The spatial characteristics of the painful thermal grill illusion

&NA; Interlaced cold and warm stimuli may induce a paradoxical burning sensation termed the “thermal grill illusion”. Studies on the grill illusion have yielded contradictory results regarding its quality and intensity, which in turn led to controversies concerning the underlying mechanism. Some controversies may result from testing the illusion with absolute temperatures thereby disregarding inter‐subjects’ variation in temperature sensitivity. Therefore, our aim was to measure the individual threshold of the painful grill illusion (PGI). Another aim was to measure, here for the first time, the spatial boundaries of the PGI by spatially separating between the cooling and warming stimuli. Subjects (10 males, 15 females) underwent measurements of heat‐pain (HPT) and cold‐pain thresholds (CPT) with 9 and 18 cm2 stimulating probes, on the forearm. Subjects also underwent measurement of pain threshold (PT), with one cooling and one heating probe (9 cm2 each) activated simultaneously, and separated by 0–30 cm (distances encompassing one or two dermatomes). Simultaneous cold and warm stimuli produced burning pain at all separation distances. PT (∼26 and 38 °C) was significantly lower than CPT and HPT, respectively, and was relatively fixed across all distances except for 30 cm at which PT increased towards CPT and HPT values. Gender did not affect the PGI. In conclusion, innocuous cold and warm stimuli can spatially summate, both within and between dermatomes and evoke a PGI. Possibly, non‐nociceptive channels integrate onto 2nd or 3rd order nociceptive neurons which in turn induce a unique painful burning resulting from the blend of cold and warm sensations.

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

[2]  N. Blumen,et al.  Sensory determinants of thermal pain. , 2002, Brain : a journal of neurology.

[3]  William D. Willis,et al.  The cells of origin of the primate spinothalamic tract , 1979, The Journal of comparative neurology.

[4]  The Spatial Condition of the Fusion of Warmth and Cold in Heat , 1920 .

[5]  P. Mantyh,et al.  Enhanced responses of spinal dorsal horn neurons to heat and cold stimuli following mild freeze injury to the skin. , 2001, Journal of neurophysiology.

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

[7]  George L. Wilcox,et al.  An instrument using a multiple layer peltier device to change skin temperature rapidly , 1984, Brain Research Bulletin.

[8]  Sydney Alrutz.  X.–NOTESON THE TEMPERATURE-SENSES. II. , 1898 .

[9]  S. Zeger,et al.  Longitudinal data analysis using generalized linear models , 1986 .

[10]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[11]  H. E. Torebjörk,et al.  Nociceptors and warm receptors innervated by C fibres in human skin. , 1982, Journal of neurology, neurosurgery, and psychiatry.

[12]  F. Morain,et al.  Investigation of the paradoxical painful sensation (‘illusion of pain’) produced by a thermal grill , 2005, Pain.

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

[14]  Jürgen Lorenz,et al.  Thermoreceptive innervation of human glabrous and hairy skin: a contact heat evoked potential analysis , 2005, Pain.

[15]  H. E. Torebjörk,et al.  Afferent C units responding to mechanical, thermal and chemical stimuli in human non-glabrous skin. , 1974, Acta physiologica Scandinavica.

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

[17]  R. Defrin,et al.  Spatial summation and spatial discrimination of pain sensation , 2006, Pain.

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

[19]  David Yarnitsky,et al.  Paradoxical heat sensation in healthy subjects: peripherally conducted by Aδ or C fibres? , 1999 .

[20]  Karen D Davis,et al.  Cold-evoked pain varies with skin type and cooling rate: a psychophysical study in humans , 1999, PAIN.

[21]  L. Watkins,et al.  Spatial summation in human thermal pain perception: comparison within and between dermatomes , 1992, Pain.

[22]  B. Green,et al.  Synthetic heat at mild temperatures , 2002, Somatosensory & motor research.

[23]  R. Dykes,et al.  "Cold" fiber population innervating palmar and digital skin of the monkey: responses to cooling pulses. , 1973, Journal of neurophysiology.

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

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

[26]  R. LaMotte,et al.  Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: simultaneous recordings in humans of sensory judgments of pain and evoked responses in nociceptors with C-fibers. , 1984, Journal of neurophysiology.

[27]  R. Dubner,et al.  Response of unmyelinated (C) polymodal nociceptors to thermal stimuli applied to monkey's face , 1976 .

[28]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[29]  W. Macrae.  The Pain System , 2005 .

[30]  J. Ochoa,et al.  Quantitative somatosensory thermotest. A key method for functional evaluation of small calibre afferent channels. , 1992, Brain : a journal of neurology.

[31]  M. Bushnell,et al.  Wide-dynamic-range dorsal horn neurons participate in the encoding process by which monkeys perceive the intensity of noxious heat stimuli , 1986, Brain Research.

[32]  R. Duclaux.  [Cutaneous thermoreceptors]. , 1977, Journal de physiologie.

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

[34]  Barry G. Green, Rya Zaharchuk.  Spatial variation in sensitivity as a factor in measurements of spatial summation of warmth and cold , 2001, Somatosensory & motor research.

[35]  H. Fruhstorfer,et al.  The significance of A‐δ and C fibres for the perception of synthetic heat , 2003 .

[36]  H. Fruhstorfer,et al.  The significance of A-delta and C fibres for the perception of synthetic heat. , 2003, European journal of pain.

[37]  Mark S. Wallace,et al.  Qualitative and quantitative characterization of the thermal grill , 2005, Pain.

[38]  K. M. Dallenbach,et al.  The Experience of Heat , 1927 .

[39]  D. Price,et al.  Neurophysiological characterization of the anterolateral spinal cord neurons contributing to pain perception in man , 1975, Pain.

[40]  L. Arendt-Nielsen,et al.  Spatial summation of heat induced pain within and between dermatomes. , 1997, Somatosensory & motor research.

[41]  E. Perl,et al.  Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: Indications of their place in dorsal horn functional organization , 1978, The Journal of comparative neurology.

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

[43]  F. Konietzny.  Peripheral neural correlates of temperature sensations in man. , 1984, Human neurobiology.

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

[45]  E. Perl,et al.  Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. , 1970, Journal of neurophysiology.