The Effects of Maternal Separation on Adult Methamphetamine Self-Administration, Extinction, Reinstatement, and MeCP2 Immunoreactivity in the Nucleus Accumbens

Overview

Journal Front Psychiatry

Specialty Psychiatry

Date 2013 Jun 21

PMID 23785337

Citations 41

Authors

Candace R Lewis

Kelsey Staudinger

Lena Scheck

M Foster Olive

Affiliations

Soon will be listed here.

Abstract

The maternal separation (MS) paradigm is an animal model of early life stress. Animals subjected to MS during the first 2 weeks of life display altered behavioral and neuroendocrinological stress responses as adults. MS also produces altered responsiveness to and self-administration (SA) of various drugs of abuse including cocaine, ethanol, and amphetamine. However, no studies have yet examined the effects of MS on methamphetamine (METH) SA. This study was performed to examine the effects of MS on the acquisition of METH SA, extinction, and reinstatement of METH-seeking behavior in adulthood. Given the known influence of early life stress and drug exposure on epigenetic processes, we also investigated group differences in levels of the epigenetic marker methyl CpG binding protein 2 (MeCP2) in the nucleus accumbens (NAc) core. Long-Evans pups and dams were separated on postnatal days (PND) 2-14 for either 180 (MS180) or 15 min (MS15). Male offspring were allowed to acquire METH SA (0.05 mg/kg/infusion) in 15 2-h daily sessions starting at PND67, followed by extinction training and cue-induced reinstatement of METH-seeking behavior. Rats were then assessed for MeCP2 levels in the NAc core by immunohistochemistry. The MS180 group self-administered significantly more METH and acquired SA earlier than the MS15 group. No group differences in extinction or cue-induced reinstatement were observed. MS15 rats had significantly elevated MeCP2-immunoreactive cells in the NAc core as compared to MS180 rats. Together, these data suggest that MS has lasting influences on METH SA as well as epigenetic processes in the brain reward circuitry.

Citing Articles

Early social isolation differentially affects the glucocorticoid receptor system and alcohol-seeking behavior in male and female Marchigian Sardinian alcohol-preferring rats.

Benvenuti F, De Carlo S, Rullo L, Caffino L, Losapio L, Morosini C Neurobiol Stress. 2023; 28:100598.

PMID: 38115888 PMC: 10727952. DOI: 10.1016/j.ynstr.2023.100598.

Sex differences in addiction-relevant behavioral outcomes in rodents following early life stress.

Rincon-Cortes M Addict Neurosci. 2023; 6.

PMID: 37101684 PMC: 10124992. DOI: 10.1016/j.addicn.2023.100067.

Early-life adversity increases anxiety-like behavior and modifies synaptic protein expression in a region-specific manner.

Hamdan J, Sierra-Fonseca J, Flores R, Saucedo Jr S, Miranda-Arango M, ODell L Front Behav Neurosci. 2022; 16:1008556.

PMID: 36338879 PMC: 9626971. DOI: 10.3389/fnbeh.2022.1008556.

Effects of prenatal opioid exposure on synaptic adaptations and behaviors across development.

Simmons S, Grecco G, Atwood B, Nugent F Neuropharmacology. 2022; 222:109312.

PMID: 36334764 PMC: 10314127. DOI: 10.1016/j.neuropharm.2022.109312.

Oxytocin as an adolescent treatment for methamphetamine addiction after early life stress in male and female rats.

Baracz S, Robinson K, Wright A, Turner A, McGregor I, Cornish J Neuropsychopharmacology. 2022; 47(8):1561-1573.

PMID: 35581382 PMC: 9206013. DOI: 10.1038/s41386-022-01336-y.

References

Francis D, Champagne F, Liu D, Meaney M . Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann N Y Acad Sci. 2000; 896:66-84. DOI: 10.1111/j.1749-6632.1999.tb08106.x. View

Roth T . Epigenetics of neurobiology and behavior during development and adulthood. Dev Psychobiol. 2012; 54(6):590-7. DOI: 10.1002/dev.20550. View

Murgatroyd C, Patchev A, Wu Y, Micale V, Bockmuhl Y, Fischer D . Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci. 2009; 12(12):1559-66. DOI: 10.1038/nn.2436. View

Skene P, Illingworth R, Webb S, Kerr A, James K, Turner D . Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol Cell. 2010; 37(4):457-68. PMC: 4338610. DOI: 10.1016/j.molcel.2010.01.030. View

Bolanos C, Nestler E . Neurotrophic mechanisms in drug addiction. Neuromolecular Med. 2004; 5(1):69-83. DOI: 10.1385/NMM:5:1:069. View

Anda R, Felitti V, Douglas Bremner J, Walker J, Whitfield C, Perry B . The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. Eur Arch Psychiatry Clin Neurosci. 2005; 256(3):174-86. PMC: 3232061. DOI: 10.1007/s00406-005-0624-4. View

Francis D, Kuhar M . Frequency of maternal licking and grooming correlates negatively with vulnerability to cocaine and alcohol use in rats. Pharmacol Biochem Behav. 2008; 90(3):497-500. PMC: 2559944. DOI: 10.1016/j.pbb.2008.04.012. View

Vazquez V, Penit-Soria J, Durand C, Besson M, Giros B, Dauge V . Maternal deprivation increases vulnerability to morphine dependence and disturbs the enkephalinergic system in adulthood. J Neurosci. 2005; 25(18):4453-62. PMC: 6725024. DOI: 10.1523/JNEUROSCI.4807-04.2005. View

Thiel K, Sanabria F, Pentkowski N, Neisewander J . Anti-craving effects of environmental enrichment. Int J Neuropsychopharmacol. 2009; 12(9):1151-6. PMC: 2832121. DOI: 10.1017/S1461145709990472. View

10.

Lippmann M, Bress A, Nemeroff C, Plotsky P, Monteggia L . Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur J Neurosci. 2007; 25(10):3091-8. DOI: 10.1111/j.1460-9568.2007.05522.x. View

11.

Piazza P, Deminiere J, Le Moal M, Simon H . Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration. Brain Res. 1990; 514(1):22-6. DOI: 10.1016/0006-8993(90)90431-a. View

12.

Breese G, Sinha R, Heilig M . Chronic alcohol neuroadaptation and stress contribute to susceptibility for alcohol craving and relapse. Pharmacol Ther. 2010; 129(2):149-71. PMC: 3026093. DOI: 10.1016/j.pharmthera.2010.09.007. View

13.

Messina N, Marinelli-Casey P, Hillhouse M, Rawson R, Hunter J, Ang A . Childhood adverse events and methamphetamine use among men and women. J Psychoactive Drugs. 2009; Suppl 5:399-409. DOI: 10.1080/02791072.2008.10400667. View

14.

Matthews K, Dalley J, Matthews C, Tsai T, Robbins T . Periodic maternal separation of neonatal rats produces region- and gender-specific effects on biogenic amine content in postmortem adult brain. Synapse. 2001; 40(1):1-10. DOI: 10.1002/1098-2396(200104)40:1<1::AID-SYN1020>3.0.CO;2-E. View

15.

Solinas M, Thiriet N, Chauvet C, Jaber M . Prevention and treatment of drug addiction by environmental enrichment. Prog Neurobiol. 2010; 92(4):572-92. DOI: 10.1016/j.pneurobio.2010.08.002. View

16.

Marmendal M, Roman E, Eriksson C, Nylander I, Fahlke C . Maternal separation alters maternal care, but has minor effects on behavior and brain opioid peptides in adult offspring. Dev Psychobiol. 2004; 45(3):140-52. DOI: 10.1002/dev.20027. View

17.

McGowan P, Sasaki A, DAlessio A, Dymov S, Labonte B, Szyf M . Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009; 12(3):342-8. PMC: 2944040. DOI: 10.1038/nn.2270. View

18.

Jaworski J, Francis D, Brommer C, Morgan E, Kuhar M . Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Psychopharmacology (Berl). 2005; 181(1):8-15. DOI: 10.1007/s00213-005-2232-4. View

19.

Kinnally E, Feinberg C, Kim D, Ferguson K, Leibel R, Coplan J . DNA methylation as a risk factor in the effects of early life stress. Brain Behav Immun. 2011; 25(8):1548-53. PMC: 3191272. DOI: 10.1016/j.bbi.2011.05.001. View

20.

Dimatelis J, Russell V, Stein D, Daniels W . Effects of maternal separation and methamphetamine exposure on protein expression in the nucleus accumbens shell and core. Metab Brain Dis. 2012; 27(3):363-75. DOI: 10.1007/s11011-012-9295-9. View