Importance of Temporal Cues for Tactile Spatial- Frequency Discrimination

While scanning a textured surface with fingers, tactile information is encoded both spatially, by differential activation of adjacent receptors, and temporally, by changes in receptor activation during movements of the fingers across the surface. We used a tactile discrimination task to examine the dependence of human tactile perception on the availability of spatial and temporal cues. Subjects discriminated between spatial frequencies of metal gratings presented simultaneously to both hands. Tactile temporal cues were eliminated by preventing lateral hand movements; tactile spatial cues were eliminated by using gloves with an attached rubber pin. Analysis revealed separation of the subjects into two groups: “spatiotemporal” (ST) and “latent-temporal” (LT). Under normal conditions, the performance of ST subjects was significantly better than that of the LT subjects. Prevention of lateral movements impaired performance of both ST and LT subjects. However, when only temporal cues were available, the performance of ST subjects was significantly impaired, whereas that of the LT subjects either improved or did not change. Under the latter condition, LT subjects changed strategy to scanning with alternating hands, at velocities similar to the velocities normally used by ST subjects. These velocities generated temporal frequencies between 15 and 30 Hz. The LT subjects were unaware of their improved performance. Nine of ten LT subjects significantly improved their performance under normal conditions when trained to scan gratings using alternating hands and velocities similar to those used by ST subjects. We conclude that (1) temporal cues are essential for spatial-frequency discrimination, (2) human subjects vary in the tactile strategies they use for texture exploration, and (3) poor tactile performers can significantly improve by using strategies that emphasize temporal cues.

[1]  R. Klatzky,et al.  Tactile roughness perception with a rigid link interposed between skin and surface , 1999, Perception & psychophysics.

[2]  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.

[3]  E Ahissar,et al.  Temporal frequency of whisker movement. II. Laminar organization of cortical representations. , 2001, Journal of neurophysiology.

[4]  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.

[5]  E Ahissar,et al.  Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[6]  A W Goodwin,et al.  Sinusoidal movement of a grating across the monkey's fingerpad: temporal patterns of afferent fiber responses , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M. Srinivasan,et al.  Tactile detection of slip: surface microgeometry and peripheral neural codes. , 1990, Journal of neurophysiology.

[8]  J. Gibson Observations on active touch. , 1962, Psychological review.

[9]  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.

[10]  K O Johnson,et al.  Neural mechanisms of spatial tactile discrimination: neural patterns evoked by braille‐like dot patterns in the monkey. , 1981, The Journal of physiology.

[11]  M. M. Taylor,et al.  Fingertip force, surface geometry, and the perception of roughness by active touch , 1972 .

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

[13]  Kenneth O. Johnson,et al.  Spatial and Nonspatial Neural Mechanisms Underlying Tactile Spatial Discrimination , 1984 .

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

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

[16]  E Ahissar,et al.  Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. , 2001, Journal of neurophysiology.

[17]  S. Hochstein,et al.  Task difficulty and the specificity of perceptual learning , 1997, Nature.

[18]  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.

[19]  C E Carr,et al.  Processing of temporal information in the brain. , 1993, Annual review of neuroscience.

[20]  H Burton,et al.  Neuronal activity in the primary somatosensory cortex in monkeys (Macaca mulatta) during active touch of textured surface gratings: responses to groove width, applied force, and velocity of motion. , 1991, Journal of neurophysiology.

[21]  V. Mountcastle,et al.  Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. , 1975, Journal of neurophysiology.

[22]  S. Lederman The perception of surface roughness by active and passive touch , 1981 .

[23]  M. M. Taylor,et al.  Tactile roughness of grooved surfaces: A model and the effect of friction , 1975 .

[24]  K O Johnson,et al.  A comparison of visual and two modes of tactual letter resolution , 1983, Perception & psychophysics.

[25]  K. Sathian,et al.  Tactile sensing of surface features , 1989, Trends in Neurosciences.

[26]  K. Sathian,et al.  Temporal Cues Contribute to Tactile Perception of Roughness , 2001, The Journal of Neuroscience.

[27]  Ehud Ahissar,et al.  Temporal-Code to Rate-Code Conversion by Neuronal Phase-Locked Loops , 1998, Neural Computation.

[28]  N. Wittenburg,et al.  Transformation from temporal to rate coding in a somatosensory thalamocortical pathway , 2022 .

[29]  L. E. Krueger David Katz’s Der Aufbau der Tastwelt (The world of touch): A synopsis , 1970 .

[30]  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.

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

[32]  R. Johansson,et al.  Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements , 1982, Brain Research.

[33]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[34]  A. Freeman,et al.  Cutaneous mechanoreceptors in macaque monkey: temporal discharge patterns evoked by vibration, and a receptor model , 1982, The Journal of physiology.

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

[36]  V B Mountcastle,et al.  Neuronal Coding by Cortical Cells of the Frequency of Oscillating Peripheral Stimuli , 1968, Science.

[37]  W. Jiang,et al.  Neuronal encoding of texture changes in the primary and the secondary somatosensory cortical areas of monkeys during passive texture discrimination. , 1997, Journal of neurophysiology.

[38]  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.

[39]  R H LaMotte,et al.  Softness discrimination with a tool. , 2000, Journal of neurophysiology.

[40]  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.

[41]  H Burton,et al.  Response patterns in second somatosensory cortex (SII) of awake monkeys to passively applied tactile gratings. , 2000, Journal of neurophysiology.