Comprehensive Physiology Wiley Online Library

Peripheral Thermosensors

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Dual Concept: Warm and Cold Sensors
1.1 Structure and Localization of Thermosensors
2 Electrophysiological Characterization
2.1 General Properties of Thermosensors
2.2 Static and Dynamic Activity of Warm Sensors
2.3 Static and Dynamic Activity of Cold Sensors
2.4 Special Functions: Orientation, Prey Detection
2.5 Burst Discharge
2.6 Transducer Mechanisms
3 Sensitivity Adjustment of Peripheral Thermosensors
3.1 Adaptation to Environmental Temperatures
3.2 Adjustment by Sympathetic Outflow and Endogenous Substances
4 Neuropeptides and Capsaicin Sensitivity of Warm Sensors
5 Processing of Thermal Afferents
5.1 Trigeminal Nuclei
5.2 Spinal Segmental Level
5.3 Ascending Pathways
5.4 Descending Control
6 Conclusions
Figure 1. Figure 1.

Average discharge rate of warm sensors from different animals at maintained temperatures, demonstrating different operating ranges and maximal values. Note low threshold for warm sensors of boa constrictor and vampire bat (prey detector) and pigeons. Warm sensors not showing bell‐shaped frequency/temperature relations similar to those of pigeons and vampire bat have been demonstrated as a minor population in most animals. Inset: Transient discharge in response to a fast warming step of boa and cat warm sensors, respectively. Note short transient response, followed by transient attenuation of boa sensor compared to 30s adaptation of cat sensor. (1) Hensel and Kenshalo 88, (2) Necker 148, (3) Duclaux and Kenshalo 50, (4) Schäfer et al. 183, (5) Hensel 81.

Figure 2. Figure 2.

Change of discharge pattern of cat lingual cold sensor during periodic temperature changes of 1°C from adaptation temperatures of 27.2 and 21.1°C, respectively. Cold sensors follow these slow and small temperature changes without reasonable time‐lag. Transition between triplets and regular discharge at 27.2°C and between triplets and doublets at 21.1°C; note different time values. Frequency period 0.1 Hz corresponding to rate of temperature change of 0.1°C/s.

Figure 3. Figure 3.

Interval histograms of discharge activity of lingual cold sensor at three different adapting temperatures before (upper line) and after (lower line) injection of 0.025 mg ouabain into lingual artery. Ouabain increases firing rate (f) and may induce or increase bursting discharge at temperatures above 20°C. Induction of bursting is indicated by the double peak after ouabain in the preparation adapted to 27.6°C. Numbers above peaks indicate peak values of intervals. After Pierau et al. 165.



Figure 1.

Average discharge rate of warm sensors from different animals at maintained temperatures, demonstrating different operating ranges and maximal values. Note low threshold for warm sensors of boa constrictor and vampire bat (prey detector) and pigeons. Warm sensors not showing bell‐shaped frequency/temperature relations similar to those of pigeons and vampire bat have been demonstrated as a minor population in most animals. Inset: Transient discharge in response to a fast warming step of boa and cat warm sensors, respectively. Note short transient response, followed by transient attenuation of boa sensor compared to 30s adaptation of cat sensor. (1) Hensel and Kenshalo 88, (2) Necker 148, (3) Duclaux and Kenshalo 50, (4) Schäfer et al. 183, (5) Hensel 81.



Figure 2.

Change of discharge pattern of cat lingual cold sensor during periodic temperature changes of 1°C from adaptation temperatures of 27.2 and 21.1°C, respectively. Cold sensors follow these slow and small temperature changes without reasonable time‐lag. Transition between triplets and regular discharge at 27.2°C and between triplets and doublets at 21.1°C; note different time values. Frequency period 0.1 Hz corresponding to rate of temperature change of 0.1°C/s.



Figure 3.

Interval histograms of discharge activity of lingual cold sensor at three different adapting temperatures before (upper line) and after (lower line) injection of 0.025 mg ouabain into lingual artery. Ouabain increases firing rate (f) and may induce or increase bursting discharge at temperatures above 20°C. Induction of bursting is indicated by the double peak after ouabain in the preparation adapted to 27.6°C. Numbers above peaks indicate peak values of intervals. After Pierau et al. 165.

References
 1. Akaike, N., K. S. Lee, and A. M. Brown. The calcium current of helix neuron. J. Gen. Physiol. 71: 509–531, 1978.
 2. Akoev, G. N., O. B. Ilyinski, and P. M. Zadan. Response of electroreceptors (ampullae of Lorenzini) of skates to electric and magnetic fields. J. Comp. Physiol. [A] 106: 127–136, 1976.
 3. Akoev, G. N., N. O. Volpe, and G. G. Zhadan. Analysis of effects of chemical and thermal stimuli of the ampullae of Lorenzini of the skate. Comp. Biochem. Physiol. 65A: 193–201 1980.
 4. Bade, H., H. A. Braun, and H. Hensel. Parameters of the static burst discharge of lingual cold receptors in the cat. Pflugers Arch. 382: 1–5, 1979.
 5. Bähr, R., K. Blumberg, and W. Jänig. Do dichotomizing afferent fibers exist which supply visceral organs as well as somatic structures? A contribution to the problem of referred pain. Neurosci. Lew. 24: 25–28, 1981.
 6. Bauman, T. K., D. A. Simone, C. N. Shain, and R. H. LaMotte. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin‐induced pain and hyperalgesia. J. Neurophysiol. 66: 212–227, 1991.
 7. Bazett, H. C. Regulation of body temperature. In: Physiology of Heat Regulation and the Science of Clothing, edited by New‐burgh. Philadelphia: 1949.
 8. Beitel, R. E., and R. Dubner. Response of unmyelinated (C) polymodal nociceptors to thermal stimuli applied to monkey's face. J. Neurophysiol. 39: 1160–1175, 1976.
 9. Beitel, R. E., R. Dubner, R. Harris, and R. Sumino. Role of thermoreceptive afferents in behavioral reaction times to warming temperature shifts applied to the monkey's face. Brain Res. 138: 329–346, 1977.
 10. Benzing, H., H. Hensel, and R. Wurster. Integrated static activity of lingual cold receptors. Pflugers Arch. 311: 50–54, 1969.
 11. Berkes, S., and A. Cost. Aktivitätsparameter temperaturreaktiver Hinterhornneurone von intakten und chronisch spinalisierten Ratten. (Inaugural diss., University of Gießen, 1980).
 12. Bing, H. I., and A. P. Skouby. Sensitization of cold receptors by substances with acetylcholine effect. Acta Physiol. Scand. 21: 286–302, 1950.
 13. Bleichmar, H., and E. De Robertis. Submicroscopic morphology of the infrared receptor of pit vipers. Z. Zellforsch. 56: 748–761, 1962.
 14. Boman, K. K. A. Electrophysiologische Untersuchungen über die Thermoreceptoren der Gesichtshaut. Acta Physiol. Scand. 44 (Suppl. 149): 5–78, 1958.
 15. Braun, H. A., H. Bade, and H. Hensel. Static and dynamic discharge patterns of bursting cold fibers related to hypothetical receptor mechanisms. Pflugers Arch. 386: 1–9, 1980.
 16. Braun, H. A., K. Schäfer, and H. Wissing. Theories and models of temperature transduction. In: Thermoreception and Temperature Transduction, edited by J. Bligh and K. H. Voigt. Heidelberg: Springer‐Verlag, 1990, p. 19–29.
 17. Bromm, B., H. Hensel, and A. T. Tagmut. The electrosensitivity of the isolated ampullae of Lorenzini in the crayfish. J. Comp. Physiol. 111: 127–136, 1976.
 18. Brück, K., and P. Hinckel. Thermoregulatory noradrenergic and serotonergic pathways to hypothalamic units. J. Physiol. (Lond.) 304: 192–202, 1980.
 19. Brück, K., and P. Hinckel. Thermoafferent systems and their adaptive modification. Pharmacol. Ther. 17: 357–381, 1982.
 20. Bullock, T. H. Electroreception. Annu. Rev. Neurosci. 5: 121–170, 1982.
 21. Bullock, T. H., and F. P. J. Diecke. Properties of an infra‐red receptor. J. Physiol. 134: 47–87, 1956.
 22. Bullock, T. H., and W. Fox. The anatomy of the infrared sense organ in the facial pit of pit vipers. Q. J. Microsc. Sci. 98: 219–234, 1957.
 23. Burton, H. Responses of spinal cord neurons to systematic changes in hindlimb skin temperatures in cats and primates. J. Neurophysiol. 38: 1060–1079, 1975
 24. Cabanac, M., and H. Brinnel. Blood flow in the emissary veins of the human head during hyperthermia. Eur. J. Appl. Physiol. 54: 172–176, 1985.
 25. Calvin, W. H. Synaptic potential summation and repetitive firing mechanisms: input‐output theory for the recruitment of neurons into epileptic bursting firing patterns. Brain Res. 39: 71–94, 1972.
 26. Calvin, W. H. Generation of spike trains in CNS neurons. Brain Res. 84: 1–22, 1975.
 27. Carpenter, D. O. Membrane potential produced directly by the Na+ pump in Aplysia neurons. Comp. Biochem. Physiol. 35: 371–385 (1970).
 28. Carpenter, D. O., and B. O. Alving. A contribution of an electrogenic Na+ pump to membrane potential of Aplysia neurons. J. Gen. Physiol. 52: 1–21, 1968.
 29. Carpenter, D. O., and R. A. Gregg. Functional significance of electrogenic pumps in neurons. In: Electrogenic Transport: Fundamental Principles and Physiological Implications, edited by M. P. Blaustein, and M. Lieberman. New York: Raven, 1984, p. 253–270.
 30. Christensen, B. N., and E. R. Perl. Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J. Neurophysiol. 33: 293–307, 1970.
 31. Cost, A., S. Berkes, K. Tsuchiya, and F.‐K. Pierau. Response of dorsal horn neurones to thermal stimulation of the scrotal skin in chronically spinalized rats [Abstract]. Proc. Int. Congr. Physiol. Sci. 27th, Paris, 1977, vol. 13, p. 149.
 32. Courtney, K., G. Brengelman, and J. W. Sundsten. Evidence for spinal cord unit activity responsive to peripheral warming in the primate. Brain Res. 43: 657–661, 1972.
 33. Craig, A. D., and K. D. Kniffki. Lumbosacral lamina I cells projecting to medial and/or lateral thalamus in the cat [Abstract]. Soc. Neurosci. 8: 95, 1982.
 34. Crawshaw, L. I., E. R. Nadel, J. A. J. Stolwijk, and B. A. Stamford. Effect of local cooling on sweating rate and cold sensation. Pflugers Arch. 354: 19–27, 1975.
 35. Darian‐Smith, I., and R. W. Dykes. Peripheral neural mechanisms of thermal sensations. In: Oral–Facial Sensory and Motor Mechanisms, edited by R. Dubner, and Y. Kawamura. New York: Appleton‐Century Crofts Meredith, 1971, p. 7–22.
 36. Darian‐Smith, I., K. O. Johnson, and R. Dykes. “Cold” fiber population innervating palmar and digital skin of the monkey: responses to cooling pulses. J. Neurophysiol. 36: 325–346, 1973.
 37. Darian‐Smith, I., K. O. Johnson, C. LaMotte, Y. Shigenaga, P. Renins, and P. Champness. Warm fibers innervating palmar and digital skin of the monkey: response to thermal stimuli. J. Neurophysiol. 42: 1297–1315, 1979.
 38. Davies, S. N. Sympathetic modulation of cold‐receptive neurones in the trigeminal system of the rat. J. Physiol. (Lond.) 366: 315–329, 1985.
 39. Davies, S. N., G. E. Goldsmith, R. F. Hellon, and D. Mitchell. Facial sensitivity to rates of temperature change: neurophysiological and psychophysical evidence from cats and humans. J. Physiol. (Lond.) 344: 161–175, 1983.
 40. Davies, S. N., G. E. Goldsmith, R. F. Hellon, and D. Mitchell. Sensory processing in a thermal afferent pathway. J. Neurophysiol. 53: 429–434, 1985.
 41. Dawson, N. J., A. H. Dickenson, R. F. Hellon, and C. J. Woolf. Inhibitory controls on thermal neurones in the spinal trigeminal nucleus of cats and rats. Brain Res. 209: 440–445, 1981.
 42. Dawson, N. J., R. F. Hellon, and J.‐L. Saumet. Which classes of neurones project to the thalamus from the marginal layer of trigeminal nucleus caudalis in cats [Abstract]. J. Physiol. (Lond.) 341: 49P, 1983.
 43. Dickenson, A. H. Specific responses of rat raphe neurones to skin temperature. J. Physiol. (Lond.) 273: 277–293, 1977.
 44. Dickenson, A. H., R. F. Hellon, and D. C. M. Taylor. Facial thermal input to the trigeminal spinal nucleus of rabbits and rats. J. Comp. Neurol. 185: 203–210, 1979.
 45. Dodt, E., and J. B. Walther. Wirkungen zentrifugaler Nervenreizung auf Thermoreceptoren. Pflugers Arch. 265: 355–364, 1957.
 46. Dodt, E., and Y. Zotterman. Mode of action of warm receptors. Acta Physiol. Scand. 26: 345–357, 1952.
 47. Dodt, E., A. P. Skouby, and Y. Zotterman. The effect of cholinergic substances on the discharges from thermal receptors. Acta Physiol. Scand. 28: 101–114, 1953.
 48. Dostrovsky, J. O., and R. F. Hellon. The representation of facial temperature in the caudal trigeminal nucleus of the cat. J. Physiol. (Lond.) 277: 29–47, 1978.
 49. Dubner, R., R. Sumino, and W. I. Wood. A peripheral “cold” fiber population responsive to innocuous and noxious thermal stimuli applied to the monkey's face. J. Neurophysiol. 38: 1373–1389, 1975.
 50. Duclaux, R., and D. R. Kenshalo. Response characteristics of cutaneous warm receptors in the monkey. J. Neurophysiol. 43: 1–15, 1980.
 51. Duclaux, R., K. Schäfer, and H. Hensel. Response of cold receptors to low skin temperatures in nose of the cat. J. Neurophysiol. 43: 1571–1577, 1980.
 52. von During, M. The radiant heat receptor and other tissue receptors in the scales of the upper jaw of boa constrictor. Z. Anat. Entwickl.‐Gesch. 145: 299–319, 1974.
 53. Dykes, R. W. Coding of steady and transient temperatures by cutaneous “cold” fibers serving the hand of monkeys. Brain Res. 98: 485–500, 1975.
 54. Eckert, R., and H. D. Lux. A voltage‐sensitive persistent calcium conductance in neuronal somata of helix. J. Physiol. 254: 129–152, 1975.
 55. Foster, R. W., and A. G. Ramage. The action of some chemical irritants on somatosensory receptors of the cat. Neuropharmacology 20: 191–198, 1981.
 56. Gamow, R. I., and J. F. Harris. The infrared receptor of snakes. Sci. Am. 228: 94–100, 1973.
 57. Geisthövel, E., and E. Simon. Autonomic heat defense of ducks in comparison to mammals. In: Thermal Physiology, edited by J. R. S. Hales. New York: Raven, 1984, p. 29–32.
 58. Goldscheider, A. Revision der Lehre von Temperatursinn. Ber. v. Kongr. Exptl. Psychol. 5: 222, 1912.
 59. Goris, R. C., and S. Terashima. The structure and function of the infrared receptors of snakes. Prog. Brain Res. 43: 159–170, 1976.
 60. Gorman, A. L. F., and M. V. Thomas. Intracellular calcium accumulation during depolarization in a molluscan neurone. J. Physiol. (Lond.) 308: 259–285, 1980.
 61. Gorman, A. L. F., and M. V. Thomas. Potassium conductance and internal calcium accumulation in a molluscan neurone. J. Physiol. (Lond.) 308: 287–313, 1980.
 62. Gorman, A. L. F., A. Hermann, and M. V. Thomas. Ionic requirements for membrane oscillations and their dependence on the calcium concentrations in a molluscan pacemaker neurone. J. Physiol. 327: 185–217, 1982.
 63. Gottschlich, K.‐W., J. Werner, and G. Schingnitz. Thermoafferent signal processing in rats: an electrophysiological analysis of midbrain influences on thermoresponsive neurons in the ventrobasal thalamus. Pflugers Arch. 401: 91–96, 1984.
 64. Guieu, J.‐D., and R. F. Hellon. The chill sensation in fever. Pflugers Arch. 384: 103–104, 1980.
 65. Hagen, E., H. Knoche, D. C. Sinclair, and G. Weddell. The role of specialized nerve terminals in cutaneous sensibility. Proc. R. Soc. Lond. B Biol. Sci. 141: 279–287, 1953.
 66. Hales, J. R. S. Thermoregulatory requirements for circulatory adjustments to promote heat loss in animals. J. Therm. Biol. 8: 219–224, 1983.
 67. Handwerker, H. O. and P. W. Reeh. Pain and inflammation. In: Pain Research and Clinical Management, edited by M. R. Bond, J. E. Charlton, and C. J. Woolf. New York: Elsevier, 1991, p. 59–70.
 68. Handwerker, H. O., A. Iggo, H. Ogawa, and R. L. Ramsay. Input characteristics and rostral projection of dorsal horn neurones in the monkey. J. Physiol. 244: 76P–77P, 1974.
 69. Heinz, M., K. Schafer, and H. A. Braun. Analysis of facial cold receptor activity in the rat. Brain Res. 521: 289–295, 1990.
 70. Hellon, R. F., and N. K. Misra. Neurones in the dorsal horn of the rat responding to scrotal skin temperature changes. J. Physiol. 232: 375–388, 1973.
 71. Hellon, R. F., and D. Mitchell. Convergence in a thermal afferent pathway in the rat. J. Physiol. (Lond.) 248: 359–376, 1975.
 72. Hellon, R. F., and D. C. M. Taylor. An analysis of a thermal afferent pathway in the rat. J. Physiol. (Lond.) 326: 319–328, 1982.
 73. Hellon, R. F., N. J. Dawson, A. A. Young, and J. G. Herington. Warm‐rearing does not modify facial cold input. J. Therm. Biol. 8: 9, 1983.
 74. Hellon, R. F., H. Hensel, and K. Schäfer. Thermal receptors in the scrotum of the rat. J. Physiol. 248: 349–357, 1975.
 75. Hensel, H. Physiologie der Thermoreception. Ergebn. Physiol. 47: 166–368, 1952.
 76. Hensel, H. Das Verhalten der Thermoreceptoren bei Temperatursprüngen. Pflugers Arch. 256: 470–478, 1953.
 77. Hensel, H. C. Quantitative Beziehungen zwischen Temperaturreiz und Aktionspotentialen der Lorenzinischen Ampullen. Z. Vgl. Physiol. 37: 509–526, 1955.
 78. Hensel, H. Cutane Warmreceptoren bei Primaten. Pflugers Arch. 313: 150–152, 1969.
 79. Hensel, H. Temperature receptors in the skin. In: Physiological and Behavioral Temperature Regulation, edited by J. D. Hardy, A. P. Gagge, and J. A. J. Stolwijk. Springfield, IL: Thomas, 1970, p. 442–462.
 80. Hensel, H. Cutaneous thermoreceptors. In: Handbook of Sensory Physiology, edited by A. Iggo. New York: Springer‐Verlag, 1973, p. 79–110.
 81. Hensel, H. Static and dynamic activity of warm receptors in boa constrictor. Pflugers Arch. 353: 191–199, 1975.
 82. Hensel, H. Correlations of neural activity and thermal sensation in man. In: Sensory Functions of the Skin in Primates, edited by Y. Zotterman. Oxford: Pergamon, 1976, p. 331–353.
 83. Hensel, H. Thermoreception and temperature regulation. In: Monographs of the Physiological Society No. 38. New York: Academic, 1981.
 84. Hensel, H. Thermal sensations and thermoreceptors in man. In: Monograph in the Bannerstone Division of American Lectures in Living Chemistry. Springfield, IL: Thomas, 1982.
 85. Hensel, H., and M. Banet. Thermoreceptor activity, insulative and metabolic changes in cold and warm adapted cats. In: New Trends in Thermal Physiology, edited by Y. Houdas, and J. D. Guieu. Paris: Masson, 1978, p. 53–55.
 86. Hensel, H., and T. Huopaniemi. Static and dynamic properties of warm fibres in the infraorbital nerve. Pflugers Arch. 309: 1–10, 1969.
 87. Hensel, H., and A. Iggo. Analysis of cutaneous warm and cold fibres in primates. Pflugers Arch. 329: 1–8, 1971.
 88. Hensel, H., and D. R. Kenshalo. Warm receptors in the nasal region of cats. J. Physiol. (Lond.) 204: 99–112, 1969.
 89. Hensel, H., and K. Schäfer. Effects of calcium on warm and cold receptors. Pflugers Arch. 352: 87–90, 1974.
 90. Hensel, H., and K. Schäfer. Activity of warm receptors in boa constrictor raised at various temperatures. Pflugers Arch. 392: 95–98, 1981.
 91. Hensel, H., and K. Schäfer. Static and dynamic activity of cold receptors in cats after long‐term exposure to various temperatures. Pflugers Arch. 392: 291–294, 1982.
 92. Hensel, H., and I. Witt. Spatial temperature gradient and thermoreceptor stimulation. J. Physiol. (Lond.) 148: 180–189, 1959.
 93. Hensel, H., and R. D. Wurster. Static behaviour of cold receptors in the trigeminal area. Pflugers Arch. 313: 153–154, 1969.
 94. Hensel, H., and R. D. Wurster. Static properties of cold receptors in nasal area of cats. J. Neurophysiol. 33: 271–275, 1970.
 95. Hensel, H., and Y. Zotterman. Action potentials of cold fibres and intracutaneous temperature gradient. J. Neurophysiol. 14: 377–385, 1951.
 96. Hensel, H., and Y. Zotterman. The effect of menthol on the thermoreceptors. Acta Physiol. Scand. 24: 27–34, 1951.
 97. Hensel, H., K. H. Andres, and M. von During. Structure and function of cold receptors. Pflugers Arch. 352: 1–10, 1974.
 98. Hensel, H., A. Iggo, and I. Witt. A quantitative study of sensitive cutaneous thermoreceptors with C afferent fibres. J. Physiol. (Lond.) 153: 113–126, 1960.
 99. Hensel, H., L. Ström, and Y. Zotterman. Electrophysiological measurements of depth of thermoreceptors. J. Neurophysiol. 14: 423–429, 1951.
 100. Holzer, P. Local effector functions of capsaicin‐sensitive sensory nerve endings: involvement of tachykinins, calcitonin generelated peptide and other neuropeptides. Neuroscience 24: 739–768, 1988.
 101. Holzer, P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol. Rev. 43: 143–201, 1991.
 102. Hori, T. The capsaicin desensitized rat: behavioral thermoregulation and thermosensitivity of hypothalamic neurons. In: Thermoregulation Mechanisms and Their Therapeutic Implications, edited by B. Cox, P. Lomax, A. S. Milton, and E. Schönbaum. Basel: Karger, 1980, p. 214–215.
 103. Hori, T. Capsaicin and central control of thermoregulation. Pharmacol. Ther. 26: 389–416, 1984.
 104. Hori, T. An update on thermosensitive neurons in the brain: from cellular biology to thermal and non‐thermal homeostatic functions. Jpn. J. Physiol. 41: 1–22, 1991.
 105. Iggo, A. Cutaneous heat and cold receptors with slowly‐conducting (C) afferent fibers. Q. J. Exp. Physiol. 44: 362–370, 1959.
 106. Iggo, A. Cutaneous thermoreceptors in primates and sub‐primates. J. Physiol. (Lond.) 200: 403–430, 1969.
 107. Iggo, A., and A. S. Paintal. The metabolic dependence of primate cutaneous cold receptors. J. Physiol. 272: 40P–41P, 1977.
 108. Iggo, A., and R. F. Ramsay. Thermosensory mechanisms in the spinal cord of monkeys. In: Sensory Functions of the Skin in Primates, edited by Y. Zotterman. Oxford: Pergamon, 1976, p. 285–304.
 109. Iggo, A., and D. W. Young. Cutaneous thermoreceptors and thermal nociceptors. In: The Somatosensory System, edited by H. H. Kornhuber. Stuttgart: Thieme, 1975, p. 5–22.
 110. Ivanov, K. P., L. Dymnikova, and N. Danilova. The hypothalamus neurons' response to the signals from surface and deep skin thermoreceptors. J. Therm. Biol. 12: 289–293, 1987.
 111. Ivanov, K., V. Konstantinov, and N. Danilova. Thermoreceptor localization in the deep and surface skin layers. J. Therm. Biol. 7: 75–78, 1982.
 112. Ivanov, K. V. Konstantinov, N. Danilova, N. Sleptchuck, and G. Rumiantsev. Thermoreceptor distribution in different skin layers and its significance for thermoregulation. J. Therm. Biol. 11: 25–29, 1986.
 113. Jahns, R. Types of neuronal responses in the rat thalamus to peripheral temperature changes. Exp. Brain Res. 23: 157–166, 1975.
 114. Jahns, R. Different projection of cutaneous thermal inputs to single units of midbrain raphe nuclei. Brain Res. 101: 355–361, 1976.
 115. Jancsó‐Gábor, A., J. Szoksányi, and N. Jancsó. Irreversible impairment of thermoregulation induced by capsaicin and similar pungent substances in rats and guinea‐pigs. J. Physiol. (Lond.) 206: 495–507, 1970.
 116. Jancsó‐Gábor, A., J. Szoksányi, and N. Jancsó. Stimulation and desensitization of the hypothalamic heat‐sensitive structures by capsaicin in rats. J. Physiol. (Lond.) 208: 449–459, 1970.
 117. Johnson, K. O., I. Darian‐Smith, and C. LaMotte. Peripheral neural determinants of temperature discrimination in man: a correlative study of responses to cooling skin. J. Neurophysiol. 36: 347–370, 1973.
 118. Kenshalo, D. R. The dynamic response of cold units of the cat. In: The Somatosensory System, edited by H. H. Kornhuber. Stuttgart: Thieme, 1975, p. 38–42.
 119. Kenshalo, D. R. Correlations of temperature sensitivity in man and monkey, a first approximation. In: Sensory Functions of the Skin, edited by Y. Zotterman. Oxford: Pergamon, 1976, p. 305–330.
 120. Kenshalo, D. R., and R. Duclaux. Response characteristics of cutaneous cold receptors in the monkey. J. Neurophysiol. 40: 319–332, 1977.
 121. Kenshalo, D. R., and E. S. Gallegos. Multiple temperature‐sensitive spots innervated by single nerve fibers. Science 158: 1064–1065, 1967
 122. Kenshalo, D. R., D. Cormier, and M. Mellos. Some response properties of cold fibers to cooling. Prog. Brain Res. 43: 129–141, 1976.
 123. Kenshalo, D. R., H. Hensel, P. Graziadei, and H. Fruhstorfer. On the anatomy, physiology and psychophysics of the cat's temperature sensing system. In: Oral‐Facial Sensory and Motor Mechanisms, edited by R. Dubner, and Y. Kawamura. New York: Appleton‐Century Crofts Meredith, 1971, p. 23–45.
 124. Klee, M. R., Fr.‐K. Pierau, and D. S. Faber. Temperature effects on resting potential and spike parameters of cat motoneurons. Exp. Brain Res. 19: 478–492, 1974.
 125. Klussmann, F. W. Der Einfluß der Temperatur auf die afferente und efferente motorische Innervation des Rückenmarks. I. Temperaturabhängigkeit der afferenten und efferenten Spontantätigkeit. Pflugers Arch. 305: 295–315, 1969.
 126. Klussman, F. W., and Fr.‐K. Pierau. Extrahypothalamic deep body thermosensitivity. In: Essays on Temperature Regulation, edited by J. Bligh, and R. E. Moore. Amsterdam: North‐Holland, 1972, p. 87–104.
 127. Konietzny, F., and H. Hensel. The dynamic response of warm units in human skin nerves. Pflugers Arch. 370: 111–114, 1977.
 128. Konietzny, F., and H. Hensel. The neural basis of the sensory quality of warmth. In: Sensory Functions of the Skin of Humans, edited by D. R. Kenshalo. New York: Plenum, 1979, p. 241–259.
 129. Kosaka, M., E. Simon, O.‐E. Walther, and R. Thauer. Response of respiration to selective heating of the spinal cord below partial transection. Experientia 25: 36–37, 1969.
 130. Kozyreva, T. V., and M. A. Yakimenko. Sensation of cold in men. Physiol. J. USSR 64: 220–225, 1978 (In Russian.)
 131. Kozyreva, T. V., and M. A. Yakimenko. The effect of adaptation to cold on skin thermoreceptors activity. Physiol. J. USSR 65: 1598–1602, 1979 (In Russian.)
 132. Kozyreva, T. V., and M. A. Yakimenko. Sensitivity of the skin cold receptors to noradrenaline in cold‐adapted and nonadapted rats. Fiziol. Zh. SSSR. 70: 331–338, 1984.
 133. Kürten, I., U. Schmidt, and K. Schäfer. Warm and cold receptors in the nose of the vampire bat Desmondus rotundus. Naturwis‐senschaften 71: 327–328, 1984.
 134. Kumazawa, T., and E. R. Perl. Differential excitation of dorsal horn and substantia gelatinosa marginal neurons by primary afferent units with fine (A δ and C) fibers. In: Sensory Functions of the Skin, edited by Y. Zotterman. New York: Pergamon, 1976, p. 67.
 135. Kumazawa, T., and E. R. Perl. Primate cutaneous sensory units with unmyelinated (C) fibers. J. Neurophysiol. 40: 1325–1338, 1977.
 136. Kumazawa, T., and E. R. Perl. Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: indications of their place in dorsal horn functional organization. J. Comp. Neurol. 177: 417–434, 1978.
 137. Lang, E., A. Novak, P. W. Reeh, and H. O. Handwerker. Chemosensitivity of fine afferents from rat skin in vitro. J. Neurophysiol. 63: 887–901, 1990.
 138. Lewis, T. Pain. London: Macmillan, 1942.
 139. Light, A. R., D. L. Trevino, and E. R. Perl. Morphological features of functionally defined neurons in the marginal zone and substantia gelatinosa of the spinal dorsal horn. J. Comp. Neurol. 186: 151–172, 1979.
 140. Loewenstein, W. R. Modulation of cutaneous mechanoreceptors by sympathetic stimulation. J. Physiol. 132: 40–60, 1956.
 141. Loewenstein, W. R. On the “specificity” of a sensory receptor. J. Neurophysiol. 24: 150–158, 1961.
 142. Long, R. R. Sensitivity of cutaneous cold fibers to noxious heat: paradoxical cold discharge. J. Neurophysiol. 40: 489–502, 1977.
 143. Louis, S. M., A. Jamieson, N. J. W. Russell, and G. J. Dockray. The role of substance P and calcitonin gene‐related peptide in neurogenic plasma extravasation and vasodilatation in the rat. Neuroscience 32: 581–586, 1989.
 144. Lux, H. D., and G. Hofmeier. Properties of a calcium‐and voltage‐activated potassium current in helix pomatia neurons. Pflugers Arch. 394: 61–69, 1982.
 145. Magerl, W., J. Szolcsányi, R. A. Westerman, and H. O. Handwerker. Laser Doppler measurements of skin vasodilation elicited by percutaneous electrical stimulation of nociceptors in humans. Neurosci Lett. 82: 349–354, 1987.
 146. Mitchell, D., A. R. Atkins, and C. H. Wyndham. Mathematical and physical models of thermoregulation. In: Essays on Temperature Regulation, edited by J. Bligh, and R. Moore. Amsterdam: North Holland, 1972, p. 37–54.
 147. Murray, R. W. The response of the ampullae of Lorenzini of the elasmobranchs to electrical stimulation. J. Exp. Biol. 39: 119–128, 1962.
 148. Necker, R. Response of trigeminal ganglion neurons to thermal stimulation of the beak in pigeons. J. Comp. Physiol. 78: 307–314, 1972.
 149. Necker, R. Temperature sensitivity of thermoreceptors and mechanoreceptors on the beak of pigeons. J. Comp. Physiol. 87: 379–391, 1973.
 150. Neya, T., and Fr.‐K. Pierau. Activity patterns of temperature‐reactive dorsal horn neurons and their reactions to peripheral receptor stimulation by Ca. Jpn. J. Physiol. 30: 921–934, 1980.
 151. Nielsen, B. Natural cooling of the brain during outdoor bicycling? Pflugers Arch. 411: 456–461, 1988.
 152. Palmes, E. D., and C. R. Park. The regulation of body temperature during fever. Arch. Environ. Health 11: 749–759, 1965.
 153. Pierau, Fr.‐K. Endoanaesthetische Beeinflussung von Receptoren der Katzenzunge. Pflugers Arch. 296: 148–169, 1967.
 154. Pierau, Fr.‐K., and R. D. Wurster. Primary afferent input from cutaneous thermoreceptors. Federation Proc. 40: 2819–2824, 1981.
 155. Pierau, Fr.‐K., C. Ewert, R. Ernst, and H. Sann. Axon reflex flare reaction after non‐nociceptive warm stimulation of the human skin. Pflugers Arch. 418: R35, 1991.
 156. Pierau, Fr.‐K., G. Fellmer, and D. C. M. Taylor. Somatovisceral convergence in cat dorsal root ganglion neurones demonstrated by double labelling with fluorescent tracers. Brain Res. 321: 63–70, 1984.
 157. Pierau, Fr.‐K., M. R. Klee, and F. W. Klussmann. Effect of temperature on postsynaptic potentials of cat spinal motoneurones. Brain Res. 114: 21–34, 1976.
 158. Pierau, Fr.‐K., J. Szolcsányi, and H. Sann. The effect of capsaicin on afferent nerves and temperature regulation of mammals and birds. J. Therm. Biol. 11: 95–100, 1986.
 159. Pierau, Fr.‐K., D. C. M. Taylor, W. Abel, and B. Friedrich. Dichotomizing peripheral fibres revealed by intracellular recording from rat sensory neurones. Neurosci. Lett. 31: 123–128, 1982.
 160. Pierau, Fr.‐K., P. Torrey, and D. O. Carpenter. Mammalian cold receptor afferents: role of an electrogenic sodium pump in sensory transduction. Brain Res. 73: 156–160, 1974.
 161. Pierau, Fr.‐K., P. Torrey, and D. Carpenter. Afferent nerve fiber activity responding to temperature changes of the scrotal skin of the rat. J. Neurophysiol. 38: 601–612, 1975.
 162. Pierau, Fr.‐K., P. Torrey, and D. Carpenter. Effect of ouabain and potassium‐free solution on mammalian thermosensitive afferents in vitro. Pflugers Arch. 359: 349–356, 1975.
 163. Pierau, Fr.‐K., J. Ulrich, and R. D. Wurster. Effect of Ca++ and EDTA on the bursting pattern of lingual cold receptors in cats. Proc. Int. Union Physiol. Sci. 13: 597, 1977.
 164. Pierau, Fr.‐K., R. D. Wurster, T. Neya, T. Yamasato, and J. Ulrich. Generation and processing of peripheral temperature signals in mammals. Int. J. Biometeorol. 24: 243–252, 1980.
 165. Pierau, Fr.‐K., R. D. Wurster, and J. Ulrich. The effect of low and high Ca concentration on ouabain‐treated lingual cold receptors in the cat. J. Therm. Biol. 8: 19–22, 1983.
 166. Pierau, Fr.‐K., T. Yamasato, A. Cost, and S. Berkes. Processing of afferent temperature signals in sensory ganglia and the spinal cord. J. Therm. Biol. 9: 51–55, 1984.
 167. Pleschka, K. Control of tongue blood flow in regulation of heat loss in mammals. Rev. Physiol. Biochem. Pharmacol. 100: 75–120, 1984.
 168. Poulos, D. A. Trigeminal temperature mechanisms. In: Oral‐Facial Sensory and Motor Mechanisms, edited by R. Dubner, and Y. Kawamura. New York: Appleton‐Century‐Crofts Meredith, 1971, p. 47–72.
 169. Poulos, D. A. Central processing of peripheral temperature information. In: The Somatosensory System, edited by H. H. Kornhuber. Stuttgart: Thieme, 1975, p. 78–93.
 170. Poulos, D. A., and J. T. Molt. Response of central trigeminal neurons to cutaneous thermal stimulation. In: Sensory Functions of the Skin in Primates, edited by Y. Zotterman. Oxford: Pergamon, 1976, p. 263–283.
 171. Raths, P., and H. Hensel. Cutane Thermoreceptoren bei Winterschläfern. Pflugers Arch. 293: 281–302, 1967.
 172. Reaves, A., and E. Heath. Interval coding of temperature by CNS neurones in thermoregulation. Nature 257: 688–690, 1975.
 173. Rempe, L., K. Schäfer, and H. A. Braun. Effects of adrenergic agonists on discharge pattern of feline cold receptors. Pflugers Arch. 411: R130, 1988.
 174. Sand, A. The function of the ampullae of Lorenzini, with some observations on the effect of temperature on sensory rhythms. Proc. R. Soc. Land. B Biol. Sci 125: 524–553, 1938.
 175. Sann, H., E. Pinter, J. Szolcsányi, and Fr.‐K. Pierau. Peptidergic afferents might contribute to the regulation of skin blood flow. Agents Actions 23: 14–15, 1988.
 176. Satinoff, E. Neural organization and evolution of thermal regulation in mammals. Science 201: 16–22, 1978.
 177. Schäfer, K. Modification of cold fibre activity by epinephrine and norepinephrine. Pflugers Arch. 400: R67, 1984.
 178. Schäfer, K. A quantitative study of the dependence of feline cold receptor activity on the calcium concentration. Pflugers Arch. 409: 208–213, 1987.
 179. Schäfer, K., and H. A. Braun. Modulation of periodic cold receptor activity by ouabain. Pflugers Arch. 417: 91–99, 1990.
 180. Schäfer, K., H. A. Braun, and H. Hensel. Static and dynamic activity of cold receptors at various calcium levels. J. Neurophysiol. 47: 1017–1028, 1982
 181. Schäfer, K., H. A. Braun, and H. Hensel. Temperature transduction in the skin. In: Thermal Physiology, edited by J. R. S. Hales. New York: Raven, 1984, p. 1–11.
 182. Schäfer, K., H. A. Braun, and C. Isenberg. Effect of menthol on cold receptor activity: analysis of receptor processes. J. Gen. Physiol. 88: 757–776, 1986.
 183. Schäfer, K., H. A. Braun, and L. Kürten. Analysis of cold and warm receptor activity in vampire bats and mice. Pflugers Arch. 412: 188–194, 1988.
 184. Schäfer, H., H. A. Braun, and L. Rempe. Classification of a calcium conductance in cold receptors. Prog. Brain Res. 74: 29–36, 1988.
 185. Schäfer, H., H. A. Braun, and L. Rempe. Discharge pattern analysis suggests existence of a low‐threshold calcium channel in cold receptors. Experientia 47: 47–50, 1991.
 186. Schäfer, K., H. A. Braun, F. Bretschneider, and P. F. M. Teunis. Ampullary electroreceptors in teleosts (pisces): temperature dependence of stimulus transduction. Pflugers Arch. 417: 100–105, 1990.
 187. Schäfer, K., R. Necker, and H. A. Braun. Analysis of avian cold receptor function. Brain Res. 501: 66–72, 1989.
 188. Schingnitz, G., and J. Werner. Thermal afferents from the scrotum: no specific system but part of nonspecific information processing. In: Thermal Physiology, edited by J. R. S. Hales. New York: Raven, 1984, p. 47–51.
 189. Shibata, M., T. Hori, T. Kiyohara, T. Nakashima, and T. Asami. Responses of anterior hypothalamic‐preoptic thermosensitive neurons to substance P and capsaicin. Neuropharmacology 27: 143–148, 1988.
 190. Simon, E. Temperature signals from skin and spinal cord converging on spinothalamic neurons. Pflugers Arch. 337: 323–332, 1972.
 191. Simon, E. Temperature regulation: the spinal cord as a site of extrahypothalamic thermoregulatory functions. Rev. Physiol. Biochem. Pharmacol. 71: 1–76, 1974.
 192. Simon, E., and M. Iriki. Sensory transmission of spinal heat and cold sensitivity in ascending spinal neurons. Pflugers Arch, 328: 103–120, 1971.
 193. Simon, E., Fr.‐K. Pierau, and D. C. M. Taylor. Central and peripheral thermal control of effectors in homeothermic temperature regulation. Physiol. Rev. 66: 235–300, 1986.
 194. Spray, D. Characteristics, specificity, and efferent control of frog cutaneous cold receptors. J. Physiol. 237: 15–38, 1974.
 195. Spray, D. C., and S. H. Galansky. Effects of cholinergic agonists and antagonists on frog cutaneous cold receptors. Comp. Biochem. Physiol. 50: 97–103, 1975.
 196. Sumino, R., and R. Dubner. Response characteristics of specific thermoreceptive afferents innervating monkey facial skin and their relationship to human thermal sensitivity. Brain Res. 3: 105–122, 1981.
 197. Swandulla, D., and U. Misgeld. Development and properties of synaptic mechanisms in a network of rat hypothalamic neurons grown in culture. J. Neurophysiol. 64: 715–726, 1990.
 198. Swandulla, D., E. Carbone, K. Schäfer, and H. D. Lux. Effect of menthol on two types of Ca currents in cultured sensory neurons of vertebrates. Pflugers Arch. 409: 52–59, 1987.
 199. Szolcsányi, J. A pharmacological approach to elucidation of the role of different nerve fibres and receptor endings in mediation of pain. J. Physiol. Paris 73: 251–259, 1977.
 200. Szolcsányi, J. Capsaicin‐type pungent agents producing pyrexia. In: Handbook of Experimental Pharmacology, edited by A. S. Milton. Berlin: Springer‐Verlag, 1982, p. 437–478.
 201. Szolcsányi, J. Disturbances of thermoregulation induced by capsaicin. J. Therm. Biol. 8: 207–212, 1983.
 202. Szolcsányi, J. Capsaicin‐sensitive chemoreceptive neural system with dual sensory‐efferent function. In: Antidromic Vasodilatation and Neurogenic Inflammation, edited by L. A. Chal, J. Szolcsányi, and F. Lembeck. Budapest: Akademiai Kiadó, 1984, p. 27–55.
 203. Szolcsányi, J. Capsaicin, irritation, and desensitization. In: Chemical Senses, edited by B. G. Green, J. R. Mason, and M. R. Rare. New York: Marcel Dekker, 1990, p. 141–169.
 204. Szolcsányi, J., and A. Jancsó‐Gábor. Analysis of the role of warmth detectors by means of capsaicin under different conditions. In: Temperature Regulation and Drug Action, edited by P. Lomax, E. Schönbaum, and J. Jacob. Basel: Karger, 1975, p. 331–338.
 205. Taylor, D. C. M. The effect of spinal cord lesions on the temperature‐responsive neurones in the ventrobasal thalamus of the rat. J. Physiol. (Lond.) 292: 21P, 1979.
 206. Taylor, D. C. M. The effects of nucleus raphe magnus lesions on an ascending thermal pathway in the rat. J. Physiol. (Lond.) 326: 309–318, 1982.
 207. Taylor, D. C. M., and R. J. Gayton. Alteration of the discharge pattern of rat diencephalic neurones with scrotal skin temperature. Neurosci. Lett. 72: 59–63, 1986.
 208. Taylor, D. C. M., and Fr.‐K. Pierau. Nociceptive afferent neurones. In: Studies in Neuroscience No. 14, edited by W. Winlow. Manchester: Manchester University Press, 1991, p. 1–153.
 209. Treede, R.‐D., D. B. Oakland, R. A. Meyer, and J. N. Campbell. The apparent heat threshold of a C‐fiber nociceptor is dependent on stimulus parameters. In: Abstracts of the 20th Annual Meeting of the Society of Neuroscience, St. Louis, Part 1. 175.5, 1990.
 210. Ulrich, J. Wirkung von Ouabain auf die Caabhängige Aktivierung von Kaltrezeptoren. (Diss. University of Giessen, 1985).
 211. Vendrik, A. J. H., and J. J. Vos. Comparison of the stimulation of the warmth sense organ by microwave and infrared. J. Appl. Physiol. 13: 435–444, 1958.
 212. Waites, G. M. H. Polypnoea evoked by heating the scrotum of the ram. Nature 190: 172, 1961.
 213. Weddell, G., and S. Miller. Cutaneous sensibility. Annu. Rev. Physiol. 24: 199–222, 1962.
 214. Weddell, G., E. Palmer, and W. Pallie. Nerve endings in mammalian skin. Biol. Rev. 30: 159–195, 1955.
 215. Willis, J. A., G. L. Gaubatz, and D. O. Carpenter. The role of the electrogenic sodium pump in modulation of pacemaker discharge of Aplysia neurons. J. Cell Physiol. 84: 463–472, 1974.
 216. Wissing, H., Braun, H. A., and K. Schäfer. Dynamic response characteristics of the ampullae of Lorenzini to thermal and electrical stimuli. Prog. Brain Res. 74: 99–107, 1988.
 217. Yamasato, T., and Fr.‐K. Pierau. Different afferent temperature inputs of single dorsal horn neurones in rats. In: Contributions to Thermal Physiology, edited by Z. Szelényi, and M. Székely. Budapest: Akademiai Kiadó, 1980, p. 65–67.
 218. Zotterman, Y. Thermal sensations. In: Handbook of Physiology. Neurophysiology, edited by J. Field, and H. W. Magoun. Washington, DC: Am. Physiol. Soc., 1959, p. 431–458.

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Friedrich‐Karl Pierau. Peripheral Thermosensors. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 85-104. First published in print 1996. doi: 10.1002/cphy.cp040105