Cold-evoked pain varies with skin type and cooling rate: a psychophysical study in humans

The psychophysical responses to noxious cold stimulation of the skin in normal human subjects are not well understood. Continuous pain ratings with the visual analogue scale is an important method to assess these responses. In this study, we addressed several important issues about the parameters with which stimuli are delivered: the type of skin stimulated, the rate with which the stimulus temperature decreases, and the dimension of the pain rated by subjects. Cold stimuli were delivered to the thenar eminence (glabrous skin) and the dorso-lateral hand (hairy skin) via a 4 cm(2) Peltier-type stimulator. Cold and pain thresholds were determined by the method of limits (MOL). A computerized visual analogue scale (VAS) was used to obtain continuous ratings of pain intensity and affect. The McGill Pain Questionnaire (MPQ) was used to assess the quality of cold-evoked pain. Supra-threshold stimuli (34 degrees C base) were delivered at 0.5, 1 or 2 degrees C/s to 2 degrees C, held for 20s and returned to baseline at 9 degrees C/s. These studies revealed: (1) Cold thresholds, measured with MOL, were lower (i.e. occurred at higher absolute temperatures) for the hairy skin of the dorso-lateral hand compared to the glabrous skin of the thenar eminence. (2) A similar pattern was evident for cold induced pain thresholds with MOL at 1.5 degrees C/s and with intensity and affect VAS scales at 0.5 and 1 degrees C/s. (3) Exponents for supra-threshold ratings fit to power functions were larger for the glabrous skin site than the hairy skin site regardless of cooling rate or dimension of pain measured. (4) All pain indices were higher for slower cooling rates. (5) No significant differences were found in the pain indices for pain ratings of intensity and affect. (6) A substantial proportion of subjects chose words representing paradoxical heat with the MPQ. (7) Painful paradoxical heat sensations occurred most often during cooling, while innocuous warm sensations mainly occurred during the rewarming phase.

[1]  S. Chéry-croze Relationship between noxious cold stimuli and the magnitude of pain sensation in man , 1983, Pain.

[2]  R. Duclaux,et al.  Thermal pain in humans: influence of the rate of stimulation , 1978, Brain Research.

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

[4]  Body site variation of cool perception thresholds, with observations on paradoxical heat. , 1993, Somatosensory & motor research.

[5]  D. Burke,et al.  Fibre function and perception during cutaneous nerve block. , 1975, Proceedings of the Australian Association of Neurologists.

[6]  D. Price,et al.  A psychophysical analysis of experiential factors that selectively influence the affective dimension of pain , 1980, Pain.

[7]  G. E. Goldsmith,et al.  Sensory processing in a thermal afferent pathway. , 1985, Journal of neurophysiology.

[8]  H. Hämäläinen,et al.  Paradoxical heat sensations during moderate cooling of the skin , 1982, Brain Research.

[9]  J T Whitton,et al.  The thickness of the epidermis , 1973, The British journal of dermatology.

[10]  H. Fruhstorfer,et al.  Method for quantitative estimation of thermal thresholds in patients. , 1976, Journal of neurology, neurosurgery, and psychiatry.

[11]  K. Davis Cold-induced pain and prickle in the glabrous and hairy skin , 1998, Pain.

[12]  E. Fleischer,et al.  Unmyelinated nociceptive units in two skin areas of the rat , 1983, Brain Research.

[13]  K. O. Johnson,et al.  Peripheral neural determinants of temperature discrimination in man: a correlative study of responses to cooling skin. , 1973, Journal of neurophysiology.

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

[15]  Robert H. LaMotte,et al.  Response properties of high-threshold cutaneous cold receptors in the primate , 1982, Brain Research.

[16]  Discrimination of painful stimuli in human beings: influence of stimulation area. , 1980, Journal of neurophysiology.

[17]  Influence of caffeine, sweating and local hyperemisation on “Marstock” thermotesting , 1992, Acta neurologica Scandinavica.

[18]  Antti Pertovaara,et al.  Influence of the rate of temperature change on thermal thresholds in man , 1985, Experimental Neurology.

[19]  M. Bushnell,et al.  The thermal grill illusion: unmasking the burn of cold pain. , 1994, Science.

[20]  R. Meyer,et al.  Evidence for two different heat transduction mechanisms in nociceptive primary afferents innervating monkey skin. , 1995, The Journal of physiology.

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

[22]  H. Fruhstorfer Thermal sensibility changes during ischemie nerve block , 1984, Pain.

[23]  H. Hensel Thermal sensations and thermoreceptors in man , 1982 .

[24]  D. Kenshalo,et al.  Response characteristics of cutaneous warm receptors in the monkey. , 1977, Journal of neurophysiology.

[25]  D. Yeomans,et al.  Nociceptive responses to high and low rates of noxious cutaneous heating are mediated by different nociceptors in the rat: behavioral evidence , 1996, Pain.

[26]  R. Gracely,et al.  Semantic functional measurement of pain: Integrating perception and language , 1983, Pain.

[27]  J. Arndt,et al.  Pain evoked by polymodal stimulation of hand veins in humans. , 1991, The Journal of physiology.

[28]  J. Ochoa,et al.  The triple cold syndrome. Cold hyperalgesia, cold hypoaesthesia and cold skin in peripheral nerve disease. , 1994, Brain : a journal of neurology.

[29]  Apostolos P. Georgopoulos,et al.  Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin , 1976 .

[30]  R. Dubner,et al.  A peripheral "cold" fiber population responsive to innocuous and noxious thermal stimuli applied to monkey's face. , 1975, Journal of neurophysiology.

[31]  B. Green,et al.  Localization of thermal sensation: An illusion and synthetic heat , 1977 .

[32]  A. Iggo,et al.  Conduction failure in myelinated and non‐myelinated axons at low temperatures , 1968, The Journal of physiology.

[33]  M. Bushnell,et al.  Temporal and qualitative properties of cold pain and heat pain: a psychophysical study , 1998, Pain.

[34]  R. Dubner,et al.  Validity and sensitivity of ratio scales of sensory and affective verbal pain descriptors: Manipulation of affect by diazepam , 1978, Pain.

[35]  D. Yarnitsky,et al.  Single C nociceptor responses and psychophysical parameters of evoked pain: effect of rate of rise of heat stimuli in humans. , 1992, The Journal of physiology.

[36]  James N. Campbell,et al.  Cutaneous injection of the capsaicin analogue, NE-21610, produces analgesia to heat but not to mechanical stimuli in man , 1992, Pain.

[37]  K. Hagbarth,et al.  Regional similarities and differences in thermoregulatory vaso‐ and sudomotor tone. , 1980, The Journal of physiology.

[38]  G. E. Goldsmith,et al.  Facial sensitivity to rates of temperature change: neurophysiological and psychophysical evidence from cats and humans. , 1983, The Journal of physiology.

[39]  A. Iggo,et al.  Cutaneous thermoreceptors in primates and sub‐primates , 1969, The Journal of physiology.

[40]  S. Harkins,et al.  Sensory-affective relationships among different types of clinical and experimental pain , 1987, Pain.

[41]  J. C. Stevens,et al.  Temperature sensitivity of the body surface over the life span. , 1998, Somatosensory & motor research.

[42]  J. Dostrovsky,et al.  Altered pain and temperature perception following cingulotomy and capsulotomy in a patient with schizoaffective disorder , 1994, Pain.

[43]  J. Ochoa,et al.  Release of cold-induced burning pain by block of cold-specific afferent input. , 1990, Brain : a journal of neurology.

[44]  T. Morrow,et al.  Cutaneous pain and detection thresholds to short CO2 laser pulses in humans: Evidence on afferent mechanisms and the influence of varying stimulus conditions , 1988, Pain.

[45]  D. Kenshalo,et al.  Effect of cooling rate on the dynamic response of cat cold units , 1977, Experimental Neurology.

[46]  M. Denišlič,et al.  Quantitative assessment of thermal and pain sensitivity , 1994, Journal of the Neurological Sciences.

[47]  Ronald Dubner,et al.  Ratio scales of sensory and affective verbal pain descriptors , 1978, Pain.

[48]  R. Melzack The McGill Pain Questionnaire: Major properties and scoring methods , 1975, PAIN.

[49]  E. Torebjörk,et al.  Central suppression of cold-induced C fibre pain by myelinated fibre input , 1989, Pain.

[50]  M. Bushnell,et al.  Noxious and innocuous cold discrimination in humans: evidence for separate afferent channels , 1996, Pain.

[51]  M. Bushnell,et al.  Comparison of verbal and visual analogue scales for measuring the intensity and unpleasantness of experimental pain , 1989, Pain.

[52]  J. Ochoa,et al.  Warm and cold specific somatosensory systems. Psychophysical thresholds, reaction times and peripheral conduction velocities. , 1991, Brain : a journal of neurology.

[53]  David Yarnitsky,et al.  Studies of heat pain sensation in man: perception thresholds, rate of stimulus rise and reaction time , 1990, Pain.

[54]  R. Treede,et al.  Paradoxical heat sensation in patients with multiple sclerosis. Evidence for a supraspinal integration of temperature sensation. , 1996, Brain : a journal of neurology.

[55]  M. Bushnell,et al.  A psychophysical comparison of sensory and affective responses to four modalities of experimental pain. , 1992, Somatosensory & motor research.

[56]  J. Ochoa,et al.  Sensations evoked by intraneural microstimulation of C nociceptor fibres in human skin nerves. , 1989, The Journal of physiology.

[57]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[58]  H. Handwerker,et al.  Discharge patterns of human C-fibers induced by itching and burning stimuli. , 1991, Journal of neurophysiology.

[59]  J. Serra,et al.  C‐polymodal nociceptors activated by noxious low temperature in human skin. , 1996, The Journal of physiology.

[60]  D. Price,et al.  The validation of visual analogue scales as ratio scale measures for chronic and experimental pain , 1983, Pain.

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