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Vol. 36, No. 1, 2014
Issue release date: March 2014
Dev Neurosci 2014;36:18-28
(DOI:10.1159/000357495)

Late-Life Effects of Chronic Methamphetamine Exposure during Puberty on Behaviour and Corticostriatal Mono-Amines in Social Isolation-Reared Rats

Strauss L. · Brink C.B. · Möller M. · Stein D.J. · Harvey B.H.
aDivision of Pharmacology, School of Pharmacy, and bCentre of Excellence for Pharmaceutical Sciences, Faculty of Health Sciences, North-West University, Potchefstroom, and cMRC Unit for Anxiety and Stress Disorders, Department of Psychiatry, University of Cape Town, Cape Town, South Africa

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Abstract

Chronic methamphetamine (MA) abuse results in an acute psychosis indistinguishable from paranoid schizophrenia. However, less is known of the interaction between MA use and environmental insults, and how this contributes to late-onset psychopathology. Using social isolation rearing (SIR), a neurodevelopmental animal model of schizophrenia, we investigated the association between changes in corticostriatal mono-amines and putative behaviours related to MA-induced psychosis in isolation and group-housed rats following chronic MA or saline exposure. Weaned male offspring of MA-naive female Wistar rats, either group- or isolation-housed from postnatal day (PND) +21, received saline (2 ml/kg s.c. b.i.d.) or an escalating dose of MA (0.2-6 mg/kg s.c. b.i.d.) for 16 days from PND +35 to +50. On PND +78, offspring were tested for deficits in social interactive behaviour (SIB) and prepulse inhibition (PPI) of startle, with frontal cortex and striatum harvested for the assessment of mono-amine concentrations. SIR significantly reduced rearing time, staying together, approaching and anogenital sniffing (outward-directed SIB), but increased self-grooming and locomotor activity (self-directed SIB), and also induced profound deficits in PPI. Pubertal MA exposure in group-housed animals also induced similar alterations in outward- and self-directed SIB and reduced PPI. Combined MA + SIR exposure evoked a similarly intense behavioural response as SIR or MA separately, with no exacerbation evident. Neither treatment separately nor together affected corticostriatal serotonin or noradrenaline levels, although frontal cortical dopamine (DA) levels were significantly increased in SIR and MA + group-housed animals. A trend towards further elevated frontal cortical DA was noted in the MA + SIR treatment group. Striatal DA was unaltered by all treatments. This study provides the first evidence that chronic pubertal MA exposure evokes postpubertal psychosis-like behaviours in rats of similar intensity to that induced by a neurodevelopmental animal model of schizophrenia (SIR). Moreover, the study is unique in that these behavioural changes occur together with associated changes in frontal cortical but not striatal DA, without affecting other mono-amines, and strongly implicates frontal cortical DA changes in the psychotogenic effects of early-life MA exposure or environmental insult. Although MA exposure in animals with a history of environmental insult (i.e. MA + SIR) has similar effects, combined exposure was not additive with regard to behavioural or neurochemical changes. We conclude that a ceiling effect or compensatory mechanisms prevent more pronounced neurobehavioural deficits occurring following MA + SIR treatment, at least under the current study conditions. © 2014 S. Karger AG, Basel



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References

  1. Yamamoto BK, Moszczynska A, Gudelsky GA: Amphetamine toxicities: classical and emerging mechanisms. Ann NY Acad Sci 2010;1187:101-121.
  2. Kirkpatrick MG, Gunderson EW, Perez AY, Haney M, Foltin RW, Hart CL: A direct comparison of the behavioural and physiological effects of methamphetamine and 3,4-methylenedioxymethamphetamine (MDMA) in humans. Psychopharmacology 2012;219:109-122.
  3. Vos PJ, Cloete KJ, Le Roux A, Kidd M, Jordaan GP: A retrospective review of the trends and clinical characteristics of methamphetamine-related acute psychiatric admissions in a South African context. Afr J Psychiatry 2010;13:390-394.
  4. Imam SZ, Ali SF: Aging increases the susceptibility to methamphetamine-induced dopaminergic neurotoxicity in rats: correlation with peroxynitrite production and hyperthermia. J Neurochem 2001;78:952-959.
  5. Grace CE, Schaefer TL, Herring NR, Graham DL, Skelton MR, Gudelsky GA, Williams MT, Vorhees CV: Effect of a neurotoxic dose regimen of (+)-methamphetamine on behaviour, plasma corticosterone, and brain monoamines in adult C57BL/6 mice. Neurotoxicol Teratol 2010;32:346-355.
  6. Srisurapanont M, Arunpongpaisal S, Wada K, Marsden J, Ali R, Kongsakon R: Comparisons of methamphetamine psychotic and schizophrenic symptoms: a differential item functioning analysis. Prog Neuropsychopharmacol Biol Psychiatry 2011;35:959-964.
  7. Hart CL, Marvin CB, Silver R, Smith EE: Is cognitive functioning impaired in methamphetamine users? A critical review. Neuropsychopharmacology 2012;37:586-608.
  8. Fone KCF, Porkess MV: Behavioural and neurochemical effects of post-weaning social isolation in rodents - relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 2008;32:1087-1102.
  9. Daenen EWPM, Wolterink G, Van Der Heyden JA, Kruse CG, Van Ree JM: Neonatal lesions in the amygdala or ventral hippocampus disrupt prepulse inhibition of the acoustic startle response: implications for an animal model of neurodevelopmental disorders like schizophrenia. Eur Neuropsychopharmacol 2003;13:187-197.
  10. Dore G, Sweeting M: Drug-induced psychosis associated with crystalline methamphetamine. Australas Psychiatry 2006;14:86-89.
  11. McKetin R, Lubman DI, Baker AL, Dawe S, Ali RL: Dose-related psychotic symptoms in chronic methamphetamine users: evidence from a prospective longitudinal study. JAMA Psychiatry 2013;70:319-324.
  12. Cruickshank CC, Dyer KR: A review of the clinical pharmacology of methamphetamine. Addiction 2009;104:1085-1099.
  13. Akiyama K, Saito A, Shimoda K: Chronic methamphetamine psychosis after long-term abstinence in Japanese incarcerated patients. Am J Addict 2011;20:240-249.
  14. Rusyniak DE: Neurologic manifestations of chronic methamphetamine abuse. Neurol Clin 2011;29:641-655.
  15. Nakamura K, Sekine Y, Takei N, Iwata Y, Suzuki K, Anitha A, Inada T, Harano M, Komiyama T, Yamada M, Iwata N, Iyo M, Sora I, Ozaki N, Ujike H, Mori N: An association study of monoamine oxidase A (MAOA) gene polymorphism in methamphetamine psychosis. Neurosci Lett 2009;455:120-123.
  16. Yui K, Ikemoto S, Ishiguro T, Goto K: Studies of amphetamine or methamphetamine psychosis in Japan: relation of methamphetamine psychosis to schizophrenia. Ann NY Acad Sci 2000;914:1-12.
  17. Dimatelis JJ, Russell VA, Stein DJ, Daniels WM: The effects of lobeline and naltrexone on methamphetamine-induced place preference and striatal dopamine and serotonin levels in adolescent rats with a history of maternal separation. Metab Brain Dis 2012;27:351-361.
  18. Seeman P: All roads to schizophrenia lead to dopamine supersensitivity and elevated dopamine D2high receptors. CNS Neurosci Ther 2011;17:118-132.
  19. Möller M, Du Preez JL, Emsley R, Harvey BH: Isolation rearing-induced deficits in sensorimotor gating and social interaction in rats are related to cortico-striatal oxidative stress, and reversed by sub-chronic clozapine administration. Eur Neuropsychopharmacol 2011;21:471-483.
  20. Toua C, Brand L, Möller M, Emsley RA, Harvey BH: The effects of sub-chronic clozapine and haloperidol administration on isolation rearing induced changes in frontal cortical N-methyl-D-aspartate and D1 receptor binding in rats. Neuroscience 2010;165:492-499.
  21. Möller M, Du Preez JL, Viljoen FP, Berk M, Harvey BH: N-acetyl cysteine reverses social isolation rearing induced changes in cortico-striatal monoamines in rats. Metabolic Brain Disease 2013;28:687-696.
  22. Möller M, Du Preez JL, Emsley RA, Harvey BH: Social isolation rearing induces mitochondrial, immunological, neurochemical and behavioral deficits in rats, and is reversed by clozapine or N-acetylcysteine. Brain Behav Immun 2013;30:156-167.
  23. Bitanihirwe BKY, Woo TUW: Oxidative stress in schizophrenia: an integrated approach. Neurosci Biobehav Rev 2011;35:878-893.
  24. Stahl SM: Beyond the dopamine hypothesis to the NMDA glutamate receptor hypofunction hypothesis of schizophrenia. CNS Spectr 2007;12:265-268.

    External Resources

  25. Howes OD, Kapur S: The dopamine hypothesis of schizophrenia: version III - the final common pathway. Schizophr Bull 2009;35:549-562.
  26. Bernacer J, Corlett PR, Ramachandra P, McFarlane B, Turner DC, Clark L, Robbins TW, Fletcher PC, Murray GK: Methamphetamine-induced disruption of frontostriatal reward learning signals: relation to psychotic symptoms. Am J Psychiatry 2013;170:1326-1334.
  27. Graham DL, Noailles P-AH, Cadet JL: Differential neurochemical consequences of an escalating dose-binge regimen followed by single-day multiple-dose methamphetamine challenges. J Neurochem 2008;105:1873-1885.
  28. Keller CM, Salvatore MF, Pruett BS, Guerin GF, Goeders NE: Biphasic dopamine regulation in mesoaccumbens pathway in response to non-contingent binge and escalating methamphetamine regimens in the Wistar rat. Psychopharmacology 2011;215:513-526.
  29. Kuczenski R, Everall IP, Crews L, Adame A, Grant I, Masliah E: Escalating dose-multiple binge methamphetamine exposure results in degeneration of the neocortex and limbic system in the rat. Exp Neurol 2007;207:42-51.
  30. Ettinger U, Hejda S, Flak V, Corr PJ: Prepulse inhibition of the acoustic startle reflex and oculomotor control. Psychophysiology 2005;42:473-482.
  31. Cadenhead KS: Startle reactivity and prepulse inhibition in prodromal and early psychosis: effects of age, antipsychotics, tobacco and cannabis in a vulnerable population. Psychiatry Res 2011;188:208-216.
  32. Wang JH, Short J, Ledent C, Lawrence AJ, Van Den Buuse M: Reduced startle habituation and prepulse inhibition in mice lacking adenosine A2A receptor. Behav Brain Res 2003;143:201-207.
  33. Van Den Buuse M, Garner B, Koch M: Neurodevelopmental animal models of schizophrenia: effects on prepulse inhibition. Curr Mol Med 2003;3:459-471.
  34. Shimazaki T, Chaki S: Anxiolytic-like effect of a selective and non-peptidergic melanocortin 4 receptor antagonist, MCL0129, in a social interaction test. Pharmacol Biochem Behav 2005;80:395-400.
  35. Ferdman N, Murmu RP, Bock J, Braun K, Leshem M: Weaning age, social isolation, and gender interact to determine adult explorative and social behaviour, and dendritic and spine morphology in prefrontal cortex of rats. Behav Brain Res 2007;180:174-182.
  36. Gonzalez LE, Andrews N, File SE: 5-HT(1A) and benzodiazepine receptors in the basolateral amygdala modulate anxiety in the social interaction test, but not in the elevated plus-maze. Brain Res 1996;732:145-153.
  37. Sherif F, Oreland L: Effects of chronic treatment with the GABA-transaminase inhibitor vigabatrin on exploratory behaviour in rats. Behav Brain Res 1994;63:11-15.
  38. Paxinos G, Watson C: The Rat Brain in Stereotaxic Coordinates, ed 5. London, Elsevier Academic Press, 2005, p 367.
  39. Harvey BH, Brand L, Jeeva Z, Stein DJ: Cortical/hippocampal monoamines, HPA-axis changes and aversive behaviour following stress and restress in an animal model of post-traumatic stress disorder. Physiol Behav 2006;87:881-890.
  40. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR: Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 2001;156:117-154.
  41. Maxwell JC: Emerging research on methamphetamine. Curr Opin Psychiatry 2005;18:235-242.
  42. Olsson SK, Larsson MK, Erhardt S: Subchronic elevation of brain kynurenic acid augments amphetamine-induced locomotor response in mice. J Neural Transm 2012;119:155-163.
  43. Grant KM, Levan TD, Wells SM, Li M, Stoltenberg SF, Gendelman HE, Carlo G, Bevins RA: Methamphetamine-associated psychosis. J Neuroimmune Pharmacol 2011;7:113-139.
  44. Carlsson A, Waters N, Holm-Waters S, Tedroff J, Nilsson M, Carlsson ML: Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu Rev Pharmacol Toxicol 2001;41:237-260.
  45. Yamamoto K, Hornykiewicz O: Proposal for a noradrenaline hypothesis of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2004;28:913-922.
  46. Leng A, Feldon J, Ferger B: Long-term social isolation and medial prefrontal cortex: dopaminergic and cholinergic neurotransmission. Pharmacol Biochem Behav 2004;77:371-379.
  47. Jones GH, Hernandez TD, Kendall DA, Marsden CA, Robbins TW: Dopaminergic and serotonergic function following isolation rearing in rats: study of behavioural responses and postmortem and in vivo neurochemistry. Pharmacol Biochem Behav 1992;43:17-35.
  48. Han X, Wang W, Shao F, Li N: Isolation rearing alters social behaviors and monoamine neurotransmission in the medial prefrontal cortex and nucleus accumbens of adult rats. Brain Res 2011;1385:175-181.
  49. Wang Y, Chou J, Jeng C-H, Morales M, Wang JY: Chronic methamphetamine exposure decreases high affinity uptake function in norepinephrine afferents in the cerebellar cortex: an electrophysiological and electrochemical study. Neuropharmacology 2000;39:2112-2123.
  50. Limón-Pacheco J, Gonsebatt ME: The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutat Res 2009;674:137-147.
  51. Wong AHC, Van Tol HHM: Schizophrenia: from phenomenology to neurobiology. Neurosci Biobehav Rev 2003;27:269-306.
  52. Ross CA, Margolis RL, Reading SAJ, Pletnikov M, Coyle JT: Neurobiology of schizophrenia. Neuron 2006;52:139-153.
  53. Nordahl TE, Salo R, Leamon M: Neuropsychological effects of chronic methamphetamine use on neurotransmitters and cognition: a review. J Neuropsychiatry Clin Neurosci 2003;15:317-325.
  54. Volkow ND, Chang L, Wang G, Fowler JS, Franceschi D, Sedler M, Gatley SJ, Miller E, Hitzemann R, Ding Y, Logan J: Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 2001;21:9414-9418.

    External Resources

  55. Leonard BE: Fundamentals of Psychopharmacology, ed 3. Chichester, Wiley, 2003.
  56. Featherstone RE, Kapur S, Fletcher PJ: The amphetamine-induced sensitized state as a model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2007;31:1556-1571.
  57. Passie T, Halpern JH, Stichtenoth DO, Emrich HM, Hintzen A: The pharmacology of lysergic acid diethylamide: a review. CNS Neurosci Ther 2008;14:295-314.
  58. Kishi T, Tsunoka T, Ikeda M, Kitajima T, Kawashima K, Okochi T, Okumura T, Yamanouchi Y, Kinoshita Y, Ujike H, Inada T, Yamada M, Uchimura N, Sora I, Iyo M, Ozaki N, Iwata N: Serotonin 1A receptor gene is associated with Japanese methamphetamine-induced psychosis patients. Neuropharmacology 2010;58:452-456.
  59. Steed E, Jones CA, McCreary AC: Serotonergic involvement in methamphetamine-induced locomotor activity: a detailed pharmacological study. Behav Brain Res 2011;220:9-19.
  60. Lysaker PH, Salyers MP: Anxiety symptoms in schizophrenia spectrum disorders: associations with social function, positive and negative symptoms, hope and trauma history. Acta Psychiatr Scand 2007;116:290-298.
  61. Ng E, McGirr A, Wong AHC, Roder JC: Using rodents to model schizophrenia and substance use comorbidity. Neurosci Biobehav Rev 2013;37:896-910.
  62. Trabace L, Zotti M, Colaianna M, Morgese MG, Schiavone S, Tucci P, Wegener G, Harvey BH, Cuomo V: Neurochemical differences in two rat strains exposed to social isolation rearing. Acta Neuropsychiatrica 2012;24:286-295.

    External Resources



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