Neonatal stress or morphine treatment alters adult mouse conditioned place preference

Neonatology

Volumn 95, Issue 3, 2009, Pages 230-239

  Boasen, Jared F ^a   McPherson, Ronald J ^a   Hays, Sarah L ^a   Juul, Sandra E ^a   Gleason, Christine A ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Behavioral activity; Neonatal brain; Neonatal stress; Perinatal morphine

Indexed keywords

CORTICOSTERONE; HORMONE; MORPHINE; SODIUM CHLORIDE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HYPOXIA; COGNITION; CONTROLLED STUDY; FEEDING; FEMALE; FORCED SWIMMING TEST; HORMONE ACTION; HYPEROXIA; MALE; MATERNAL DEPRIVATION; MAZE TEST; MOUSE; NEONATAL STRESS; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PLACE PREFERENCE; PREMATURITY; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE;

ANALGESICS, OPIOID; ANIMALS; ANIMALS, NEWBORN; ANOXIA; CONDITIONING, CLASSICAL; CORTICOSTERONE; DISEASE MODELS, ANIMAL; HYPEROXIA; MAZE LEARNING; MICE; MICE, INBRED C57BL; MORPHINE; STRESS, PHYSIOLOGICAL;

MUS; RATTUS;

EID: 54449083712     PISSN: 16617800     EISSN: 16617819     Source Type: Journal    
DOI: 10.1159/000165379     Document Type: Article

References (78)

1. 1 Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME: Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989; 298: 564-567.
2. Barker DJ, Shiell AW, Barker ME, Law CM: Growth in utero and blood pressure levels in the next generation. J Hypertens 2000; 18: 843-846.
3. Anand KJ, Scalzo FM: Can adverse neonatal experiences alter brain development and subsequent behavior? Biol Neonate 2000; 77: 69-82.
4. Bellu R, de Waal K, Zanini R: Opioids for neonates receiving mechanical ventilation. Cochrane Database Syst Rev 2008:CD004212.
5. Committee: Prevention and management of pain and stress in the neonate. American Academy of Pediatrics. Committee on Fetus and Newborn. Committee on Drugs. Section on Anesthesiology. Section on Surgery. Canadian Paediatric Society. Fetus and Newborn Committee. Pediatrics 2000; 105: 454-461.
6. Anand KJ: Consensus statement for the prevention and management of pain in the newborn. Arch Pediatr Adolesc Med 2001; 155: 173-180.
7. Bergman I, Steeves M, Burckart G, Thompson A: Reversible neurologic abnormalities associated with prolonged intravenous midazolam and fentanyl administration. J Pediatr 1991; 119: 644-649.
8. MacGregor R, Evans D, Sugden D, Gaussen T, Levene M: Outcome at 5-6 years of prematurely born children who received morphine as neonates. Arch Dis Child Fetal Neonatal Ed 1998; 79:F40-F43.
9. Orsini AJ, Leef KH, Costarino A, Dettorre MD, Stefano JL: Routine use of fentanyl infusions for pain and stress reduction in infants with respiratory distress syndrome. J Pediatr 1996; 129: 140-145.
10. Quinn MW, Wild J, Dean HG, Hartley R, Rushforth JA, Puntis JW, Levene MI: Randomised double-blind controlled trial of effect of morphine on catecholamine concentrations in ventilated pre-term babies. Lancet 1993; 342: 324-327.
11. Anand KJ, Hall RW, Desai N, Shephard B, Bergqvist LL, Young TE, Boyle EM, Carbajal R, Bhutani VK, Moore MB, Kronsberg SS, Barton BA: Effects of morphine analgesia in ventilated preterm neonates: primary outcomes from the NEOPAIN randomised trial. Lancet 2004; 363: 1673-1682.
12. Simons SH, van Dijk M, van Lingen RA, Roofthooft D, Duivenvoorden HJ, Jongeneel N, Bunkers C, Smink E, Anand KJ, van den Anker JN, Tibboel D: Routine morphine infusion in preterm newborns who received ventilatory support: a randomized controlled trial. JAMA 2003; 290: 2419-2427.
13. Rao R, Sampers JS, Kronsberg SS, Brown JV, Desai NS, Anand KJ: Neurobehavior of preterm infants at 36 weeks postconception as a function of morphine analgesia. Am J Perinatol 2007; 24: 511-517.
14. Brunson KL, Kramar E, Lin B, Chen Y, Colgin LL, Yanagihara TK, Lynch G, Baram TZ: Mechanisms of late-onset cognitive decline after early-life stress. J Neurosci 2005; 25: 9328-9338.
15. Matthews K, Dalley JW, Matthews C, Tsai TH, Robbins TW: Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain. Synapse 2001; 40: 1-10.
16. Matthews K, Robbins TW: Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neurosci Biobehav Rev 2003; 27: 45-55.
17. Matthews K, Wilkinson LS, Robbins TW: Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol Behav 1996; 59: 99-107.
18. Matthews K, Hall FS, Wilkinson LS, Robbins TW: Retarded acquisition and reduced expression of conditioned locomotor activity in adult rats following repeated early maternal separation: effects of prefeeding, D -amphetamine, dopamine antagonists and clonidine. Psychopharmacology (Berl) 1996; 126: 75-84.
19. Will MJ, Watkins LR, Maier SF: Uncontrollable stress potentiates morphine's rewarding properties. Pharmacol Biochem Behav 1998; 60: 655-664.
20. Piazza PV, Deminiere JM, le Moal M, Simon H: Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration. Brain Res 1990; 514: 22-26.
21. Shaham Y, Stewart J: Exposure to mild stress enhances the reinforcing efficacy of intravenous heroin self-administration in rats. Psychopharmacology (Berl) 1994; 114: 523-527.
22. McLaughlin JP, Marton-Popovici M, Chavkin C: Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 2003; 23: 5674-5683.
23. Sternberg WF, Scorr L, Smith LD, Ridgway CG, Stout M: Long-term effects of neonatal surgery on adulthood pain behavior. Pain 2005; 113: 347-353.
24. Gagin R, Kook N, Cohen E, Shavit Y: Prenatal morphine enhances morphine-conditioned place preference in adult rats. Pharmacol Biochem Behav 1997; 58: 525-528.
25. McPherson RJ, Gleason C, Mascher-Denen M, Chan M, Kellert B, Juul SE: A new model of neonatal stress which produces lasting neurobehavioral effects in adult rats. Neonatology 2007; 92: 33-41.
26. Clancy B, Finlay BL, Darlington RB, Anand KJ: Extrapolating brain development from experimental species to humans. Neurotoxicology 2007; 28: 931-937.
27. Levine S, Huchton DM, Wiener SG, Rosenfeld P: Time course of the effect of maternal deprivation on the hypothalamic-pituitaryadrenal axis in the infant rat. Dev Psychobiol 1991; 24: 547-558.
28. Messer M, Thoman EB, Galofre A, Dallman T, Dallman PR: Artificial feeding of infant rats by continuous gastric infusion. J Nutr 1969; 98: 404-410.
29. Carbajal R, Lenclen R, Jugie M, Paupe A, Barton BA, Anand KJ: Morphine does not provide adequate analgesia for acute procedural pain among preterm neonates. Pediatrics 2005; 115: 1494-1500.
30. Scott CS, Riggs KW, Ling EW, Fitzgerald CE, Hill ML, Grunau RV, Solimano A, Craig KD: Morphine pharmacokinetics and pain assessment in premature newborns. J Pediatr 1999; 135: 423-429.
31. File SE, Lippa AS, Beer B, Morgen TL: Animal tests of anxiety; in Current Protocols in Neuroscience. New York, Wiley, 2000, chapt 8.3.6.
32. Li S, Lee ML, Bruchas MR, Chan GC, Storm DR, Chavkin C: Calmodulin-stimulated adenylyl cyclase gene deletion affects morphine responses. Mol Pharmacol 2006; 70: 1742-1749.
33. Langroudi RM, Khoshnoodi MA, Abadi NY, Fahadan PT, Ghahremani MH, Dehpour AR: Effect of cyclosporin A on morphine-induced place conditioning in mice: involvement of nitric oxide. Eur J Pharmacol 2005; 507: 107-115.
34. Rezayof A, Zatali H, Haeri-Rohani A, Zarrindast MR: Dorsal hippocampal muscarinic and nicotinic receptors are involved in mediating morphine reward. Behav Brain Res 2006; 166: 281-290.
35. D'Amato FR, Cabib S, Puglisi-Allegra S, Patacchioli FR, Cigliana G, Maccari S, Angelucci L: Effects of acute and repeated exposure to stress on the hypothalamo-pituitary-adrenocortical activity in mice during postnatal development. Horm Behav 1992; 26: 474-485.
36. Groer MW, Hill J, Wilkinson JE, Stuart A: Effects of separation and separation with supplemental stroking in BALB/c infant mice. Biol Res Nurs 2002; 3: 119-131.
37. Romeo RD, Fossella JA, Bateup HS, Sisti HM, Brake WG, McEwen BS: Maternal separation suppresses TGF-α mRNA expression in the prefrontal cortex of male and female neonatal C57BL/6 mice. Brain Res Dev Brain Res 2004; 152: 73-77.
38. Gutman DA, Nemeroff CB: Neurobiology of early life stress: rodent studies. Semin Clin Neuropsychiatry 2002; 7: 89-95.
39. Millstein RA, Holmes A: Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 2007; 31: 3-17.
40. Millstein RA, Ralph RJ, Yang RJ, Holmes A: Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes Brain Behav 2006; 5: 346-354.
41. Ogawa T, Mikuni M, Kuroda Y, Muneoka K, Mori KJ, Takahashi K: Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open field-induced behaviors. Pharmacol Biochem Behav 1994; 49: 961-967.
42. Parfitt DB, Levin JK, Saltstein KP, Klayman AS, Greer LM, Helmreich DL: Differential early rearing environments can accentuate or attenuate the responses to stress in male C57BL/6 mice. Brain Res 2004; 1016: 111-118.
43. Avitsur R, Hunzeker J, Sheridan JF: Role of early stress in the individual differences in host response to viral infection. Brain Behav Immun 2006; 20: 339-348.
44. Craft TK, Zhang N, Glasper ER, Hurn PD, Devries AC: Neonatal factors influence adult stroke outcome. Psychoneuroendocrinology 2006; 31: 601-613.
45. Zaharia MD, Kulczycki J, Shanks N, Meaney MJ, Anisman H: The effects of early postnatal stimulation on Morris water-maze acquisition in adult mice: genetic and maternal factors. Psychopharmacology (Berl) 1996; 128: 227-239.
46. Loizzo A, Loizzo S, Galietta G, Caiola S, Spampinato S, Campana G, Seghieri G, Ghirlanda G, Franconi F: Overweight and metabolic and hormonal parameter disruption are induced in adult male mice by manipulations during lactation period. Pediatr Res 2006; 59: 111-115.
47. Romeo RD, Mueller A, Sisti HM, Ogawa S, McEwen BS, Brake WG: Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Horm Behav 2003; 43: 561-567.
48. Veenema AH, Bredewold R, Neumann ID: Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 2007; 32: 437-450.
49. D'Amato FR, Cabib S, Ventura R, Orsini C: Long-term effects of postnatal manipulation on emotionality are prevented by maternal anxiolytic treatment in mice. Dev Psychobiol 1998; 32: 225-234.
50. Ferry B, Roozendaal B, McGaugh JL: Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala. Biol Psychiatry 1999; 46: 1140-1152.
51. McGaugh JL, McIntyre CK, Power AE: Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol Learn Mem 2002; 78: 539-552.
52. Ladd CO, Thrivikraman KV, Huot RL, Plotsky PM: Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates. Psychoneuroendocrinology 2005; 30: 520-533.
53. Dirks A, Fish EW, Kikusui T, van der Gugten J, Groenink L, Olivier B, Miczek KA: Effects of corticotropin-releasing hormone on distress vocalizations and locomotion in maternally separated mouse pups. Pharmacol Biochem Behav 2002; 72: 993-999.
54. Schmidt MV, Levine S, Alam S, Harbich D, Sterlemann V, Ganea K, de Kloet ER, Holsboer F, Muller MB: Metabolic signals modulate hypothalamic-pituitary- adrenal axis activation during maternal separation of the neonatal mouse. J Neuroendocrinol 2006; 18: 865-874.
55. Rahman W, Fitzgerald M, Aynsley-Green A, Dickenson A: The effects of neonatal exposure to inflammation and/or morphine on neuronal responses and morphine analgesia in adult rats; in Jensen TS, Turner JA, Wiesenfeld-Hallin Z (eds): Proceedings of the 8th World Congress on Pain: Progress in Pain Research and Management. Seattle, IASP Press, 1997, pp 783-790.
56. Ruda MA, Ling QD, Hohmann AG, Peng YB, Tachibana T: Altered nociceptive neuronal circuits after neonatal peripheral inflammation. Science 2000; 289: 628-631.
57. Hammer RP Jr, Ricalde AA, Seatriz JV: Effects of opiates on brain development. Neurotoxicology 1989; 10: 475-483.
58. Kornblum HI, Loughlin SE, Leslie FM: Effects of morphine on DNA synthesis in neonatal rat brain. Brain Res 1987; 428: 45-52.
59. Hu S, Sheng WS, Lokensgard JR, Peterson PK: Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 2002; 42: 829-836.
60. Lim G, Wang S, Lim JA, Mao J: Activity of adenylyl cyclase and protein kinase A contributes to morphine-induced spinal apoptosis. Neurosci Lett 2005; 389: 104-108.
61. Singhal P, Kapasi A, Reddy K, Franki N: Opiates promote T cell apoptosis through JNK and caspase pathway. Adv Exp Med Biol 2001; 493: 127-135.
62. Boronat MA, Garcia-Fuster MJ, Garcia-Sevilla JA: Chronic morphine induces up-regulation of the pro-apoptotic Fas receptor and down-regulation of the anti-apoptotic Bcl-2 oncoprotein in rat brain. Br J Pharmacol 2001; 134: 1263-1270.
63. Frenklakh L, Bhat RS, Bhaskaran M, Sharma S, Sharma M, Dinda A, Singhal PC: Morphine-induced degradation of the host defense barrier role of intestinal mucosal injury. Dig Dis Sci 2006; 51: 318-325.
64. Hauser KF, Houdi AA, Turbek CS, Elde RP, Maxson W 3rd: Opioids intrinsically inhibit the genesis of mouse cerebellar granule neuron precursors in vitro: differential impact of mu and delta receptor activation on proliferation and neurite elongation. Eur J Neurosci 2000; 12: 1281-1293.
65. Wigger A, Neumann ID: Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 1999; 66: 293-302.
66. Kawakami SE, Quadros IM, Takahashi S, Suchecki D: Long maternal separation accelerates behavioural sensitization to ethanol in female, but not in male mice. Behav Brain Res 2007.
67. MacQueen GM, Ramakrishnan K, Ratnasingan R, Chen B, Young LT: Desipramine treatment reduces the long-term behavioural and neurochemical sequelae of early-life maternal separation. Int J Neuropsychopharmacol 2003; 6: 391-396.
68. Gallegos G, Salazar L, Ortiz M, Marquez W, Davis A, Sanchez S, Conner D, Schreiber HL 3rd: Simple disturbance of the dam in the neonatal period can alter haloperidol-induced catalepsy in the adult offspring. Behav Neural Biol 1990; 53: 172-188.
69. Hall RW, Kronsberg SS, Barton BA, Kaiser JR, Anand KJ: Morphine, hypotension, and adverse outcomes among preterm neonates: who's to blame? Secondary results from the NEOPAIN trial. Pediatrics 2005; 115: 1351-1359.
70. Anderson BJ, Palmer GM: Recent developments in the pharmacological management of pain in children. Curr Opin Anaesthesiol 2006; 19: 285-292.
71. Mikkelsen S, Feilberg VL, Christensen CB, Lundstrom KE: Morphine pharmacokinetics in premature and mature newborn infants. Acta Paediatr 1994; 83: 1025-1028.
72. Lugo RA, Kern SE: Clinical pharmacokinetics of morphine. J Pain Palliat Care Pharmacother 2002; 16: 5-18.
73. Bouwmeester NJ, Anderson BJ, Tibboel D, Holford NH: Developmental pharmacokinetics of morphine and its metabolites in neonates, infants and young children. Br J Anaesth 2004; 92: 208-217.
74. AAP: Prevention and management of pain and stress in the neonate. American Academy of Pediatrics. Committee on Fetus and Newborn. Committee on Drugs. Section on Anesthesiology. Section on Surgery. Canadian Paediatric Society. Fetus and Newborn Committee. Pediatrics 2000; 105: 454-461.
75. Peabody JL, Martin GI: From how small is too small to how much is too much. Ethical issues at the limits of neonatal viability. Clin Perinatol 1996; 23: 473-489.
76. Anand KJ, Aranda JV, Berde CB, Buckman S, Capparelli EV, Carlo W, Hummel P, Johnston CC, Lantos J, Tutag-Lehr V, Lynn AM, Maxwell LG, Oberlander TF, Raju TN, Soriano SG, Taddio A, Walco GA: Summary proceedings from the neonatal pain-control group. Pediatrics 2006; 117:S9-S22.
77. Clancy GT, Anand KJ, Lally P: Neonatal pain management. Crit Care Nurs Clin North Am 1992; 4: 527-535.
78. Kikusui T, Faccidomo S, Miczek KA: Repeated maternal separation: differences in cocaine-induced behavioral sensitization in adult male and female mice. Psychopharmacology (Berl) 2005; 178: 202-210.