Early neonatal experience of Long-Evans rats results in long-lasting changes in morphine tolerance and dependence

Kalinichev, Mikhail; Easterling, Keith W.; Holtzman, Stephen G.

doi:10.1007/s002130100806

Cited by 56Neuropeptides and Animal PhysiologyStress Responses and CortisolNeurotransmitter Receptor Influence on Behavior

Early neonatal experience of Long-Evans rats results in long-lasting changes in morphine tolerance and dependence

Kalinichev, Mikhail, Easterling, Keith W., Holtzman, Stephen G.·2001·Psychopharmacology

DOI 10.1007/s002130100806

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Abstract

Rationale Daily, 3-h separations from the dam on postnatal days 2-14 produce long-lasting changes in behavioral and neuroendocrine responses to stressors and sensitivity to acute morphine in Long-Evans rats.Objective We tested whether offspring that were separated from their dam for 3 h daily (MS) on postnatal days 2-14 exhibit altered sensitivity to chronic morphine, compared to animals that experienced only brief (15 min) separations (H) from the dam or that were left undisturbed (NH) during the same period.Methods Subjects received 1 week SC infusion of either morphine, or saline via osmotic pumps. Twenty-hours after pump removal, the global opioid withdrawal scores were recorded. Four hours later, animals were tested for antinociception (tail-flick and hot-plate tests) during cumulative morphine administration.Results MS males and MS females undergoing withdrawal from chronic morphine had higher global withdrawal scores compared to NH controls. MS males (but not MS females) were less sensitive to the antinociceptive effects of morphine compared to H and NH controls, primarily in the hot-plate test, regardless of whether they had received a saline or a morphine infusion. MS males consistently exhibited significant morphine tolerance, whereas control males failed to exhibit tolerance either in the hot-plate test (NH group) or in both antinociception assays (H group). In contrast, tolerance was exhibited by all females in both tests for antinociception.Conclusions These data indicate that repeated neonatal maternal separation alters sensitivity to chronic morphine administration in a sex-dependent manner.

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Maternal separation is associated with changes to the opioid system, but results conflict depending on methodology, showing both increases and decreases in endogenous peptide levels and ligand sensitivity.
“Changes to the opioid system are also apparent with maternal separation, but conflicting results also exist based on specific methodology, demonstrating both increases and decreases in levels of endogenous peptides (Ploj et al., 2003; Vazquez et al., 2005) as well as sensitivity to ligands (Kalinichev et al., 2001; Vazquez et al., 2005).”
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Heim, C. (2000) · JAMA · doi:10.1001/jama.284.5.592 · Cited by 1,968 · see citing works
Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Posttraumatic stress disorder in abused and neglected children grown up
Widom, C. S. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.8.1223 · Cited by 945 · see citing works
Early Environmental Regulation of Forebrain Glucocorticoid Receptor Gene Expression: Implications for Adrenocortical Responses to Stress; pp. 49–60
Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R., & Plotsky, P. M. (2010) · Developmental Neuroscience · doi:10.1159/000111395 · Cited by 878 · see citing works
Infantile Experience and Resistance to Physiological Stress
Levine, S. (1957) · Science · doi:10.1126/science.126.3270.405 · Cited by 659 · see citing works
The Effects of Early Rearing Environment on the Development of GABAA and Central Benzodiazepine Receptor Levels and Novelty-Induced Fearfulness in the Rat
Caldji, C. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 606 · see citing works
Catecholaminergic Modulation of Corticotropin-Releasing Factor and Adrenocorticotropin Secretion
Plotsky, P. M., Cunningham, E. T., & Widmaier, E. P. (1989) · Endocrine Reviews · doi:10.1210/edrv-10-4-437 · Cited by 530 · see citing works
Development of physical dependence on morphine in respect to time and dosage and quantification of the precipitated withdrawal syndrome in rats
Bl�sig, J., Herz, A., Reinhold, K., & Zieglg�nsberger, S. (1973) · Psychopharmacology · doi:10.1007/bf00428791 · Cited by 521 · see citing works
Influence of Neonatal Rearing Conditions on Stress‐Induced Adrenocorticotropin Responses and Norepinepherine Release in the Hypothalamic Paraventricular Nucleus
Liu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 451 · see citing works
Periodic Maternal Deprivation Induces Gender-Dependent Alterations in Behavioral and Neuroendocrine Responses to Emotional Stress in Adult Rats
Wigger, A., & Neumann, I. D. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00300-x · Cited by 443 · see citing works
The effects of neonatal handling on the development of the adrenocortical response to stress: Implications for neuropathology and cognitive deficits in later life
Meaney, M. J., Mitchell, J. B., Aitken, D. H., Bhatnagar, S., Bodnoff, S. R., Iny, L. J., & Sarrieau, A. (1991) · Psychoneuroendocrinology · doi:10.1016/0306-4530(91)90072-2 · Cited by 370 · see citing works
Mother rats interact differently with male amd female offspring.
Moore, C. L., & Morelli, G. A. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077599 · Cited by 353 · see citing works
Relationship of childhood maltreatment to the onset and course of major depression in adulthood
Bernet, C. Z., & Stein, M. B. (1999) · Depression and Anxiety · doi:10.1002/(sici)1520-6394(1999)9:4 · Cited by 289 · see citing works
Continuous recording of maternal behaviour in Rattus norvegicus
Grota, L. J., & Ader, R. (1969) · Animal Behaviour · doi:10.1016/s0003-3472(69)80019-9 · Cited by 265 · see citing works
Development and maintenance of morphine tolerance and dependence in the rat by scheduled access to morphine drinking solutions.
Gellert, V. F., & Holtzman, S. G. (1978) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)31261-9 · Cited by 265 · see citing works
Self-citation
Childhood physical assault as a risk factor for PTSD, depression, and substance abuse: Findings from a national survey.
Duncan, R. D., Saunders, B. E., Kilpatrick, D. G., Hanson, R. F., & Resnick, H. S. (1996) · American Journal of Orthopsychiatry · doi:10.1037/h0080194 · Cited by 260 · see citing works
Short- and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects
McIntosh, J. F., Anisman, H., & Merali, Z. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00005-x · Cited by 255 · see citing works
Persistent changes in corticotropin-releasing factor systems due to early life stress: relationship to the pathophysiology of major depression and post-traumatic stress disorder.
Heim, C. C., Owens, M. J., Plotsky, P. M., & Nemeroff, C. B. (1997) · PubMed · Cited by 206 · see citing works
Childhood Trauma and Posttraumatic Stress Disorder in Substance Abuse Inpatients
Triffleman, E., Marmar, C. R., Delucchi, K., & Ronfeldt, H. M. (1995) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-199503000-00008 · Cited by 185 · see citing works
Aetiology of anxiety and depressive disorders in an inner-city population. 1. Early adversity
Brown, G. W., & Harris, T. (1993) · Psychological Medicine · doi:10.1017/s0033291700038939 · Cited by 183 · see citing works
Hyperalgesia during Naloxone-Precipitated Withdrawal from Morphine Is Associated with Increased On-Cell Activity in the Rostral Ventromedial Medulla
Bederson, J. B., Fields, H. L., & Barbaro, N. M. (1990) · Somatosensory & Motor Research · doi:10.3109/08990229009144706 · Cited by 182 · see citing works
Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood
Matthews, K., Wilkinson, L. S., & Robbins, T. W. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02069-1 · Cited by 178 · see citing works
Childhood Victimization and Risk for Alcohol and Drug Arrests
Ireland, T. O., & Widom, C. S. (1994) · International Journal of the Addictions · doi:10.3109/10826089409047380 · Cited by 177 · see citing works
Differential effects of spinal cord lesions on narcotic and non-narcotic supression of nociceptive reflexes: Further evidence for the physiologic multiplicity of pain modulation
Hayes, R. L., Price, D. D., Bennett, G. J., Wilcox, G. L., & Mayer, D. J. (1978) · Brain Research · doi:10.1016/0006-8993(78)90307-4 · Cited by 157 · see citing works
Repeated neonatal maternal separation alters intravenous cocaine self-administration in adult rats
Matthews, K., Robbins, T. W., Everitt, B. J., & Caine, S. B. (1999) · Psychopharmacology · doi:10.1007/s002130050816 · Cited by 141 · see citing works
Effects of early experience on adrenocortical reactivity
Ader, R., & Grota, L. J. (1969) · Physiology & Behavior · doi:10.1016/0031-9384(69)90179-6 · Cited by 140 · see citing works
Development of tolerance to the analgesic activity of mu agonists after continuous infusion of morphine, meperidine or fentanyl in rats.
Paronis, C. A., & Holtzman, S. G. (1992) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)10719-2 · Cited by 138 · see citing works
Self-citation
Afferent and efferent connections of the rat tail flick reflex (a model used to analyze pain control mechanisms)
Grossman, M. L., Basbaum, A. I., & Fields, H. L. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902060103 · Cited by 133 · see citing works
Behaviorally functional opioid systems in infant rats: II. Evidence for pharmacological, physiological, and psychological mediation of pain and stress.
Kehoe, P., & Blass, E. M. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.5.624 · Cited by 120 · see citing works
Prevalence of Childhood Trauma in a Community Sample of Substance-Abusing Women
Medrano, M. A., Zule, W. A., Hatch, J. P., & Desmond, D. P. (1999) · The American Journal of Drug and Alcohol Abuse · doi:10.1081/ada-100101872 · Cited by 112 · see citing works
Hot plate versus tail flick: Evaluation of acute tolerance to continuous morphine infusion in the rat model
Langerman, L., Zakowski, M. I., Piskoun, B., et al. (1995) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/1056-8719(94)00077-h · Cited by 102 · see citing works
Tolerance to the analgesic, but not discriminative stimulus effects of morphine after brief social defeat in rats
Miczek, K. A. (1991) · Psychopharmacology · doi:10.1007/bf02244176 · Cited by 91 · see citing works
Characterization of stress-induced potentiation of opioid effects in the rat.
Appelbaum, B. D., & Holtzman, S. G. (1984) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)21691-3 · Cited by 83 · see citing works
Self-citation
MORPHINE PHYSICAL DEPENDENCE IN THE DOG
Martin, W. R., Eades, C. G., Thompson, W. O., et al. (1974) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)29884-6 · Cited by 83 · see citing works
Mother-infant interactions in two strains of rats: Implications for dissociating mechanism and function of a maternal pattern
Moore, C., Wong, L., Daum, M. C., & Leclair, O. U. (1997) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199705)30:4 · Cited by 77 · see citing works
Morphine analgesia and tolerance in the tail-flick and formalin tests: Dose-response relationships
Abbott, F. V., Melzack, R., & Leber, B. F. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90123-x · Cited by 72 · see citing works
Immobilization stress-induced oral opioid self-administration and withdrawal in rats: role of conditioning factors and the effect of stress on “relapse” to opioid drugs
Shaham, Y. (1993) · Psychopharmacology · doi:10.1007/bf02253539 · Cited by 69 · see citing works
Analgesia Following Defeat in an Aggressive Encounter: Development of Tolerance and Changes in Opioid Receptorsa
Miczek, K. A., Thompson, M. L., & Shuster, L. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb14615.x · Cited by 65 · see citing works
Repeated neonatal maternal separation alters morphine-induced antinociception in male rats
Kalinichev, M., Easterling, K. W., & Holtzman, S. G. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00485-3 · Cited by 65 · see citing works
Self-citation
Tolerance and dependence after continuous morphine infusion from osmotic pumps measured by operant responding in rats
Adams, J. U., & Holtzman, S. G. (1990) · Psychopharmacology · doi:10.1007/bf02243995 · Cited by 57 · see citing works
Self-citation
Child Maltreatment and Substance Use: A Review of the Literature
Arellano, C. M. (1996) · Substance Use & Misuse · doi:10.3109/10826089609063963 · Cited by 57 · see citing works
Exposure to uncontrollable stress alters withdrawal from morphine.
Williams, J. L., Drugan, R. C., & Maier, S. F. (1984) · Behavioral Neuroscience · doi:10.1037//0735-7044.98.5.836 · Cited by 32 · see citing works
Early life events and panic disorder: Course of illness and comorbidity
Servant, D., & Parquet, P. J. (1994) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(94)90069-8 · Cited by 23 · see citing works
Repetitive exposure to the hot-plate test produces stress induced analgesia and alters β-endorphin neuronal transmission within the periaqueductal gray of the rat
Hawranko, A. A., Monroe, P. J., & Smith, D. J. (1994) · Brain Research · doi:10.1016/0006-8993(94)91508-3 · Cited by 22 · see citing works
Amniotic-Fluid Ingestion Enhances \nMorphine Analgesia During Morphine \nTolerance and Withdrawal in RatsPreprint
Doerr, J. C., & Kristal, M. B. (1991) · CogPrints (University of Southampton) · Cited by 14 · see citing works
Chronic morphine administration and in vivo pertussis toxin treatment induce hyperalgesia and enhance 3H-nitrendipine binding.
Inoki, R., Ohnishi, T., Saito, K., et al. (1990) · PubMed · Cited by 12 · see citing works
Acute morphine dependence in mice selectively-bred for high and low analgesia
Kest, B., McLemore, G. L., Sadowski, B., et al. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00772-1 · Cited by 10 · see citing works

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“, 2005) as well as sensitivity to ligands (Kalinichev et al., 2001; Vazquez et al., 2005).”
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Authors: Kalinichev, M., Easterling, K. W., & Holtzman, S. G.
Affiliations: Emory University (US)
ORCID: Kalinichev, Mikhail
Venue: Psychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2001-07-25
Volume: 157
Issue: 3
Pages: 305-312
ISSN: 0033-3158 (ISSN-L)
1432-2072
DOI: 10.1007/s002130100806
OpenAlex: W1979162388
Cited by: 56
References: 47
Citations by year: 2024: 1 · 2023: 2 · 2021: 5 · 2019: 1 · 2018: 4 · 2017: 3 · 2015: 1 · 2014: 2 · 2013: 1 · 2012: 3
FWCI: 1.11
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Psychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute on Drug Abuse (K05-DA00008, DA11384, K05DA000008, R21DA011384)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: neonatal maternal separation, morphine tolerance, morphine dependence, opioid withdrawal, antinociception, sex differences, postnatal development, Long-Evans rats, chronic morphine administration
MeSH terms: Analgesics, Opioid, Animals, Animals, Newborn, Drug Tolerance, Female, Male, Maternal Deprivation, Morphine, Morphine Dependence, Pain Measurement, Reaction Time, Sex Characteristics, Substance Withdrawal Syndrome, Rats, Long-Evans, Rats

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Early neonatal experience of Long-Evans rats results in long-lasting changes in morphine tolerance and dependence

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