Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand.

Intraneural microstimulation (i.n.m.s.) was performed in awake human volunteers, using tungsten micro‐electrodes inserted into median and ulnar nerve fascicles supplying the skin of the hand. The same electrodes were used alternatively to record impulse activity from single nerve fibres at the i.n.m.s. sites. Monitoring occasionally, with a proximal electrode, the impulse traffic evoked by i.n.m.s. distally in the same fascicle, established that the stimulation procedure could be made selective enough to activate single myelinated fibres in isolation, while also permitting multifibre recruitment. Monitoring propagated impulses also established that i.n.m.s. of a single myelinated fibre supplying a low‐threshold mechanoreceptor in the hand might evoke an elementary sensation. Such sensations were fully endowed with cognitive attributes amenable to psychophysical estimation: quality, magnitude and localized projection. Psychophysical tests were made during i.n.m.s. at intraneural sites where single‐unit activity was recorded from classified RA, PC, SA I or SA II mechanoreceptors. Changes in excitability of the nerve fibre of an identified unit, induced by further i.n.m.s., certified that the recorded unit had been stimulated during psychophysical tests. Comparing physical location of the receptive field of a recorded unit and localization of the projected field of the corresponding elementary sensation, revealed that either predicted the other accurately. This further assisted identification of the unit activated by i.n.m.s. The type of a recorded unit and the quality of the elementary sensation evoked by its activation were also reciprocally predictive. RA units evoked intermittent tapping, PC units vibration or tickle and SA I units evoked pressure. SA II units evoked no sensation when activated in isolation. Afferent impulse frequency determined magnitude of pressure in the SA I system, and frequency of vibration in the PC system. In the RA system, stimulation frequency determined frequency of tapping‐flutter‐vibration sensation at relatively low rates and subjective intensity of sensation at high rates. These findings endorse the concept that quality of sensation is coded in specific sensory systems. Further, they provide novel evidence that sensory quality, magnitude and localization can be exquisitely resolved at cognitive levels on the basis of input initiated in a single mechanoreceptor unit.

[1]  THE DISTRIBUTION OF AFFERENT NERVES IN THE SKIN. , 1906 .

[2]  G. H. Bishop RESPONSES TO ELECTRICAL STIMULATION OF SINGLE SENSORY UNITS OF SKIN , 1943 .

[3]  S SUNDERLAND,et al.  The intraneural topography of the radial, median and ulnar nerves. , 1945, Brain : a journal of neurology.

[4]  I. Tasaki Properties of myelinated fibers in frog sciatic nerve and in spinal cord as examined with micro-electrodes. , 1952, The Japanese journal of physiology.

[5]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[6]  V. Mountcastle,et al.  Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. , 1959, Bulletin of the Johns Hopkins Hospital.

[7]  Denis Williams THE EXCITABLE CORTEX , 1959 .

[8]  H. Hensel,et al.  Afferent impulses in cutaneous sensory nerves in human subjects. , 1960, Journal of neurophysiology.

[9]  P. Wall,et al.  Cord cells responding to touch, damage, and temperature of skin. , 1960, Journal of neurophysiology.

[10]  A. Vallbo,et al.  Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. , 1968, Experimental neurology.

[11]  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.

[12]  K. Hagbarth,et al.  Afferent impulses in median nerve fascicles evoked by tactile stimuli of the human hand. , 1970, Brain research.

[13]  K. Hagbarth,et al.  Single unit potentials with complex waveform seen in microelectrode recordings from the human median nerve. , 1970, Brain research.

[14]  M. Merzenich,et al.  Representation of slowly and rapidly adapting cutaneous mechanoreceptors of the hand in Brodmann's areas 3 and 1 of Macaca mulatta. , 1972, Brain research.

[15]  P. Wall,et al.  Factors forming the edge of a receptive field: the presence of relatively ineffective afferent terminals , 1972, The Journal of physiology.

[16]  Juhani Hyvärinen,et al.  Electrical stimulation of human hair follicles via microelectrodes , 1973 .

[17]  M. Knibestöl Stimulus‐response functions of slowly adapting mechanoreceptors in the human glabrous skin area. , 1975, The Journal of physiology.

[18]  Å.B. Vallbo,et al.  SKIN MECHANORECEPTORS IN THE HUMAN HAND: NEURAL AND PSYCHOPHYSICAL THRESHOLDS , 1976 .

[19]  O. Franzén,et al.  CODING OF VELOCITY OF SKIN INDENTATION IN MAN AND MONKEY A PERCEPTUAL-NEUROPHYSIOLOGICAL CORRELATION , 1976 .

[20]  A. Vallbo,et al.  Prediction of propagation block on the basis of impulse shape in single unit recordings from human nerves. , 1976, Acta physiologica Scandinavica.

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

[22]  R. Johansson Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. , 1978, The Journal of physiology.

[23]  V. Mountcastle,et al.  An organizing principle for cerebral function : the unit module and the distributed system , 1978 .

[24]  J. Kaas,et al.  Double representation of the body surface within cytoarchitectonic area 3b and 1 in “SI” in the owl monkey (aotus trivirgatus) , 1978, The Journal of comparative neurology.

[25]  A. Vallbo,et al.  Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. , 1979, Physiological reviews.

[26]  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.

[27]  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.

[28]  H. E. Torebjörk,et al.  Specific sensations evoked by activity in single identified sensory units in man. , 1980 .

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

[30]  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.

[31]  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.

[32]  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.

[33]  G. Parry,et al.  Arachidonate-induced experimental nerve infarction , 1981, Journal of the Neurological Sciences.

[34]  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.

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

[36]  A. Vallbo,et al.  Sensations evoked from the glabrous skin of the human hand by electrical stimulation of unitary mechanosensitive afferents , 1981, Brain Research.

[37]  B. Libet Brain stimulation in the study of neuronal functions for conscious sensory experiences. , 1982, Human neurobiology.

[38]  R. Johansson,et al.  Sensitivity to edges of mechanoreceptive afferent units innervating the glabrous skin of the human hand , 1982, Brain Research.

[39]  D. Zealear,et al.  Stimulating and recording from axons within their myelin sheaths: a stable and nondamaging method for studying single motor units , 1982, Journal of Neuroscience Methods.

[40]  R. Johansson,et al.  Tactile sensory coding in the glabrous skin of the human hand , 1983, Trends in Neurosciences.

[41]  H. E. Torebjörk,et al.  Peripheral projections of nerve fibres in the human median nerve , 1983, Brain Research.

[42]  H. E. Torebjörk,et al.  Peripheral projections of fascicles in the human median nerve. , 1983, Brain : a journal of neurology.