Abstract
Exposure of an animal to stressful stimuli, perceived by the animal as a threatening, emergency condition, elicits a transient decrease of pain sensitivity, which often affects thermoregulatory mechanisms in the threatened organism. We studied the interaction between emergency and thermoregulatory components of swim stress in developing swim stress-induced analgesia (SSIA). The subjects were mice selectively bred for high analgesia (HA) induced by swimming in 20 °C water, and displaying profound swim hypothermia. The mice were acclimated to one of the following conditions: (1) ambient cold (5 °C, mimicking the thermal component of swim stress); (2) daily 3-min swimming at 32 °C (mimicking the emergency, emotional in nature, component of swim stress), or (3) daily swimming at 20 °C (a combination of both emergency and thermal component of swim stress). Following each of the procedures the analgesia induced by swimming in 20 °C water and by acute exposure to −2.5°C in helium/oxygen (Helox) atmosphere was measured. Analgesia was also assessed in a group of naive mice immersed in 20 °C shallow water with the purpose of eliminating the emergency condition, but assuring the animal's contact with the cold water environment. Cold acclimation markedly attenuated Helox-induced analgesia (HIA) without affecting SSIA, whereas repeated swims attenuated SSIA without affecting HIA. The results suggest that hypothermia is the only stimulus eliciting HIA, while the emergency condition of swimming is essential for inducing SSIA. The significantly lower magnitude of SSIA in mice acclimated to repeated swims in 20 °C than in 32°C water suggests that SSIA develops due to an interaction between the emergency and hypothermic components of swim stress. This is further supported by a greater hypothermia and greater analgesia in freely swimming than in immersed naive mice.
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References
Amit Z, Galina ZH (1986) Stress-induced analgesia: adaptive pain suppression. Physiol Rev 66:1091–1120
Błaszczyk J, Tajchert K, Łapo I, Sadowski B (2000) Acoustic startle and open-field behavior in mice bred for magnitude of swim analgesia. Physiol Behav 70:471–476
Bodnar RJ, Kelly DD, Spiaggia A, Glusman M (1978) Stress-induced analgesia: adaptation following chronic cold water swims. Bull Psychon Soc 11:337–340
Bodnar RJ, Merrigan KP, Sperber E (1983) Potentiation of cold-water swim analgesia and hypothermia by clonidine. Pharmacol Biochem Behav 19:447–451
Cooper K, Carmody J (1982) The characteristics of the opioid-related analgesia induced by the stress of swimming in the mouse. Neurosci Lett 31:165–170
Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman and Hall, New York, pp 143–144
Gabrielsen GW (1985) Free and forced diving in ducks: habituation of the initial dive response. Acta Physiol Scand 123:67–72
Gabrielsen GW, Smith EN (1985) Physiological responses associated with feigned death in the American opossum. Acta Physiol Scand 123:393–398
Gabrielsen GW, Blix AS, Ursin H (1985) Orienting and freezing responses in incubating ptarmigan hens. Physiol Behav 34:925–934
Girardot MN, Holloway FA (1984) Intermittent cold water stress-analgesia in rats: cross-tolerance to morphine. Pharmacol Biochem Behav 20:631–633
Henderson ND (1989) Interpreting studies that compare high- and low-selected lines on new characters. Behav Genet 19:473–502
Jensen TS, Smith DF (1982) Effect of emotions on nociceptive threshold in rats. Physiol Behav 28:597–599
Kavaliers M (1988) Evolutionary and comparative aspects of nociception. Brain Res Bull 21:923–931
Kavaliers M (1990) Responsiveness of deer mice to a predator, the short-tailed weasel: population differences and neuromodulatory mechanisms. Physiol Zool 63:338–407
Kavaliers M, Colwell DD (1991) Sex differences in opioid and non-opioid mediated predator-induced analgesia in mice. Brain Res 568:173–177
Kavaliers M, Innes D (1987) Stress-induced opioid analgesia and activity in deer mice: sex and population differences. Brain Res 425:49–56
Kavaliers M, Innes D (1989) Population differences in benzodiazepine sensitive male scent-induced analgesia in the deer mouse, Peromyscus maniculatus. Pharmacol Biochem Behav 32:613–619
Konarzewski M, Sadowski B, Jóźwik I (1997) Metabolic correlates of selection for swim stress-induced analgesia in laboratory mice. Am J Physiol 273:R337–R343
Lester LS, Fanselow MS (1985) Exposure to a cat produces opioid analgesia in rats. Behav Neurosci 99:756–759
Lichtman AH, Fanselow MS (1990) Cats produce analgesia in rats on the tail-flick test: naltrexone sensitivity is determined by the nociceptive test stimulus. Brain Res 533:91–94
Łapo IB, Konarzewski M, Sadowski B (2003) Differential metabolic capacity of mice selected for magnitude of swim stress-induced analgesia. J Appl Physiol 94:677–684
Marek P, Szacki J (1988) Environmentally induced analgesia in wild mice: comparison with laboratory mice. Physiol Zool 61:330–332
Miczek KA, Thompson ML, Shuster L (1982) Opioid-like analgesia in defeated mice. Science 215:1520–1522
Mogil JS, Sternberg WF, Balian H, Liebeskind JC, Sadowski B (1996) Opioid and non-opioid swim stress-induced analgesia: a parametric analysis in mice. Physiol Behav 59:123–132
O'Connor P, Chipkin RE (1984) Comparisons between warm and cold water swim stress in mice. Life Sci 35:631–639
Panocka I, Marek P, Sadowski B (1986) Inheritance of stress-induced analgesia in mice. Selective breeding study. Brain Res 397:152–155
Panocka I, Massi M, Łapo I, Świderski T, Kowalczyk M, Sadowski B (2001) Antidepressant-type effect of the NK3 tachykinin receptor agonist aminosenktide in mouse lines differing in endogenous opioid system activity. Peptides 22:1037–1042
Pavlovic Z, Bodnar JR (1993) Antinociceptive and hypothermic crosstolerance between continuous and intermittent cold-water swims in rats. Physiol Behav 54:1081–1084
Rosenmann M, Morrison P (1974) Maximum oxygen consumption and heat loss facilitation in small homeotherms by He-O2. Am J Physiol 226:490–495
Sadowski B, Konarzewski M (1999) Analgesia in selectively bred mice exposed to cold in helium/oxygen atmosphere. Physiol Behav 66:145–151
Sadowski B, Sas R, Świderski T, Trzasko M (1996) Differentiation of opioid and non-opioid pain inhibitory mechanisms, and of thermoregulation in mice selectively bred for high and low swim stress-induced analgesia. Analgesia 2:211–218
SAS Institute (1990) SAS/STAT Users Guide, version 6, 4th Edn. SAS Institute, Cary
Schmidt-Nielsen K (1991) Scaling. Why is animal size so important? Cambridge University Press, Cambridge
Terman GW, Shavit Y, Lewis JW, Cannon JT, Liebeskind JC (1984) Intrinsic mechanisms of pain inhibition: activation by stress. Science 226:1270–1272
Terman GW, Morgan MJ, Liebeskind, JC (1986) Opioid and non-opioid stress analgesia from cold water swim: importance of stress severity. Brain Res 372:167–171
Teskey GC, Kavaliers M, Hirst M (1984) Social conflict activates opioid analgesic and ingestive behaviors in male mice. Life Sci 35:303–315
Watkins LR, Mayer DJ (1982) The organization of endogenous opiate and non-opiate pain control. Science 216:1185–1192
Acknowledgements
The authors thank D. Janero, J.S. Mogil, A.H. Świergiel and two anonymous reviewers for criticism and comments. We also thank I. Gąsiorkiewicz, M. Lewoc, B. Lewończuk and B. Sobolewska for technical assistance. This study was supported by Polish Committee for Scientific Research (KBN) grants Nr 6PO4C01616 and Nr 6PO4C01818 to B. Sadowski.
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Łapo, I.B., Konarzewski, M. & Sadowski, B. Analgesia induced by swim stress: interaction between analgesic and thermoregulatory mechanisms. Pflugers Arch - Eur J Physiol 446, 463–469 (2003). https://doi.org/10.1007/s00424-003-1060-9
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DOI: https://doi.org/10.1007/s00424-003-1060-9