Sensations evoked by microstimulation of single mechanoreceptive afferents innervating the human face and mouth.

Intraneural microneurography and microstimulation were performed on single afferent axons in the inferior alveolar and lingual nerves innervating the face, teeth, labial, or oral mucosa. Using natural mechanical stimuli, 35 single mechanoreceptive afferents were characterized with respect to unit type [fast adapting type I (FA I), FA hair, slowly adapting type I and II (SA I and SA II), periodontal, and deep tongue units] as well as size and shape of the receptive field. All afferents were subsequently microstimulated with pulse trains at 30 Hz lasting 1.0 s. Afferents recordings whose were stable thereafter were also tested with single pulses and pulse trains at 5 and 60 Hz. The results revealed that electrical stimulation of single FA I, FA hair, and SA I afferents from the orofacial region can evoke a percept that is spatially matched to the afferent's receptive field and consistent with the afferent's response properties as observed on natural mechanical stimulation. Stimulation of FA afferents typically evoked sensations that were vibratory in nature; whereas those of SA I afferents were felt as constant pressure. These afferents terminate superficially in the orofacial tissues and seem to have a particularly powerful access to perceptual levels. In contrast, microstimulation of single periodontal, SA II, and deep tongue afferents failed to evoke a sensation that matched the receptive field of the afferent. These afferents terminate more deeply in the tissues, are often active in the absence of external stimulation, and probably access perceptual levels only when multiple afferents are stimulated. It is suggested that the spontaneously active afferents that monitor tension in collagen fibers (SA II and periodontal afferents) may have the role to register the mechanical state of the soft tissues, which has been hypothesized to help maintain the body's representation in the central somatosensory system.

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

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

[3]  A. Vallbo,et al.  Intraneural microstimulation in man. Its relation to specificity of tactile sensations. , 1987, Brain : a journal of neurology.

[4]  H. E. Torebjörk,et al.  Projected and receptive fields: a comparison of projected areas of sensations evoked by intraneural stimulation of mechanoreceptive units, and their innervation territories. , 1983, Acta physiologica Scandinavica.

[5]  R. S. Johansson,et al.  Mechanoreceptor activity from the human face and oral mucosa , 2004, Experimental Brain Research.

[6]  M. Trulsson,et al.  Receptor encoding of moving tactile stimuli in humans. I. Temporal pattern of discharge of individual low-threshold mechanoreceptors , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. Johansson,et al.  Slowly Adapting Mechanoreceptors in the Borders of the Human Fingernail Encode Fingertip Forces , 2009, The Journal of Neuroscience.

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

[9]  M. Trulsson,et al.  Receptive field properties of human periodontal afferents responding to loading of premolar and molar teeth. , 2003, Journal of neurophysiology.

[10]  D. Burke,et al.  Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. , 1990, The Journal of physiology.

[11]  M. Trulsson Sensory-motor function of human periodontal mechanoreceptors. , 2006, Journal of oral rehabilitation.

[12]  R S Johansson,et al.  Directional sensitivity of human periodontal mechanoreceptive afferents to forces applied to the teeth. , 1992, The Journal of physiology.

[13]  M. Trulsson Multiple-tooth receptive fields of single human periodontal mechanoreceptive afferents. , 1993, Journal of neurophysiology.

[14]  Steven M. Barlow,et al.  Mechanical frequency detection thresholds in the human face , 1987, Experimental Neurology.

[15]  M. Nordin,et al.  Mechanoreceptive units in the human infra-orbital nerve. , 1989, Acta physiologica Scandinavica.

[16]  J. Ochoa,et al.  Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. , 1983, The Journal of physiology.

[17]  R. Johansson,et al.  ENCODING OF TOOTH LOADS BY HUMAN PERIODONTAL AFFERENTS AND THEIR ROLE IN JAW MOTOR CONTROL , 1996, Progress in Neurobiology.

[18]  Benoni B. Edin,et al.  Single unit retrieval in microneurography: a microprocessor-based device controlled by an operator , 1988, Journal of Neuroscience Methods.

[19]  Cortical responses to single mechanoreceptive afferent microstimulation revealed with fMRI , 2000, NeuroImage.

[20]  S. Yamane,et al.  What facial features activate face neurons in the inferotemporal cortex of the monkey? , 2004, Experimental Brain Research.

[21]  Uwe Proske,et al.  Kinesthesia: The role of muscle receptors , 2006, Muscle & nerve.

[22]  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.

[23]  A B Vallbo,et al.  Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. , 1995, The Journal of physiology.

[24]  R. Johansson,et al.  Mechanoreceptive afferent activity in the infraorbital nerve in man during speech and chewing movements , 2004, Experimental Brain Research.

[25]  G. Essick,et al.  Low-threshold mechanoreceptive afferents in the human lingual nerve. , 1997, Journal of neurophysiology.

[26]  Roland S Johansson,et al.  Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors , 2002, Behavioural Brain Research.

[27]  R. Johansson,et al.  Microelectrode recordings from human oral mechanoreceptors , 1976, Brain Research.

[28]  '. B.Vallbo Properties of cutaneous mechanoreceptors in the human hand-related to touch sensation , 1999 .

[29]  M. Byers Sensory innervation of periodontal ligament of rat molars consists of unencapsulated Ruffini‐like mechanoreceptors and free nerve endings , 1985, The Journal of comparative neurology.

[30]  M. Trulsson,et al.  Periodic microstimulation of single mechanoreceptive afferents produces frequency-following responses in human EEG. , 1997, Journal of neurophysiology.

[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]  M. Knibestöl,et al.  Single unit analysis of mechanoreceptor activity from the human glabrous skin. , 1970, Acta physiologica Scandinavica.

[33]  R. Melzack,et al.  Experimental phantom limbs. , 1973, Experimental neurology.

[34]  F. J. Clark,et al.  Microstimulation of single tactile afferents from the human hand. Sensory attributes related to unit type and properties of receptive fields. , 1984, Brain : a journal of neurology.

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

[36]  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.