signals. Amplification of small amplitude signals by resonance could facilitate detection of stimuli that would otherwise fail to drive neural activity. The systematic map of frequency sensitivity across the face could facilitate texture discrimination through somatotopic encoding of frequency content. These findings suggest strong parallels between vibrissa tactile processing and auditory encoding, in which the cochlea also uses resonance to amplify low-amplitude signals and to generate a spatial map of frequency sensitivity.

[1]  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.

[2]  Daniel J Simons,et al.  Response properties of whisker-associated trigeminothalamic neurons in rat nucleus principalis. , 2003, Journal of neurophysiology.

[3]  D. Kleinfeld,et al.  Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. , 2003, Journal of neurophysiology.

[4]  M. A. Neimark,et al.  A model of texture encoding by vibrissa resonance properties , 2002 .

[5]  Mitra J. Hartmann,et al.  c ○ 2001 Kluwer Academic Publishers. Manufactured in The Netherlands. Active Sensing Capabilities of the Rat Whisker System , 2022 .

[6]  H. Bleckmann,et al.  Hydrodynamic Trail-Following in Harbor Seals (Phoca vitulina) , 2001, Science.

[7]  M Zacksenhouse,et al.  Temporal and spatial coding in the rat vibrissal system. , 2001, Progress in brain research.

[8]  D. Simons,et al.  Circuit dynamics and coding strategies in rodent somatosensory cortex. , 2000, Journal of neurophysiology.

[9]  D. Simons,et al.  Coding of deflection velocity and amplitude by whisker primary afferent neurons: implications for higher level processing. , 2000, Somatosensory & motor research.

[10]  G. Jacobs,et al.  Neural Mapping of Direction and Frequency in the Cricket Cercal Sensory System , 1999, The Journal of Neuroscience.

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

[12]  J. Roddey,et al.  Information theoretic analysis of dynamical encoding by filiform mechanoreceptors in the cricket cercal system. , 1996, Journal of neurophysiology.

[13]  John P. Miller,et al.  Broadband neural encoding in the cricket cereal sensory system enhanced by stochastic resonance , 1996, Nature.

[14]  D. Simons,et al.  Task- and subject-related differences in sensorimotor behavior during active touch. , 1995, Somatosensory & motor research.

[15]  H. Bleckmann Reception of hydrodynamic stimuli in aquatic and semiaquatic animals , 1994 .

[16]  D. M. Freeman,et al.  Hydrodynamic analysis of a two-dimensional model for micromechanical resonance of free-standing hair bundles , 1990, Hearing Research.

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

[19]  B. Munger,et al.  A comparative light microscopic analysis of the sensory innervation of the mystacial pad. I. Innervation of vibrissal follicle‐sinus complexes , 1986, The Journal of comparative neurology.

[20]  E. A. Wright,et al.  A quantitative study of hair growth using mouse and rat vibrissal follicles. I. Dermal papilla volume determines hair volume. , 1982, Journal of embryology and experimental morphology.

[21]  Stanley A. Gelfand,et al.  Hearing: An Introduction to Psychological and Physiological Acoustics, Fourth Edition , 1998 .

[22]  T. Yohro Structure of the sinus hair follicle in the big‐clawed shrew, Sorex unguiculatus , 1977, Journal of morphology.

[23]  T. Woolsey,et al.  Comparative anatomical studies of the Sml face cortex with special reference to the occurrence of “barrels” in layer IV , 1975, The Journal of comparative neurology.

[24]  M. Merzenich,et al.  Representation of the cochlear partition of the superior temporal plane of the macaque monkey. , 1973, Brain research.

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

[26]  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.

[27]  K. Weiss Vibration Problems in Engineering , 1965, Nature.

[28]  W. Thomson Theory of vibration with applications , 1965 .

[29]  N Y KIANG,et al.  STIMULUS CODING IN THE COCHLEAR NUCLEUS. , 1965, The Annals of otology, rhinology, and laryngology.

[30]  Den Hartog Advanced Strength of Materials , 1952 .

[31]  Georg v. Békésy,et al.  The Variation of Phase Along the Basilar Membrane with Sinusoidal Vibrations , 1947 .

[32]  S. Timoshenko,et al.  Theory of elasticity , 1975 .

[33]  Stephen P. Timoshenko,et al.  Vibration problems in engineering , 1928 .