Tactile Functions of Mechanoreceptive Afferents Innervating the Hand

Summary Four types of mechanoreceptive afferents innervate the glabrous skin of the hand. Evidence from more than three decades of combined psychophysical and neurophysiological research supports the idea that each afferent type serves a distinctly different sensory function and that these functions explain most of tactual perceptual function. The available evidence supports the following hypotheses: (1) The slowly adapting type 1 system provides the information on which form and texture perception are based. (2) The cutaneous rapidly adapting system provides information about minute skin motion and, thereby, plays a critical role in grip control. (3) The Pacinian system is responsible for the detection and perception of distant events by vibrations transmitted through objects, probes, and tools held in the hand. (4) The slowly adapting type 2 system provides information for the perception of hand conformation and for the perception of forces acting on the hand. The authors review the evidence on which these hypotheses are based. They also review the role of proprioceptive afferents in the perception of hand conformation because they appear to play a significant role along with cutaneous afferents.

[1]  H. Kowarzyk Structure and Function. , 1910, Nature.

[2]  E. J. Gates The Determination of the Limens of Single and Dual Impression by the Method of Constant Stimuli , 2022 .

[3]  M. Zigler,et al.  An Experimental Study of the Perceptions Roughness and Smoothness , 1923 .

[4]  E D Adrian,et al.  The impulse discharge from the pacinian corpuscle , 1929, The Journal of physiology.

[5]  J D Hardy,et al.  STUDIES IN TEMPERATURE SENSATION. III. THE SENSITIVITY OF THE BODY TO HEAT AND THE SPATIAL SUMMATION OF THE END ORGAN RESPONSES. , 1937, The Journal of clinical investigation.

[6]  J. Malcolm,et al.  The initiation of nerve impulses by mesenteric Pacinian corpuscles , 1950, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[7]  John Cohen The World of Touch , 1952, Nature.

[8]  N. Cauna,et al.  Nerve supply and nerve endings in Meissner's corpuscles. , 1956, The American journal of anatomy.

[9]  M SATO,et al.  Response of Pacinian corpuscles to sinusoidal vibration , 1961, The Journal of physiology.

[10]  C. Hunt,et al.  On the nature of vibration receptors in the hind limb of the cat , 1961, The Journal of physiology.

[11]  S. S. Stevens,et al.  The scaling of subjective roughness and smoothness. , 1962, Journal of experimental psychology.

[12]  R. T. Verrillo,et al.  Effect of Contactor Area on the Vibrotactile Threshold , 1963 .

[13]  P J Dyck,et al.  A quantitative study of Meissner's corpuscles in man , 1966, Neurology.

[14]  U. Lindblom,et al.  The discharge from vibration-sensitive receptors in the monkey foot. , 1966, Experimental neurology.

[15]  S. Gelfan,et al.  Muscle sense in man. , 1967, Experimental neurology.

[16]  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.

[17]  M. R. Chambers,et al.  The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. , 1972, Quarterly journal of experimental physiology and cognate medical sciences.

[18]  E Moberg,et al.  Fingers were made before forks. , 1972, The Hand.

[19]  D. McCloskey,et al.  Position sense following surgical removal of joints in man. , 1973, Brain research.

[20]  P. Matthews,et al.  Sensations of finger movement elicited by pulling upon flexor tendons in man. , 1974, The Journal of physiology.

[21]  K. O. Johnson,et al.  Reconstruction of population response to a vibratory stimulus in quickly adapting mechanoreceptive afferent fiber population innervating glabrous skin of the monkey. , 1974, Journal of neurophysiology.

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

[23]  V B Mountcastle,et al.  The view from within: pathways to the study of perception. , 1975, The Johns Hopkins medical journal.

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

[25]  R. Johansson,et al.  SKIN MECHANORECEPTORS IN THE HUMAN HAND: AN INFERENCE OF SOME POPULATION PROPERTIES , 1976 .

[26]  M. Hulliger,et al.  The responses of afferent fibres from the glabrous skin of the hand during voluntary finger movements in man. , 1979, The Journal of physiology.

[27]  F. J. Clark,et al.  Contributions of cutaneous and joint receptors to static knee-position sense in man. , 1979, Journal of neurophysiology.

[28]  R. Johansson,et al.  Detection of tactile stimuli. Thresholds of afferent units related to psychophysical thresholds in the human hand. , 1979, The Journal of physiology.

[29]  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.

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

[31]  R. Johansson,et al.  Spatial properties of the population of mechanoreceptive units in the glabrous skin of the human hand , 1980, Brain Research.

[32]  R. Johansson,et al.  Thresholds of mechanosensitive afferents in the human hand as measured with von Frey hairs , 1980, Brain Research.

[33]  K. O. Johnson,et al.  Peripheral neural representation of spatial dimensions of a textured surface moving across the monkey's finger pad. , 1980, The Journal of physiology.

[34]  A B Vallbo,et al.  Intensity of sensation related to activity of slowly adapting mechanoreceptive units in the human hand , 1980, The Journal of physiology.

[35]  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.

[36]  K O Johnson,et al.  Tactile spatial resolution. I. Two-point discrimination, gap detection, grating resolution, and letter recognition. , 1981, Journal of neurophysiology.

[37]  J. Loomis On the tangibility of letters and braille , 1981, Perception & psychophysics.

[38]  K. O. Johnson,et al.  Tactile spatial resolution. III. A continuum mechanics model of skin predicting mechanoreceptor responses to bars, edges, and gratings. , 1981, Journal of neurophysiology.

[39]  K. O. Johnson,et al.  Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. , 1981, Journal of neurophysiology.

[40]  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.

[41]  K. Andres,et al.  Morphology of cutaneous receptors. , 1982, Annual review of neuroscience.

[42]  M. Hulliger,et al.  The absence of position response in spindle afferent units from human finger muscles during accurate position holding. , 1982, The Journal of physiology.

[43]  D. McCloskey,et al.  Sensory effects of pulling or vibrating exposed tendons in man. , 1983, Brain : a journal of neurology.

[44]  E. Moberg The role of cutaneous afferents in position sense, kinaesthesia, and motor function of the hand. , 1983, Brain : a journal of neurology.

[45]  B. Munger,et al.  The sensory innervation of primate facial skin. II. Vermilion border and mucosa of lip , 1983, Brain Research Reviews.

[46]  D. McCloskey,et al.  Proprioceptive sensation at the terminal joint of the middle finger. , 1983, The Journal of physiology.

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

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

[49]  Susan J. Lederman,et al.  Tactual roughness perception in human: a psychophysical assessment of the role of vibration , 1985 .

[50]  Jack M. Loomis,et al.  Tactile recognition of raised characters: A parametric study , 1985 .

[51]  L. Kaufman,et al.  Handbook of perception and human performance , 1986 .

[52]  R H LaMotte,et al.  Tactile detection of a dot on a smooth surface: peripheral neural events. , 1986, Journal of neurophysiology.

[53]  J M Weisenberger Sensitivity to amplitude-modulated vibrotactile signals. , 1986, The Journal of the Acoustical Society of America.

[54]  C. J. Keemink,et al.  Envelope detection of amplitude-modulated high-frequency sinusoidal signals by skin mechanoreceptors. , 1986, The Journal of the Acoustical Society of America.

[55]  D. McCloskey,et al.  The role of joint receptors in human kinaesthesia when intramuscular receptors cannot contribute. , 1987, The Journal of physiology.

[56]  D. Burke,et al.  Responses to passive movement of receptors in joint, skin and muscle of the human hand. , 1988, The Journal of physiology.

[57]  P. Matthews Proprioceptors and their contribution to somatosensory mapping: complex messages require complex processing. , 1988, Canadian journal of physiology and pharmacology.

[58]  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.

[59]  F. J. Clark,et al.  The contribution of articular receptors to proprioception with the fingers in humans. , 1989, Journal of neurophysiology.

[60]  E P Gardner,et al.  Simulation of motion on the skin. I. Receptive fields and temporal frequency coding by cutaneous mechanoreceptors of OPTACON pulses delivered to the hand. , 1989, Journal of neurophysiology.

[61]  H. Muijser,et al.  The influence of spatial contrast on the frequency-dependent nature of vibration sensitivity , 1990, Perception & psychophysics.

[62]  J. L. Taylor,et al.  Ability to detect angular displacements of the fingers made at an imperceptibly slow speed. , 1990, Brain : a journal of neurology.

[63]  B. Edin,et al.  Dynamic response of human muscle spindle afferents to stretch. , 1990, Journal of neurophysiology.

[64]  E P Gardner,et al.  Simulation of motion on the skin. IV. Responses of Pacinian corpuscle afferents innervating the primate hand to stripe patterns on the OPTACON. , 1990, Journal of neurophysiology.

[65]  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.

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

[67]  K. O. Johnson,et al.  Human tactile pattern recognition: active versus passive touch, velocity effects, and patterns of confusion. , 1991, Journal of neurophysiology.

[68]  J. Abbs,et al.  Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand. , 1991, Journal of neurophysiology.

[69]  J C Craig,et al.  Perceptual processing of adjacent and nonadjacent tactile nontargets , 1992, Perception & psychophysics.

[70]  T. Yoshioka,et al.  Neural mechanisms of tactual form and texture perception. , 1992, Annual review of neuroscience.

[71]  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.

[72]  B. Edin Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. , 1992, Journal of neurophysiology.

[73]  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.

[74]  T. G. Forrest,et al.  The role of frequency selectivity in measures of auditory and vibrotactile temporal resolution. , 1992, The Journal of the Acoustical Society of America.

[75]  J. Kaas The functional organization of somatosensory cortex in primates. , 1993, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[76]  Mark Holliins,et al.  Perceptual dimensions of tactile surface texture: A multidimensional scaling analysis , 1993, Perception & psychophysics.

[77]  S S Hsiao,et al.  Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. , 1993, Journal of neurophysiology.

[78]  J. Bell,et al.  The structure and function of pacinian corpuscles: A review , 1994, Progress in Neurobiology.

[79]  E. P. Gardner,et al.  Discrimination of the direction of motion on the human hand: a psychophysical study of stimulation parameters. , 1994, Journal of neurophysiology.

[80]  J C Craig,et al.  The effect of spatial orientation on the perception of moving tactile stimuli , 1994, Perception & psychophysics.

[81]  K O Johnson,et al.  The limit of tactile spatial resolution in humans , 1994, Neurology.

[82]  K. O. Johnson,et al.  A psychophysical study of the mechanisms of sensory recovery following nerve injury in humans. , 1994, Brain : a journal of neurology.

[83]  R. Fitzpatrick,et al.  Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. , 1994, The Journal of physiology.

[84]  Serge Marchand Touch, Temperature, and Pain in Health and Disease: Mechanisms and Assessments , 1995 .

[85]  A. Goodwin,et al.  Representation of curved surfaces in responses of mechanoreceptive afferent fibers innervating the monkey's fingerpad , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  B. Edin,et al.  Skin strain patterns provide kinaesthetic information to the human central nervous system. , 1995, The Journal of physiology.

[87]  J C Craig,et al.  Tactile selective attention and temporal masking , 1995, Perception & psychophysics.

[88]  Steven S. Hsiao,et al.  Neural mechanisms of tactile form recognition , 1995 .

[89]  A. Wohlert,et al.  Tactile perception of spatial stimuli on the lip surface by young and older adults. , 1996, Journal of speech and hearing research.

[90]  E P Gardner,et al.  Discrimination of simulated texture patterns on the human hand. , 1996, Journal of neurophysiology.

[91]  M. Srinivasan,et al.  An investigation of the mechanics of tactile sense using two-dimensional models of the primate fingertip. , 1996, Journal of biomechanical engineering.

[92]  K. Sathian,et al.  Tactile spatial acuity at the human fingertip and lip , 1996, Neurology.

[93]  Steven S. Hsiao,et al.  Linearity as the basic law of psychophysics: Evidence from studies of the neural mechanisms of roughness magnitude estimation , 1996 .

[94]  K. O. Johnson,et al.  Monkey cutaneous SAI and RA responses to raised and depressed scanned patterns: effects of width, height, orientation, and a raised surround. , 1997, Journal of neurophysiology.

[95]  A. Goodwin,et al.  Encoding of object curvature by tactile afferents from human fingers. , 1997, Journal of neurophysiology.

[96]  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.

[97]  G. Essick,et al.  Factors affecting direction discrimination of moving tactile stimuli , 1998 .

[98]  A. Goodwin,et al.  Peripheral Neural Mechanisms Determining the Orientation of Cylinders Grasped by the Digits , 1998, The Journal of Neuroscience.

[99]  J. Craig,et al.  Factors affecting tactile spatial acuity. , 1998, Somatosensory & motor research.

[100]  M. Wiesendanger,et al.  Manual dexterity and the making of tools – an introduction from an evolutionary perspective , 1999, Experimental Brain Research.

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

[102]  James Biggs,et al.  Extrinsic muscles of the hand signal fingertip location more precisely than they signal the angles of individual finger joints , 1999, Experimental Brain Research.

[103]  G. Essick,et al.  A letter-recognition task to assess lingual tactile acuity. , 1999, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[104]  K. O. Johnson,et al.  SA1 and RA receptive fields, response variability, and population responses mapped with a probe array. , 1999, Journal of neurophysiology.

[105]  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.

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

[107]  J. Craig,et al.  Grating orientation as a measure of tactile spatial acuity. , 1999, Somatosensory & motor research.

[108]  S S Hsiao,et al.  Detection of vibration transmitted through an object grasped in the hand. , 1999, Journal of neurophysiology.

[109]  F. Horak,et al.  Precision contact of the fingertip reduces postural sway of individuals with bilateral vestibular loss , 1999, Experimental Brain Research.

[110]  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.

[111]  Á. Pascual-Leone,et al.  Tactile spatial resolution in blind Braille readers , 2000, Neurology.

[112]  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.

[113]  J C Craig,et al.  Processing of sequential tactile patterns: Effects of a neutral stimulus , 2000, Perception & psychophysics.

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

[115]  Kenneth O. Johnson,et al.  The Two-Point Threshold , 2000 .

[116]  A. Goodwin,et al.  Tactile discrimination of gaps by slowly adapting afferents: effects of population parameters and anisotropy in the fingerpad. , 2000, Journal of neurophysiology.