Maternal Separation Leads to Persistent Reductions in Pain Sensitivity in Female Rats

Journal of Pain

Volumn 8, Issue 12, 2007, Pages 962-969

  Weaver, Shelley A ^a,b   Diorio, Josie ^c   Meaney, Michael J ^c  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Hot plate; maternal separation; morphine; neonatal handling; opioid

Indexed keywords

ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MORPHINE; MU OPIATE RECEPTOR; TRITIUM;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN REGION; CONTROLLED STUDY; DIESTRUS; FEMALE; HOT PLATE TEST; LICKING; LIFE HISTORY; LONG EVANS RAT; MATERNAL DEPRIVATION; MOTIVATION; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN ASSESSMENT; PAIN THRESHOLD; PREOPTIC NUCLEUS; RAT; RECEPTOR BINDING; THERMAL STIMULATION;

ANALYSIS OF VARIANCE; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; ESTROUS CYCLE; FEMALE; MATERNAL DEPRIVATION; MORPHINE; NARCOTICS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PREGNANCY; PROTEIN BINDING; RADIOGRAPHY; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; REACTION TIME; TIME FACTORS; TRITIUM;

EID: 36348975007     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2007.07.001     Document Type: Article

References (52)

1. Alberts J.R. Huddling by rat pups: Group behavioral mechanisms of temperature regulation and energy conservation. J Comp Physiol Psychol 92 (1978) 231-245
2. Boccia M.L., and Pedersen C.A. Brief vs long maternal separations in infancy: Contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology 26 (2001) 657-672
3. Brake W.G., Zhang T.Y., Diorio J., Meaney M.J., and Gratton A. Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioural responses to psychostimulants and stressors in adult rats. Eur J Neurosci 19 (2004) 1863-1874
4. Caldji C., Francis D., Sharma S., Plotsky P.M., and Meaney M.J. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22 (2000) 219-229
5. Champagne F., and Meaney M.J. Like mother, like daughter: Evidence for non-genomic transmission of parental behavior and stress responsivity. Prog Brain Res 133 (2001) 287-302
6. Champagne F.A., Francis D.D., Mar A., and Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79 (2003) 359-371
7. Coghill R.C., McHaffie J.G., and Yen Y.F. Neural correlates of interindividual differences in the subjective experience of pain. Proc Natl Acad Sci U S A 100 (2003) 8538-8542
8. Coolen L.M., Fitzgerald M.E., Yu L., and Lehman M.N. Activation of mu opioid receptors in the medial preoptic area following copulation in male rats. Neuroscience 124 (2004) 11-21
9. Coutinho S.V., Plotsky P.M., Sablad M., Miller J.C., Zhou H., Bayati A.I., McRoberts J.A., and Mayer E.A. Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 282 (2002) G307-G316
10. Cui X.Y., Lundeberg T., and Yu L.C. Role of corticotropin-releasing factor and its receptor in nociceptive modulation in the central nucleus of amygdala in rats. Brain Res 995 (2004) 23-28
11. Davis D.A., Luecken L.J., and Zautra A.J. Are reports of childhood abuse related to the experience of chronic pain in adulthood?. A meta-analytic review of the literature. Clin J Pain 21 (2005) 398-405
12. Denenberg V.H., Brumaghim J.T., Haltmeyer G.C., and Zarrow M.X. Increased adrenocortical activity in the neonatal rat following handling. Endocrinology 81 (1967) 1047-1052
13. Dhabhar F.S., McEwen B.S., and Spencer R.L. Stress response, adrenal steroid receptor levels and corticosteroid-binding globulin levels: A comparison between Sprague-Dawley, Fischer 344 and Lewis rats. Brain Res 616 (1993) 89-98
14. Diatchenko L., Slade G.D., Nackley A.G., Bhalang K., Sigurdsson A., Belfer I., Goldman D., Xu K., Shabalina S.A., Shagin D., Max M.B., Makarov S.S., and Maixner W. Genetic basis for individual variations in pain perception and the development of a chronic pain condition. Hum Mol Genet 14 (2005) 135-143
15. Dionne R.A., Bartoshuk L., Mogil J., and Witter J. Individual responder analyses for pain: Does one pain scale fit all?. Trends Pharmacol Sci 26 (2005) 125-130
16. Edwards R.R. Individual differences in endogenous pain modulation as a risk factor for chronic pain. Neurology 65 (2005) 437-443
17. Elmer G.I., Pieper J.O., Negus S.S., and Woods J.H. Genetic variance in nociception and its relationship to the potency of morphine-induced analgesia in thermal and chemical tests. Pain 75 (1998) 129-140
18. Fillingim R.B., and Edwards R.R. Is self-reported childhood abuse history associated with pain perception among healthy young women and men?. Clin J Pain 21 (2005) 387-397
19. Fillingim R.B., Kaplan L., Staud R., Ness T.J., Glover T.L., Campbell C.M., Mogil J.S., and Wallace M.R. The A118G single nucleotide polymorphism of the mu-opioid receptor gene (OPRM1) is associated with pressure pain sensitivity in humans. J Pain 6 (2005) 159-167
20. Frye C.A., Cuevas C.A., and Kanarek R.B. Diet and estrous cycle influence pain sensitivity in rats. Pharmacol Biochem Behav 45 (1993) 255-260
21. Gomez F., De Kloet E.R., and Armario A. Glucocorticoid negative feedback on the HPA axis in five inbred rat strains. Am J Physiol 274 (1998) R420-R427
22. Grota L.J., Bienen T., and Felten D.L. Corticosterone responses of adult Lewis and Fischer rats. J Neuroimmunol 74 (1997) 95-101
23. Hammer Jr. R.P. Mu-opiate receptor binding in the medial preoptic area is cyclical and sexually dimorphic. Brain Res 515 (1990) 187-192
24. Kalinichev M., Easterling K.W., and Holtzman S.G. Early neonatal experience of Long-Evans rats results in long-lasting changes in morphine tolerance and dependence. Psychopharmacology (Berl) 157 (2001) 305-312
25. Kalinichev M., Easterling K.W., and Holtzman S.G. Repeated neonatal maternal separation alters morphine-induced antinociception in male rats. Brain Res Bull 54 (2001) 649-654
26. Kalinichev M., Easterling K.W., and Holtzman S.G. Early neonatal experience of Long-Evans rats results in long-lasting changes in reactivity to a novel environment and morphine-induced sensitization and tolerance. Neuropsychopharmacology 27 (2002) 518-533
27. Kayser V., Berkley K.J., Keita H., Gautron M., and Guilbaud G. Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat. Brain Res 742 (1996) 352-354
28. Kitchen I., Slowe S.J., Matthes H.W., and Kieffer B. Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res 778 (1997) 73-88
29. Liu D., Caldji C., Sharma S., Plotsky P.M., and Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinephrine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12 (2000) 5-12
30. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., and Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1659-1662
31. Nielsen C.S., Price D.D., Vassend O., Stubhaug A., and Harris J.R. Characterizing individual differences in heat-pain sensitivity. Pain 119 (2005) 65-74
32. Perkins F.M., and Kehlet H. Chronic pain as an outcome of surgery: A review of predictive factors. Anesthesiology 93 (2000) 1123-1133
33. Plotsky P.M., and Meaney M.J. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18 (1993) 195-200
34. Plotsky P.M., Thrivikraman K.V., Nemeroff C.B., Caldji C., Sharma S., and Meaney M.J. Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology 30 (2005) 2192-2204
35. Pryce C.R., Bettschen D., and Feldon J. Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev Psychobiol 38 (2001) 239-251
36. Rosztoczy A., Fioramonti J., Jarmay K., Barreau F., Wittmann T., and Bueno L. Influence of sex and experimental protocol on the effect of maternal deprivation on rectal sensitivity to distension in the adult rat. Neurogastroenterol Motil 15 (2003) 679-686
37. Schaefer Jr. T., Weingarten F.S., and Towne J.C. Temperature change: the basic variable in the early handling phenomenon?. Science 135 (1962) 41-42
38. Schwetz I., McRoberts J.A., Coutinho S.V., Bradesi S., Gale G., Fanselow M., Million M., Ohning G., Tache Y., Plotsky P.M., and Mayer E.A. Corticotropin-releasing factor receptor 1 mediates acute and delayed stress-induced visceral hyperalgesia in maternally separated Long-Evans rats. Am J Physiol Gastrointest Liver Physiol 289 (2005) G704-G712
39. Smythe J.W., McCormick C.M., Rochford J., and Meaney M.J. The interaction between prenatal stress and neonatal handling on nociceptive response latencies in male and female rats. Physiol Behav 55 (1994) 971-974
40. Sora I., Takahashi N., Funada M., Ujike H., Revay R.S., Donovan D.M., Miner L.L., and Uhl G.R. Opiate receptor knockout mice define mu receptor roles in endogenous nociceptive responses and morphine-induced analgesia. Proc Natl Acad Sci U S A 94 (1997) 1544-1549
41. Stammberger U., Steinacher C., Hillinger S., Schmid R.A., Kinsbergen T., and Weder W. Early and long-term complaints following video-assisted thoracoscopic surgery: Evaluation in 173 patients. Eur J Cardiothorac Surg 18 (2000) 7-11
42. Stephan M., Helfritz F., Pabst R., and von Horsten S. Postnatally induced differences in adult pain sensitivity depend on genetics, gender and specific experiences: reversal of maternal deprivation effects by additional postnatal tactile stimulation or chronic imipramine treatment. Behav Brain Res 133 (2002) 149-158
43. Sternberg E.M., Glowa J.R., Smith M.A., Calogero A.E., Listwak S.J., Aksentijevich S., Chrousos G.P., Wilder R.L., and Gold P.W. Corticotropin releasing hormone related behavioral and neuroendocrine responses to stress in Lewis and Fischer rats. Brain Res 570 (1992) 54-60
44. Sternberg W.F., and Ridgway C.G. Effects of gestational stress and neonatal handling on pain, analgesia, and stress behavior of adult mice. Physiol Behav 78 (2003) 375-383
45. Sternberg W.F., Scorr L., Smith L.D., Ridgway C.G., and Stout M. Long-term effects of neonatal surgery on adulthood pain behavior. Pain 113 (2005) 347-353
46. Sternini C., Spann M., Anton B., Keith Jr. D.E., Bunnett N.W., von Zastrow M., Evans C., and Brecha N.C. Agonist-selective endocytosis of mu opioid receptor by neurons in vivo. Proc Natl Acad Sci U S A 93 (1996) 9241-9246
47. Tseng L.F., and Wang Q. Forebrain sites differentially sensitive to beta-endorphin and morphine for analgesia and release of Met-enkephalin in the pentobarbital-anesthesized rat. J Pharmacol Exp Ther 261 (1992) 1028-1036
48. Uhl G.R., Sora I., and Wang Z. The mu opiate receptor as a candidate gene for pain: polymorphisms, variations in expression, nociception, and opiate responses. Proc Natl Acad Sci U S A 96 (1999) 7752-7755
49. Verhaak P.F., Kerssens J.J., Dekker J., Sorbi M.J., and Bensing J.M. Prevalence of chronic benign pain disorder among adults: a review of the literature. Pain 77 (1998) 231-239
50. Vincler M., Maixner W., Vierck C.J., and Light A.R. Estrous cycle modulation of nociceptive behaviors elicited by electrical stimulation and formalin. Pharmacol Biochem Behav 69 (2001) 315-324
51. Vit J.P., Clauw D.J., Moallem T., Boudah A., Ohara P.T., and Jasmin L. Analgesia and hyperalgesia from CRF receptor modulation in the central nervous system of Fischer and Lewis rats. Pain 121 (2006) 241-260
52. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110