Neural Coding Mechanisms Underlying Perceived Roughness of Finely Textured Surfaces

Combined psychophysical and neurophysiological studies have shown that the perceived roughness of surfaces with element spacings of >1 mm is based on spatial variation in the firing rates of slowly adapting type 1 (SA1) afferents (mean absolute difference in firing rates between SA1 afferents with receptive fields separated by ∼2 mm). The question addressed here is whether this mechanism accounts for the perceived roughness of surfaces with element spacings of <1 mm. Twenty triangular and trapezoidal gratings plus a smooth surface were used as stimulus patterns [spatial periods, 0.1–2.0 mm; groove widths (GWs), 0.1–2.0 mm; and ridge widths (RWs), 0–1.0 mm]. In the human psychophysical studies, we found that the following equation described the mean roughness magnitude estimates of the subjects accurately (0.99 correlation): 0.2 + 1.6GW − 0.5RW − 0.25GW2. In the neurophysiological studies, these surfaces were scanned across the receptive fields of SA1, rapidly adapting, and Pacinian (PC) afferents, innervating the glabrous skin of anesthetized macaque monkeys. SA1 spatial variation was highly correlated (0.97) with human roughness judgments. There was no consistent relationship between PC responses and roughness judgments; PC afferents responded strongly and almost equally to all of the patterns. Spatial variation in SA1 firing rates is the only neural code that accounts for the perceived roughness of surfaces with finely and coarsely spaced elements. When surface elements are widely spaced, the spatial variation in firing rates is determined primarily by the surface pattern; when the elements are finely spaced, the variation in firing rates between SA1 afferents is determined by stochastic variation in spike rates.

[1]  M. Kendall,et al.  The Logic of Scientific Discovery. , 1959 .

[2]  S S Stevens,et al.  To Honor Fechner and Repeal His Law: A power function, not a log function, describes the operating characteristic of a sensory system. , 1961, Science.

[3]  J. Platt Strong Inference: Certain systematic methods of scientific thinking may produce much more rapid progress than others. , 1964, Science.

[4]  David R. Cox,et al.  The statistical analysis of series of events , 1966 .

[5]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[6]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[7]  V. Mountcastle,et al.  Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibers innervating the monkey hand. , 1972, Journal of neurophysiology.

[8]  S. Lederman Tactile roughness of grooved surfaces: The touching process and effects of macro- and microsurface structure , 1974 .

[9]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[10]  I. Darian‐Smith,et al.  Innervation density of mechanoreceptive fibres supplying glabrous skin of the monkey's index finger. , 1980, The Journal of physiology.

[11]  I. Darian‐Smith,et al.  Peripheral neural representation of the spatial frequency of a grating moving across the monkey's finger pad. , 1980, The Journal of physiology.

[12]  A. Freeman,et al.  A model accounting for effects of vibratory amplitude on responses of cutaneous mechanoreceptors in macaque monkey , 1982, The Journal of physiology.

[13]  S. Lederman,et al.  The role of vibration in the tactual perception of roughness , 1982, Perception & psychophysics.

[14]  S. Lederman Tactual roughness perception: Spatial and temporal determinants. , 1983 .

[15]  G. Lamb Tactile discrimination of textured surfaces: psychophysical performance measurements in humans. , 1983, The Journal of physiology.

[16]  Kenneth O. Johnson,et al.  A rotating drum stimulator for scanning embossed patterns and textures across the skin , 1988, Journal of Neuroscience Methods.

[17]  Gary James Jason,et al.  The Logic of Scientific Discovery , 1988 .

[18]  K Sathian,et al.  Spatial and temporal factors determining afferent fiber responses to a grating moving sinusoidally over the monkey's fingerpad , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  D. Katz The World of Touch , 1989 .

[20]  A. Goodwin,et al.  Perceived roughness of a grating: correlation with responses of mechanoreceptive afferents innervating the monkey's fingerpad , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  C. Connor,et al.  Tactile roughness: neural codes that account for psychophysical magnitude estimates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. Phillips,et al.  Responses of human mechanoreceptive afferents to embossed dot arrays scanned across fingerpad skin , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  K. Johnson,et al.  Neural coding of tactile texture: comparison of spatial and temporal mechanisms for roughness perception , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  P. Matthews,et al.  Texture perception and afferent coding distorted by cooling the human ulnar nerve , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  K. O. Johnson,et al.  Evaluation of the relative roles of slowly and rapidly adapting afferent fibers in roughness perception. , 1994, Canadian journal of physiology and pharmacology.

[26]  Kenneth O. Johnson,et al.  Neural Coding Mechanisms in Tactile Pattern Recognition: The Relative Contributions of Slowly and Rapidly Adapting Mechanoreceptors to Perceived Roughness , 1997, The Journal of Neuroscience.

[27]  J. DiCarlo,et al.  Structure of Receptive Fields in Area 3b of Primary Somatosensory Cortex in the Alert Monkey , 1998, The Journal of Neuroscience.

[28]  K. O. Johnson,et al.  Surround suppression in the responses of primate SA1 and RA mechanoreceptive afferents mapped with a probe array. , 1999, Journal of neurophysiology.

[29]  J. DiCarlo,et al.  Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey , 1999, The Journal of Neuroscience.

[30]  B. Whitsel,et al.  Response of anterior parietal cortex to cutaneous flutter versus vibration. , 1999, Journal of neurophysiology.

[31]  J. DiCarlo,et al.  Spatial and Temporal Structure of Receptive Fields in Primate Somatosensory Area 3b: Effects of Stimulus Scanning Direction and Orientation , 2000, The Journal of Neuroscience.

[32]  C. E. Chapman,et al.  Relative effects of the spatial and temporal characteristics of scanned surfaces on human perception of tactile roughness using passive touch , 2000, Experimental Brain Research.

[33]  M. Hollins,et al.  Imposed Vibration Influences Perceived Tactile Smoothness , 2000, Perception.

[34]  M. Hollins,et al.  Evidence for the duplex theory of tactile texture perception , 2000, Perception & psychophysics.