Environmental Enrichment Components Required to Reduce Methamphetamine-Induced Behavioral Sensitization in Mice: Examination of Behaviors and Neural Substrates

Overview

Journal J Clin Med

Specialty General Medicine

Date 2022 Jun 10

PMID 35683439

Authors

Cai-N Cheng

Shaw-Jye Wu

Andrew Chih Wei Huang

Affiliations

Soon will be listed here.

Abstract

Environmental enrichment (EE) involves the presentation of various sensory, physical, social, and cognitive stimuli in order to alter neural activity in specific brain areas, which can ameliorate methamphetamine (MAMPH)-induced behavioral sensitization and comorbid anxiety symptoms. No previous studies have comprehensively examined which EE components are critical for effectively reducing MAMPH-induced behavioral sensitization and anxiety. This study examined different housing conditions, including standard housing (SH, No EE), standard EE (STEE), physical EE (PEE), cognitive EE (CEE), and social EE (SEE). In the beginning, mice were randomly assigned to the different combinations of housing conditions and injections, consisting of No EE/Saline, No EE/MAMPH, STEE/MAMPH, PEE/MAMPH, CEE/MAMPH, and SEE/MAMPH groups. Then, the mice received intraperitoneal injections of 1 mg/kg MAMPH or normal saline daily for 7 days, followed by a final injection of 0.5 mg/kg MAMPH or normal saline. After behavioral tests, all mice were examined for c-Fos immunohistochemical staining. The results showed that MAMPH induced behavioral sensitization as measured by distance traveled. MAMPH appeared to induce lowered anxiety responses and severe hyperactivity. All EE conditions did not affect MAMPH-induced lowered anxiety behaviors. STEE was likely more effective for reducing MAMPH-induced behavioral sensitization than PEE, CEE, and SEE. The c-Fos expression analysis showed that the medial prefrontal cortex (i.e., cingulate cortex 1 (Cg1), prelimbic cortex (PrL), and infralimbic cortex (IL)), nucleus accumbens (NAc), basolateral amygdala (BLA), ventral tegmental area (VTA), caudate-putamen (CPu), and hippocampus (i.e., CA1, CA3, and dentate gyrus (DG)) contributed to MAMPH-induced behavioral sensitization. The Cg1, IL, NAc, BLA, VTA, CPu, CA3, and DG also mediated STEE reductions in MAMPH-induced behavioral sensitization. This study indicates that all components of EE are crucial for ameliorating MAMPH-induced behavioral sensitization, as no individual EE component was able to effectively reduce MAMPH-induced behavioral sensitization. The present findings provide insight into the development of non-pharmacological interventions for reducing MAMPH-induced behavioral sensitization.

Citing Articles

Different Doses of Methamphetamine Are Needed to Produce Locomotor or Blood Pressure Sensitization in Mice.

Busceti C, Bucci D, De Lucia M, Ferrucci M, Scioli M, Carrizzo A Life (Basel). 2024; 14(6).

PMID: 38929706 PMC: 11205198. DOI: 10.3390/life14060723.

The systemic effects of the enriched environment on the conditioned fear reaction.

Grigoryan G Front Behav Neurosci. 2023; 17:1227575.

PMID: 37674611 PMC: 10477375. DOI: 10.3389/fnbeh.2023.1227575.

References

Herbert C, Hughes R . A comparison of 1-benzylpiperazine and methamphetamine in their acute effects on anxiety-related behavior of hooded rats. Pharmacol Biochem Behav. 2008; 92(2):243-50. DOI: 10.1016/j.pbb.2008.12.003. View

Cao M, Pu T, Wang L, Marshall C, He H, Hu G . Early enriched physical environment reverses impairments of the hippocampus, but not medial prefrontal cortex, of socially-isolated mice. Brain Behav Immun. 2017; 64():232-243. DOI: 10.1016/j.bbi.2017.04.009. View

Weiss F, Ciccocioppo R, Parsons L, Katner S, Liu X, Zorrilla E . Compulsive drug-seeking behavior and relapse. Neuroadaptation, stress, and conditioning factors. Ann N Y Acad Sci. 2001; 937:1-26. DOI: 10.1111/j.1749-6632.2001.tb03556.x. View

Robinson T, Becker J . Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res. 1986; 396(2):157-98. DOI: 10.1016/s0006-8993(86)80193-7. View

Walsh R, Cummins R . The Open-Field Test: a critical review. Psychol Bull. 1976; 83(3):482-504. View

Bardo M, Bowling S, Rowlett J, Manderscheid P, Buxton S, Dwoskin L . Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine. Pharmacol Biochem Behav. 1995; 51(2-3):397-405. DOI: 10.1016/0091-3057(94)00413-d. View

Thiel K, Pentkowski N, Peartree N, Painter M, Neisewander J . Environmental living conditions introduced during forced abstinence alter cocaine-seeking behavior and Fos protein expression. Neuroscience. 2010; 171(4):1187-96. PMC: 3010380. DOI: 10.1016/j.neuroscience.2010.10.001. View

Kentner A, Takeuchi A, James J, Miki T, Seino S, Hayley S . The effects of rewarding ventral tegmental area stimulation and environmental enrichment on lipopolysaccharide-induced sickness behavior and cytokine expression in female rats. Brain Res. 2008; 1217:50-61. DOI: 10.1016/j.brainres.2008.04.041. View

Cain M, Mersmann M, Gill M, Pittenger S . Dose-dependent effects of differential rearing on amphetamine-induced hyperactivity. Behav Pharmacol. 2012; 23(8):744-53. DOI: 10.1097/FBP.0b013e32835a38ec. View

10.

Marques J, Olsson I . The effect of preweaning and postweaning housing on the behaviour of the laboratory mouse (Mus musculus). Lab Anim. 2007; 41(1):92-102. DOI: 10.1258/002367707779399482. View

11.

Garcia E, Haddon T, Saucier D, Cain M . Differential housing and novelty response: Protection and risk from locomotor sensitization. Pharmacol Biochem Behav. 2017; 154:20-30. PMC: 5370571. DOI: 10.1016/j.pbb.2017.01.004. View

12.

Nobre M . Environmental enrichment may protect against neural and behavioural damage caused by withdrawal from chronic alcohol intake. Int J Dev Neurosci. 2016; 55:15-27. DOI: 10.1016/j.ijdevneu.2016.09.003. View

13.

Redolat R, Mesa-Gresa P, Sampedro-Piquero P, Cutuli D . Editorial: Environmental Enrichment as a Treatment? Epigenetic Mechanisms, Challenges and Limitations. Front Pharmacol. 2021; 12:658970. PMC: 8103319. DOI: 10.3389/fphar.2021.658970. View

14.

El Rawas R, Thiriet N, Lardeux V, Jaber M, Solinas M . Environmental enrichment decreases the rewarding but not the activating effects of heroin. Psychopharmacology (Berl). 2008; 203(3):561-70. DOI: 10.1007/s00213-008-1402-6. View

15.

Wang Y, Wang C, Lee C, Huang A . Effects of single and group housing conditions and alterations in social and physical contexts on amphetamine-induced behavioral sensitization in rats. Neurosci Lett. 2010; 486(1):34-7. DOI: 10.1016/j.neulet.2010.09.039. View

16.

Nicolas C, Hofford R, Dugast E, Lardeux V, Belujon P, Solinas M . Prevention of relapse to methamphetamine self-administration by environmental enrichment: involvement of glucocorticoid receptors. Psychopharmacology (Berl). 2021; 239(4):1009-1018. DOI: 10.1007/s00213-021-05770-6. View

17.

Paez-Martinez N, Pellicer F, Gonzalez-Trujano M, Cruz-Lopez B . Environmental enrichment reduces behavioural sensitization in mice previously exposed to toluene: The role of D1 receptors. Behav Brain Res. 2020; 390:112624. DOI: 10.1016/j.bbr.2020.112624. View

18.

Decker S, Grider G, Cobb M, Li X, Huff M, El-Mallakh R . Open field is more sensitive than automated activity monitor in documenting ouabain-induced hyperlocomotion in the development of an animal model for bipolar illness. Prog Neuropsychopharmacol Biol Psychiatry. 2000; 24(3):455-62. DOI: 10.1016/s0278-5846(99)00111-6. View

19.

Aghaie C, Hausknecht K, Wang R, Dezfuli P, Haj-Dahmane S, Kane C . Prenatal Ethanol Exposure and Postnatal Environmental Intervention Alter Dopaminergic Neuron and Microglia Morphology in the Ventral Tegmental Area During Adulthood. Alcohol Clin Exp Res. 2019; 44(2):435-444. PMC: 7153307. DOI: 10.1111/acer.14275. View

20.

Gehrke B, Cass W, Bardo M . Monoamine-depleting doses of methamphetamine in enriched and isolated rats: consequences for subsequent methamphetamine-induced hyperactivity and reward. Behav Pharmacol. 2006; 17(5-6):499-508. DOI: 10.1097/00008877-200609000-00016. View