Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin.

1. Mechano‐ and heat‐sensitive A fibre nociceptors (AMHs) and C fibre nociceptors (CMHs) in hairy skin (forty‐six AMHs and twenty‐one CMHs) and in glabrous skin (fifty‐nine AMHs and ten CMHs) of anaesthetized monkeys were tested with a 30 s, 53 degrees C heat stimulus, delivered by a laser thermal stimulator (0.1 s rise time, 7.5 mm diameter). 2. Two types of heat response were observed in hairy skin AMHs. Type I AMHs had a peak discharge towards the end of the stimulus, response latencies to heat of up to several seconds, a median heat threshold greater than 53 degrees C, and a mean conduction velocity of 25 m s‐1 (n = 33). Type II AMHs had a peak discharge within 1‐3 s, a mean response latency of 120 ms, a median heat threshold of 46 degrees C, and a mean conduction velocity of 15 m s‐1 (n = 13). Type I AMH fibres were sensitized to heat, whereas heat responses of type II AMHs were suppressed following the intense heat stimulus. 3. In glabrous skin, only type I AMHs were found. The absence of type II AMHs is consistent with the absence of first pain to heat in glabrous skin. 4. C fibre nociceptors in hairy skin had a peak discharge near stimulus onset, a mean response latency of 100 ms and a median heat threshold of 41 degrees C. Heat responses of CMHs in glabrous skin were not significantly different from those in hairy skin. 5. Only type II AMHs had response latencies that were short enough to explain first pain to heat. Heat thresholds of type II AMHs were significantly higher than those of CMHs. 6. These results suggest two different heat transduction mechanisms in nociceptive afferents. For one, heat energy is quickly transduced into action potentials, and the peak discharge is reached soon after stimulus onset. For the other, the transduction of heat is distinctly slower, and the peak discharge occurs near the end of the stimulus. Chemically mediated sensitization may be involved in the second transduction mechanism.

[1]  James N. Campbell,et al.  Latency to detection of first pain , 1983, Brain Research.

[2]  A. Iggo,et al.  Primate cutaneous thermal nociceptors. , 1971, The Journal of physiology.

[3]  E. Perl,et al.  Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. , 1969, Journal of neurophysiology.

[4]  Richard A. Meyer,et al.  A Laser Stimulator for the Study of Cutaneous Thermal and Pain Sensations , 1976, IEEE Transactions on Biomedical Engineering.

[5]  R. Meyer,et al.  Chemosensitivity and sensitization of nociceptive afferents that innervate the hairy skin of monkey. , 1993, Journal of neurophysiology.

[6]  B Bromm,et al.  Late somatosensory evoked cerebral potentials in response to cutaneous heat stimuli. , 1988, Electroencephalography and clinical neurophysiology.

[7]  R. Meyer,et al.  Responses to heat of C-fiber nociceptors in monkey are altered by injury in the receptive field but not by adjacent injury , 1988, Pain.

[8]  K. D. Davis,et al.  Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey , 1990, Pain.

[9]  R. Treede,et al.  Nerve fibre discharges, cerebral potentials and sensations induced by CO2 laser stimulation. , 1984, Human neurobiology.

[10]  B. Matthews Responses of intradental nerves to electrical and thermal stimulation of teeth in dogs. , 1977, The Journal of physiology.

[11]  R. Kakigi,et al.  Estimation of conduction velocity of Aδ fibers in humans , 1991 .

[12]  Jens Schouenborg,et al.  Multiple spinal pathways mediate cutaneous nociceptive C fibre input to the primary somatosensory cortex (SI) in the rat , 1993, Brain Research.

[13]  R. Meyer,et al.  Sensitization of unmyelinated nociceptive afferents in monkey varies with skin type. , 1983, Journal of neurophysiology.

[14]  R. Meyer,et al.  Myelinated nociceptive afferents account for the hyperalgesia that follows a burn to the hand. , 1981, Science.

[15]  B. Lynn,et al.  The sensitization of high threshold mechanoreceptors with myelinated axons by repeated heating. , 1977, The Journal of physiology.

[16]  R. Treede,et al.  Pain related cerebral potentials: late and ultralate components. , 1987, The International journal of neuroscience.

[17]  K L Casey,et al.  Variability of laser-evoked potentials: attention, arousal and lateralized differences. , 1993, Electroencephalography and clinical neurophysiology.

[18]  J. Gybels,et al.  Latencies of chemically evoked discharges in human cutaneous nociceptors and of the concurrent subjective sensations , 1980, Neuroscience Letters.

[19]  H. Handwerker,et al.  Chemosensitivity of fine afferents from rat skin in vitro. , 1990, Journal of neurophysiology.

[20]  R. Meyer,et al.  Sensitization of myelinated nociceptive afferents that innervate monkey hand. , 1979, Journal of neurophysiology.

[21]  R. LaMotte,et al.  Comparison of responses of warm and nociceptive C-fiber afferents in monkey with human judgments of thermal pain. , 1978, Journal of neurophysiology.

[22]  W. Willis,et al.  Differential activation and classification of cutaneous afferents in the rat. , 1993, Journal of neurophysiology.

[23]  J. Gybels,et al.  Response properties of thin myelinated (A-delta) fibers in human skin nerves. , 1983, Journal of neurophysiology.

[24]  E. Perl,et al.  Myelinated afferent fibres innervating the primate skin and their response to noxious stimuli , 1968, The Journal of physiology.

[25]  S. Kilo,et al.  Unresponsive afferent nerve fibres in the sural nerve of the rat. , 1991, The Journal of physiology.

[26]  R. LaMotte,et al.  Peripheral neural mechanisms of cutaneous hyperalgesia following mild injury by heat , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  R. Frostig,et al.  Primary afferent and spinal sensory neurons that respond to brief pulses of intense infrared laser radiation: A preliminary survey in rats , 1982, Experimental Neurology.

[28]  R. Meyer,et al.  Comparison of heat and mechanical receptive fields of cutaneous C-fiber nociceptors in monkey. , 1990, Journal of neurophysiology.

[29]  C J Robinson,et al.  Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: a comparison of neural events in monkey with sensory judgments in human. , 1983, Journal of neurophysiology.

[30]  R. Treede,et al.  Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. , 1993, Electroencephalography and clinical neurophysiology.

[31]  W D Willis,et al.  Classification of primate spinothalamic and somatosensory thalamic neurons based on cluster analysis. , 1986, Journal of neurophysiology.

[32]  A. Carmon,et al.  Peripheral fiber correlates to noxious thermal stimulation in humans , 1980, Neuroscience Letters.

[33]  H. Kawamura,et al.  Cerebral-evoked responses elicited by direct stimulation of the lateral spinothalamic tract in the human. , 1985, Applied Neurophysiology.