Impact of altered environment and early postnatal methamphetamine exposure on serotonin levels in the rat hippocampus during adolescence

. 2024 Feb 02 ; 40 (1) : 1. [epub] 20240202

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38308379

Grantová podpora
GAUK144212 Univerzita Karlova v Praze
Cooperatio Neurosciences Univerzita Karlova v Praze
GA 21-30795S Grantová Agentura České Republiky
PharmaBrain CZ.02.1.01/0.0/0.0/16025/0007444 OPVVV

Odkazy

PubMed 38308379
PubMed Central PMC10835812
DOI 10.1186/s42826-024-00192-9
PII: 10.1186/s42826-024-00192-9
Knihovny.cz E-zdroje

BACKGROUND: Methamphetamine (MA) is a highly abused psychostimulant across all age groups including pregnant women. Because developing brain is vulnerable by the action of drugs, or other noxious stimuli, the aim of our study was to examine the effect of early postnatal administration of MA alone or in combination with enriched environment (EE) and/or stress of separate housing, on the levels of serotonin (5HT) in the hippocampus of male rat pups at three stages of adolescence (postnatal day (PND) 28, 35 and 45). MA (5 mg/kg/ml) was administered subcutaneously (sc) to pups (direct administration), or via mothers' milk between PND1 and PND12 (indirect administration). Controls were exposed saline (SA). Pups were exposed to EE and/or to separation from the weaning till the end of the experiment. RESULTS: On PND 28, in sc-treated series, EE significantly increased the muted 5HT in SA pups after separation and restored the pronounced inhibition of 5HT by MA. No beneficial effect of EE was present in pups exposed to combination of MA and separation. 5HT development declined over time; EE, MA and separation had different effects on 5HT relative to adolescence stage. CONCLUSIONS: Present study shows that MA along with environment or housing affect 5HT levels, depending on both the age and the method of application (direct or indirect). These findings extend the knowledge on the effects of MA alone and in combination with different housing conditions on the developing brain and highlight the increased sensitivity to MA during the first few months after birth.

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Cechova B, Slamberova R. Methamphetamine, neurotransmitters and neurodevelopment. Physiol Res. 2021;70(S3):S301–S315. doi: 10.33549/physiolres.934821. PubMed DOI PMC

Jayanthi S, Daiwile AP, Cadet JL. Neurotoxicity of methamphetamine: main effects and mechanisms. Exp Neurol. 2021;344:113795. doi: 10.1016/j.expneurol.2021.113795. PubMed DOI PMC

Bellia F, Suarez A, D'Addario C, Pautassi RM, Fabio MC. Transient serotonin depletion at adolescence, but not at early infancy, reduced subsequent anxiety-like behavior and alcohol intake in female mice. Psychopharmacology. 2021;238(1):215–225. doi: 10.1007/s00213-020-05670-1. PubMed DOI

Park HS, Kim TW, Park SS, Lee SJ. Swimming exercise ameliorates mood disorder and memory impairment by enhancing neurogenesis, serotonin expression, and inhibiting apoptosis in social isolation rats during adolescence. J Exerc Rehabil. 2020;16(2):132–140. doi: 10.12965/jer.2040216.108. PubMed DOI PMC

Ziemens D, Touma C, Rappeneau V. Neurobiological mechanisms modulating emotionality, cognition and reward-related behaviour in high-fat diet-fed rodents. Int J Mol Sci. 2022;23(14):7952. doi: 10.3390/ijms23147952. PubMed DOI PMC

Crews F, He J, Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav. 2007;86(2):189–199. doi: 10.1016/j.pbb.2006.12.001. PubMed DOI

Anton-Toro LF, Bruna R, Del Cerro-Leon A, Shpakivska D, Mateos-Gordo P, Porras-Truque C, et al. Electrophysiological resting-state hyperconnectivity and poorer behavioural regulation as predisposing profiles of adolescent binge drinking. Addict Biol. 2022;27(4):e13199. doi: 10.1111/adb.13199. PubMed DOI PMC

Semple BD, Blomgren K, Gimlin K, Ferriero DM, Noble-Haeusslein LJ. Brain development in rodents and humans: identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol. 2013;106–107:1–16. doi: 10.1016/j.pneurobio.2013.04.001. PubMed DOI PMC

Jacob FD, Habas PA, Kim K, Corbett-Detig J, Xu D, Studholme C, et al. Fetal hippocampal development: analysis by magnetic resonance imaging volumetry. Pediatr Res. 2011;69(5 Pt 1):425–429. doi: 10.1203/PDR.0b013e318211dd7f. PubMed DOI PMC

Kim EJ, Pellman B, Kim JJ. Stress effects on the hippocampus: a critical review. Learn Mem. 2015;22(9):411–416. doi: 10.1101/lm.037291.114. PubMed DOI PMC

Trakhtenberg EF, Goldberg JL. The role of serotonin in axon and dendrite growth. Int Rev Neurobiol. 2012;106:105–126. doi: 10.1016/B978-0-12-407178-0.00005-3. PubMed DOI

Rice D, Barone S., Jr Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000;108(Suppl 3):511–533. doi: 10.1289/ehp.00108s3511. PubMed DOI PMC

Petrikova-Hrebickova I, Sevcikova M, Slamberova R. The impact of neonatal methamphetamine on spatial learning and memory in adult female rats. Front Behav Neurosci. 2021;15:629585. doi: 10.3389/fnbeh.2021.629585. PubMed DOI PMC

Slamberova R. Review of long-term consequences of maternal methamphetamine exposure. Physiol Res. 2019;68(Suppl 3):S219–S231. doi: 10.33549/physiolres.934360. PubMed DOI

Zhang Y, Gong F, Liu P, He Y, Wang H. Effects of prenatal methamphetamine exposure on birth outcomes, brain structure, and neurodevelopmental outcomes. Dev Neurosci. 2021;43(5):271–280. doi: 10.1159/000517753. PubMed DOI

Slamberova R, Pometlova M, Schutova B, Hruba L, Macuchova E, Nova E, et al. Do prenatally methamphetamine-exposed adult male rats display general predisposition to drug abuse in the conditioned place preference test? Physiol Res. 2012;61(Suppl 2):S129–S138. doi: 10.33549/physiolres.932391. PubMed DOI

Yamamotova A, Slamberova R. Behavioral and antinociceptive effects of different psychostimulant drugs in prenatally methamphetamine-exposed rats. Physiol Res. 2012;61(Suppl 2):S139–S147. doi: 10.33549/physiolres.932428. PubMed DOI

Bernaskova K, Matejovska I, Slamberova R. Postnatal challenge dose of methamphetamine amplifies anticonvulsant effects of prenatal methamphetamine exposure on epileptiform activity induced by electrical stimulation in adult male rats. Exp Neurol. 2011;229(2):282–287. doi: 10.1016/j.expneurol.2011.02.011. PubMed DOI

Slamberova R, Pometlova M, Macuchova E, Nohejlova K, Stuchlik A, Vales K. Do the effects of prenatal exposure and acute treatment of methamphetamine on anxiety vary depending on the animal model used? Behav Brain Res. 2015;292:361–369. doi: 10.1016/j.bbr.2015.07.001. PubMed DOI

Rokyta R, Yamamotova A, Slamberova R, Franek M, Vaculin S, Hruba L, et al. Prenatal and perinatal factors influencing nociception, addiction and behavior during ontogenetic development. Physiol Res. 2008;57(Suppl 3):S79–S88. doi: 10.33549/physiolres.931602. PubMed DOI

Spear LP. Assessment of adolescent neurotoxicity: rationale and methodological considerations. Neurotoxicol Teratol. 2007;29(1):1–9. doi: 10.1016/j.ntt.2006.11.006. PubMed DOI PMC

Bayne K. Environmental enrichment and mouse models: current perspectives. Anim Model Exp Med. 2018;1(2):82–90. doi: 10.1002/ame2.12015. PubMed DOI PMC

Zentall TR. Effect of environmental enrichment on the brain and on learning and cognition by animals. Animals (Basel) 2021;11(4):973. doi: 10.3390/ani11040973. PubMed DOI PMC

Mahar I, Bambico FR, Mechawar N, Nobrega JN. Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects. Neurosci Biobehav Rev. 2014;38:173–192. doi: 10.1016/j.neubiorev.2013.11.009. PubMed DOI

Yao X, Yang C, Wang C, Li H, Zhao J, Kang X, et al. High-fat diet consumption in adolescence induces emotional behavior alterations and hippocampal neurogenesis deficits accompanied by excessive microglial activation. Int J Mol Sci. 2022;23(15):8316. doi: 10.3390/ijms23158316. PubMed DOI PMC

Orben A, Tomova L, Blakemore SJ. The effects of social deprivation on adolescent development and mental health. Lancet Child Adolesc Health. 2020;4(8):634–640. doi: 10.1016/S2352-4642(20)30186-3. PubMed DOI PMC

Nelson CA, 3rd, Gabard-Durnam LJ. Early adversity and critical periods: neurodevelopmental consequences of violating the expectable environment. Trends Neurosci. 2020;43(3):133–143. doi: 10.1016/j.tins.2020.01.002. PubMed DOI PMC

Luikinga SJ, Kim JH, Perry CJ. Developmental perspectives on methamphetamine abuse: exploring adolescent vulnerabilities on brain and behavior. Prog Neuropsychopharmacol Biol Psychiatry. 2018;87(Pt A):78–84. doi: 10.1016/j.pnpbp.2017.11.010. PubMed DOI

Sevcikova M, Petrikova I, Slamberova R. Methamphetamine exposure during the first, but not the second half of prenatal development, affects social play behavior. Physiol Res. 2020;69(2):319–330. doi: 10.33549/physiolres.934230. PubMed DOI PMC

Slamberova R, Nohejlova K, Ochozkova A, Mihalcikova L. What is the role of subcutaneous single injections on the behavior of adult male rats exposed to drugs? Physiol Res. 2018;67(Suppl 4):S665–S672. doi: 10.33549/physiolres.934053. PubMed DOI

Hruba L, Schutova B, Slamberova R. Sex differences in anxiety-like behavior and locomotor activity following prenatal and postnatal methamphetamine exposure in adult rats. Physiol Behav. 2012;105(2):364–370. doi: 10.1016/j.physbeh.2011.08.016. PubMed DOI

Slamberova R, Mikulecka A, Pometlova M, Schutova B, Hruba L, Deykun K. Sex differences in social interaction of methamphetamine-treated rats. Behav Pharmacol. 2011;22(7):617–623. doi: 10.1097/FBP.0b013e32834afea4. PubMed DOI

Schaefer TL, Skelton MR, Herring NR, Gudelsky GA, Vorhees CV, Williams MT. Short- and long-term effects of (+)-methamphetamine and (+/-)-3,4-methylenedioxymethamphetamine on monoamine and corticosterone levels in the neonatal rat following multiple days of treatment. J Neurochem. 2008;104(6):1674–1685. doi: 10.1111/j.1471-4159.2007.05112.x. PubMed DOI PMC

Schaefer TL, Grace CE, Gudelsky GA, Vorhees CV, Williams MT. Effects on plasma corticosterone levels and brain serotonin from interference with methamphetamine-induced corticosterone release in neonatal rats. Stress. 2010;13(6):469–480. doi: 10.3109/10253891003786407. PubMed DOI

Vorhees CV, Ahrens KG, Acuff-Smith KD, Schilling MA, Fisher JE. Methamphetamine exposure during early postnatal development in rats: II. Hypoactivity and altered responses to pharmacological challenge. Psychopharmacology (Berl). 1994;114(3):402–8. PubMed

Vorhees CV, Ahrens KG, Acuff-Smith KD, Schilling MA, Fisher JE. Methamphetamine exposure during early postnatal development in rats: I. Acoustic startle augmentation and spatial learning deficits. Psychopharmacology (Berl). 1994;114(3):392–401. PubMed

Schenk S, Highgate Q. Methylenedioxymethamphetamine (MDMA): serotonergic and dopaminergic mechanisms related to its use and misuse. J Neurochem. 2021;157(5):1714–1724. doi: 10.1111/jnc.15348. PubMed DOI

Buck JM, Morris AS, Weber SJ, Raber J, Siegel JA. Effects of adolescent methamphetamine and nicotine exposure on behavioral performance and MAP-2 immunoreactivity in the nucleus accumbens of adolescent mice. Behav Brain Res. 2017;323:78–85. doi: 10.1016/j.bbr.2017.01.010. PubMed DOI PMC

Biggio F, Mostallino MC, Talani G, Locci V, Mostallino R, Calandra G, et al. Social enrichment reverses the isolation-induced deficits of neuronal plasticity in the hippocampus of male rats. Neuropharmacology. 2019;151:45–54. doi: 10.1016/j.neuropharm.2019.03.030. PubMed DOI

Fosnocht AQ, Lucerne KE, Ellis AS, Olimpo NA, Briand LA. Adolescent social isolation increases cocaine seeking in male and female mice. Behav Brain Res. 2019;359:589–596. doi: 10.1016/j.bbr.2018.10.007. PubMed DOI PMC

Ohline SM, Abraham WC. Environmental enrichment effects on synaptic and cellular physiology of hippocampal neurons. Neuropharmacology. 2019;145(Pt A):3–12. doi: 10.1016/j.neuropharm.2018.04.007. PubMed DOI

Galaj E, Barrera ED, Ranaldi R. Therapeutic efficacy of environmental enrichment for substance use disorders. Pharmacol Biochem Behav. 2020;188:172829. doi: 10.1016/j.pbb.2019.172829. PubMed DOI PMC

Sbrini G, Brivio P, Bosch K, Homberg JR, Calabrese F. Enrichment environment positively influences depression- and anxiety-like behavior in serotonin transporter knockout rats through the modulation of neuroplasticity, spine, and GABAergic markers. Genes (Basel) 2020;11(11):1248. doi: 10.3390/genes11111248. PubMed DOI PMC

Kempermann G. Environmental enrichment, new neurons and the neurobiology of individuality. Nat Rev Neurosci. 2019;20(4):235–245. doi: 10.1038/s41583-019-0120-x. PubMed DOI

Gutierrez A, Jablonski SA, Amos-Kroohs RM, Barnes AC, Williams MT, Vorhees CV. Effects of housing on methamphetamine-induced neurotoxicity and spatial learning and memory. ACS Chem Neurosci. 2017;8(7):1479–1489. doi: 10.1021/acschemneuro.6b00419. PubMed DOI

Arrant AE, Jemal H, Kuhn CM. Adolescent male rats are less sensitive than adults to the anxiogenic and serotonin-releasing effects of fenfluramine. Neuropharmacology. 2013;65:213–222. doi: 10.1016/j.neuropharm.2012.10.010. PubMed DOI PMC

Hrebickova I, Sevcikova M, Macuchova E, Slamberova R. How methamphetamine exposure during different neurodevelopmental stages affects social behavior of adult rats? Physiol Behav. 2017;179:391–400. doi: 10.1016/j.physbeh.2017.07.009. PubMed DOI

Hrebickova I, Sevcikova M, Nohejlova K, Slamberova R. Does effect from developmental methamphetamine exposure on spatial learning and memory depend on stage of neuroontogeny? Physiol Res. 2016;65(Suppl 5):S577–S589. doi: 10.33549/physiolres.933534. PubMed DOI

Melega WP, Cho AK, Harvey D, Lacan G. Methamphetamine blood concentrations in human abusers: application to pharmacokinetic modeling. Synapse. 2007;61(4):216–220. doi: 10.1002/syn.20365. PubMed DOI

Cho AK, Melega WP, Kuczenski R, Segal DS. Relevance of pharmacokinetic parameters in animal models of methamphetamine abuse. Synapse. 2001;39(2):161–166. doi: 10.1002/1098-2396(200102)39:2<161::AID-SYN7>3.0.CO;2-E. PubMed DOI

Sevcikova M, Hrebickova I, Macuchova E, Slamberova R. The influence of methamphetamine on maternal behavior and development of the pups during the neonatal period. Int J Dev Neurosci. 2017;59:37–46. doi: 10.1016/j.ijdevneu.2017.03.005. PubMed DOI

Liu D, Diorio J, Day JC, Francis DD, Meaney MJ. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000;3(8):799–806. doi: 10.1038/77702. PubMed DOI

Sbrini G, Hanswijk SI, Brivio P, Middelman A, Bader M, Fumagalli F, et al. Peripheral serotonin deficiency affects anxiety-like behavior and the molecular response to an acute challenge in rats. Int J Mol Sci. 2022;23(9):4941. doi: 10.3390/ijms23094941. PubMed DOI PMC

Albert PR, Vahid-Ansari F, Luckhart C. Serotonin-prefrontal cortical circuitry in anxiety and depression phenotypes: pivotal role of pre- and post-synaptic 5-HT1A receptor expression. Front Behav Neurosci. 2014;8:199. doi: 10.3389/fnbeh.2014.00199. PubMed DOI PMC

Blazevic S, Colic L, Culig L, Hranilovic D. Anxiety-like behavior and cognitive flexibility in adult rats perinatally exposed to increased serotonin concentrations. Behav Brain Res. 2012;230(1):175–181. doi: 10.1016/j.bbr.2012.02.001. PubMed DOI

Mosienko V, Bert B, Beis D, Matthes S, Fink H, Bader M, et al. Exaggerated aggression and decreased anxiety in mice deficient in brain serotonin. Transl Psychiatry. 2012;2(5):e122. doi: 10.1038/tp.2012.44. PubMed DOI PMC

Holubova-Kroupova A, Slamberova R. Perinatal stress and methamphetamine exposure decreases anxiety-like behavior in adult male rats. Front Behav Neurosci. 2021;15:648780. doi: 10.3389/fnbeh.2021.648780. PubMed DOI PMC

Seiden LS, Commins DL, Vosmer G, Axt K, Marek G. Neurotoxicity in dopamine and 5-hydroxytryptamine terminal fields: a regional analysis in nigrostriatal and mesolimbic projections. Ann N Y Acad Sci. 1988;537:161–172. doi: 10.1111/j.1749-6632.1988.tb42104.x. PubMed DOI

Buening MK, Gibb JW. Influence of methamphetamine and neuroleptic drugs on tyrosine hydroxylase activity. Eur J Pharmacol. 1974;26(1):30–34. doi: 10.1016/0014-2999(74)90070-3. PubMed DOI

Hotchkiss AJ, Gibb JW. Long-term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J Pharmacol Exp Ther. 1980;214(2):257–262. PubMed

Holubova A, Stofkova A, Jurcovicova J, Slamberova R. The effect of neonatal maternal stress on plasma levels of adrenocorticotropic hormone, corticosterone, leptin, and ghrelin in adult male rats exposed to acute heterotypic stressor. Physiol Res. 2016;65(Suppl 5):S557–S566. doi: 10.33549/physiolres.933530. PubMed DOI

Holubova A, Ponist S, Jurcovicova J, Slamberova R. Different oxytocin responses to acute methamphetamine treatment in juvenile female rats perinatally exposed to stress and/or methamphetamine administration. Front Physiol. 2019;10:305. doi: 10.3389/fphys.2019.00305. PubMed DOI PMC

Holubova A, Lukaskova I, Tomasova N, Suhajdova M, Slamberova R. Early postnatal stress impairs cognitive functions of male rats persisting until adulthood. Front Behav Neurosci. 2018;12:176. doi: 10.3389/fnbeh.2018.00176. PubMed DOI PMC

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