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When pain and stress interact: looking at stress-induced analgesia and hyperalgesia in birds

Published online by Cambridge University Press:  20 August 2019

B.I. BAKER ,
K.L. MACHIN  and
K. SCHWEAN-LARDNER
B.I. BAKER
Affiliation:
Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, S7N 5A8, Canada
K.L. MACHIN
Affiliation:
Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, S7N 5B4, Canada
K. SCHWEAN-LARDNER*
Affiliation:
Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, S7N 5A8, Canada
*
Corresponding author: [email protected]
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Abstract

Stress can exert modulatory effects on pain perception in animals, as exposure to a stressor can result in either the reduction or amplification of the perceived severity of pain. These phenomena are widely described as stress-induced analgesia (SIA) and stress-induced hyperalgesia (SIH). The two are mediated by the same underlying mechanisms, but occur due to different stressors and different responses from the pain pathway. SIA and SIH have been demonstrated with a variety of stress and pain stimuli in rodents, humans and other mammals. There is some evidence that SIA occurs in birds and that they have the neurological systems and brain regions necessary for SIH. Tonic immobility (TI) is related to SIA in mammals, and there is evidence the avian brain is compatible with TI having analgesic effect, but it could have a hyperalgesic effect. This review looks at the mechanisms and evidence of SIA, SIH and TI in mammals and discusses evidence relating to the occurrence of these phenomena in birds.

Keywords

tonic immobilitypain modulationaviannociceptionanalgesiastressendogenous analgesiabrain
Type
Review
Information
World's Poultry Science Journal , Volume 75 , Issue 3 , September 2019 , pp. 457 - 468
Copyright
Copyright © World's Poultry Science Association 2019 

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References

AGUGGIA, M. (2003) Neurophysiology of pain. Neurological Science 24: 57-60.Google Scholar
AMIT, Z. and GALINA, Z.H. (1986) Stress-Induced Analgesia: Adaptive Pain Suppression. Physiological Reviews 66 (4): 1091-1120.10.1152/physrev.1986.66.4.1091Google Scholar
BLAS, J. (2015) Stress in birds, in: SCANES, C.G. (Ed) Sturkie's Avian Physiology, 6th ed, pp. 769-810 (London, Elsevier).Google Scholar
BODNAR, R.J., KELLY, D.D., BRUTUS, M. and GLUSMAN, M. (1979) Stress-Induced Analgesia: Neural and Hormonal Determinants I. Neuroscience & Biobehavioral Reviews 4: 87-100.10.1016/0149-7634(80)90028-7Google Scholar
BODNAR, R.J. (1986) Neuropharmacological and Neuroendocrine Substrates of Stress Induced Analgesia. Annals New York Academy of Sciences 467 (1): 345-360.10.1111/j.1749-6632.1986.tb14639.xGoogle Scholar
BOKKERS, E.A.M., KOENE, P., RODENBURG, T.B., ZIMMERMAN, P.H. and SPRUIJT, B.M. (2004) Working for food under conditions of varying motivation in broilers. Animal Behaviour 68 (1): 105-113.10.1016/j.anbehav.2003.10.013Google Scholar
BUTLER, R.K. and FINN, D.P. (2009) Stress-Induced Analgesia. Progress in Neurobiology 88: 184-202.10.1016/j.pneurobio.2009.04.003Google Scholar
CARSTEN, E.E. (1987) Endogenous pain suppression mechanism. Journal of American Veterinary Medical Association 191 (10): 1203-1206.Google Scholar
DA SILVA, L.F.S. and MENESCAL-DE-OLIVEIRA, L. (2007) Role of opioidergic and GABAergic neurotransmission of the nucleus raphe magnus in the modulation of tonic immobility in guinea pigs. Brain Research Bulletin 72: 25-31.10.1016/j.brainresbull.2006.12.005Google Scholar
DOUGLAS, J.M., GUZMAN, D.S.M. and PAUL-MURPHY, J.R. (2018) Pain in Birds: The Anatomical and Physiological Basis. Veterinary Clinics of North America: Exotic Clinics 21: 17-31.Google Scholar
DICKENSON, A.H. and KIEFFER, B.H. (2013) Opiods: Basic Mechanisms, in: MCMAHON, S., KOLTZENBURG, M., TRACEY, I. & TURK, D. (Eds) Wall & Melzack's Textbook of Pain, 6th ed, pp. 413-428 (Philadelphia, Elsevier Saunders).Google Scholar
FELTENSTEIN, M.W., FORDA, N.G., FREEMAN, K.B. and SUFKAA, K.J. (2002) Dissociation of stress behaviours in the chick social-separation-stress procedure. Physiology & Behavior 75: 675-679.10.1016/S0031-9384(02)00660-1Google Scholar
FOWLER, C.J., NILSSON, O., ANDERSSON, M., DISNEY, G., JACOBSSON, S.O.P. and TIGER, G. (2001) Pharmacological Properties of Cannabinoid Receptors in the Avian brain: Similarity of Rat and Chicken Cannabinoid1 Receptor Recognition Sites and Expression of Cannabinoid2 Receptor-Like Immunoreactivity in the Embryonic Chick Brain. Pharmacology & Toxicology 88: 213-222.Google Scholar
GENTLE, M.J. (2011) Pain issues in poultry. Applied Animal Behaviour Science 135: 252-258.Google Scholar
GENTLE, M.J. and CORR, S.A. (1995) Endogenous analgesia in the chicken. Neuroscience Letters 201: 211-214.10.1016/0304-3940(95)12181-1Google Scholar
GENTLE, M.J, JONES, R.B. and WOOLLEY, S.C. (1989) Physiological Changes during Tonic Immobility in Gallus gallus var domesticus. Physiology & Behavior 46: 843-847.10.1016/0031-9384(89)90046-2Google Scholar
GENTLE, M.J. and TILSTON, V.L. (1999) Reduction in Peripheral Inflammation by Changes in Attention. Physiology & Behavior 66 (2): 289-292.10.1016/S0031-9384(98)00297-2Google Scholar
HOHMANN, A.G. and RICE, A.S.C. (2013) Cannabinoids, in: MCMAHON, S., KOLTZENBURG, M., TRACEY, I. & TURK, D. (Eds) Wall & Melzack's Textbook of Pain, 6th ed, pp. 538-551 (Philadelphia, Elsevier Saunders).Google Scholar
IMBE, H., IWAI-LIAO, Y. and SENBA, E. (2006) Stress-induced hyperalgesia: animal models and putative mechanisms. Frontiers in Bioscience 11: 2179-2192.10.2741/1960Google Scholar
IASP (1994) Part III: Pain Terms, A Current List with Definitions and Notes on Usage, in: MERSKEY, H. & BOGDUK, N. (Eds) Classification of Chronic Pain, pp. 209-214 (Seattle, IASP Press).Google Scholar
JENNINGS, E.M., OKINE, B.N., ROCHE, M. and FINN, D.P. (2014) Stress-induced hyperalgesia. Progress in Neurobiology 121: 1-18.Google Scholar
JONES, R.B., BEUVING, G. and BLOKHUIS, H.J. (1987) Tonic Immobility and Heterophil/Lymphocyte Responses of the Domestic Fowl to Corticosterone Infusion. Physiology & Behavior 42: 249-253.Google Scholar
JØRUM, E. (1988) Analgesia or hyperalgesia following stress correlated with emotional behaviour in rats. Pain 32: 341-348.10.1016/0304-3959(88)90046-2Google Scholar
KAPITZKE, D., VETTER, I. and CABOT, P.J. (2005) Endogenous opioid analgesia in peripheral tissues and the clinical implications for pain control. Therapeutics and Clinical Risk Management 1 (4): 279-297.Google Scholar
KAVALIERS, M. and COLWELL, D.D. (1991) Sex differences in opioid and non-opioid mediated predator-induced analgesia in mice, Brain Research 568: 173-177.10.1016/0006-8993(91)91394-GGoogle Scholar
KUENZEL, W.J. (2007) Neurobiological Basis of Sensory Perception: Welfare Implications of Beak Trimming. Poultry Science 86 (6): 1273-1282.10.1093/ps/86.6.1273Google Scholar
LARIVIERE, W.R. and MELZACK, R. (2000) The role of corticotropin-releasing factor in pain and analgesia. Pain 84: 1-12.10.1016/S0304-3959(99)00193-1Google Scholar
MACHIN, K. (2005) Avian Pain: Physiology and Evaluation. Compendium 27 (2): 98-108.Google Scholar
MARTENSON, M.E., CETAS, J.S. and HEINRICHER, M.M. (2009) A possible neural basis for stress-induced hyperalgesia. Pain 142: 236-244.10.1016/j.pain.2009.01.011Google Scholar
MAUK, M.D., OLSON, R.D., LAHOSTE, G.J. and OLSON, G.A. (1981) Tonic Immobility Produces Hyperalgesia and Antagonizes Morphine Analgesia. Science 213: 353-354.10.1126/science.7244620Google Scholar
MELLEU, F.F., LINO-DE-OLIVERIA, C. and MARINO-NETO, J. (2017) The mesencephalic GCt–ICo complex and tonic immobility in pigeons (Columba livia): a c-Fos study. Brain Structure and Function 222: 1253-1265.10.1007/s00429-016-1275-0Google Scholar
MORMÈDE, P., ANDANSON, S., AUPÉRIN, B., BEERDA, B., GUÉMENÉ, D., MALMKVIST, J., MANTECA, X., MANTEUFFEL, G., PRUNET, P., VAN REENEN, C.G., RICHARD, S. and VEISSIER, I. (2007) Exploration of the hypothalamic–pituitary–adrenal function as a tool to evaluate animal welfare. Physiology & Behavior 92: 317-339.10.1016/j.physbeh.2006.12.003Google Scholar
MUIR, W.W. (2009) Pain and Stress, in: GAYNOR, J.S. & MUIR, W.W. (Eds) Handbook of Veterinary Pain Management, pp. 42-56 (St. Louis, Elsevier).Google Scholar
PARIKH, D., HAMID, A., FRIEDMAN, T.C., NGUYEN, K., TSENG, A., MARQUEZ, P. and LUTFY, K. (2011) Stress-induced analgesia and endogenous opioid peptides: The importance of stress duration. European Journal of Pharmacology 650: 563-567.10.1016/j.ejphar.2010.10.050Google Scholar
PETERS, R.H. and HUGHES, R.A. (1978) Naloxone Interactions with Morphine- and Shock-Potentiated Tonic Immobility in Chickens. Pharmacology Biochemistry & Behavior 9: 153-156.10.1016/0091-3057(78)90157-0Google Scholar
PORRO, C.A. and CARLI, G. (1988) Immobilization and restraint effects on pain reactions in animals. Pain 32: 289-307.10.1016/0304-3959(88)90041-3Google Scholar
REINER, A., YAMAMOTO, K. and KARTEN, H.J. (2005) Organization and Evolution of the Avian Forebrain. The Anatomical Record 287 (A): 1080-1102.10.1002/ar.a.20253Google Scholar
SIEGEL, H.S. (1980) Physiological Stress in Birds. Bioscience 30 (8): 529-534.10.2307/1307973Google Scholar
STAROWICZ, K. and FINN, D.P. (2017) Cannabinoids and Pain: sites and Mechanisms of Action. Advances in Pharmacology 80: 437-475.Google Scholar
SUFKA, K.J. and HUGHES, R.A. (1991) Differential Effects of Handling on Isolation-Induced Vocalizations, Hypoalgesia, and Hyperthermia in Domestic Fowl. Physiology & Behavior 50: 129-133.10.1016/0031-9384(91)90508-LGoogle Scholar
TRAMULLAS, M., DINAN, T.G. and CRYAN, J.F. (2012) Chronic psychosocial stress induces visceral hyperalgesia in mice. Stress 15 (3): 281-292.Google Scholar
TREBILCOCK, P.D. (2015) Investigating the electrical response of the brain of the domestic chicken (Gallus gallus domesticus) to nociception through the use of depth electroencephalography (dEEG). M.Sc. Thesis, Massey University.Google Scholar
ULRICH-LAI, Y.M. and HERMAN, J.P. (2009) Neural Regulation of Endocrine and Autonomic Stress Responses. Nature Reviews Neuroscience 10 (6): 397-409.Google Scholar
WALLNAU, L.B. and GALLUP, G.G. (1977) A Serotonergic, Midbrain-Raphe Model of Tonic Immobility. Biobehavioral Reviews 1: 35-43.Google Scholar
WEEKS, C.A. and NICOL, C.J. (2006) Behavioural needs, priorities and preferences of laying hens. World's Poultry Science Journal 62 (2): 296-307.Google Scholar
WOODHAMS, S.G., SAGAR, D.R., BURSTON, J.J. and CHAPMAN, V. (2015) The role of the Endocannabinoid Systems in Pain, in: SCHAIBLE, H.G. (Ed) Pain Control, Handbook of Experimental Pharmacology, vol 227, pp. 119-143 (Berlin, Springer).Google Scholar
WYLIE, L.M. and GENTLE, M.J. (1998) Feeding-induced Tonic Pain Suppression in the Chicken: Reversal by Naloxone. Physiology & Behavior 64 (1): 27-30.Google Scholar
YAMADA, K. and NABESHIMA, T. (1995) Stress-induced behavioral responses and multiple opioid systems in the brain. Behavioural Brain Research 67: 133-145.Google Scholar
YILMAZ, P., DIERS, M., DIENER, S., RANCE, M., WESSA, M. and FLOR, H. (2010) Brain correlates of stress-induced analgesia. Pain 151: 552-529.Google Scholar