The reinstatement of the expression phase of morphine-induced conditioned place preference in male Wistar rats under ventral tegmental area stimulation and brief inactivation

Mozhgan Ghobadi Pour , Hojjatollah Alaei

Abstract


Background and purpose: Previous research has found that the electrical stimulation of the ventral tegmental area (VTA) is involved in drug-dependent behaviors and plays a role in reward-seeking. However, the mechanisms remain unknown, especially the effect of electrical stimulation on this area. Therefore, this study aimed to investigate how the electrical stimulation and the temporary inactivation of VTA affect the morphine-dependent behavior in male rats.

Experimental approach: The adult Wistar male rats were anesthetized with ketamine and xylazine. The stimulation electrode (unilaterally) and the microinjection cannula (bilaterally) were implanted into the VTA, stereotaxically. Then, the rats underwent three-day of repeated conditioning with subcutaneous morphine                 (0.5 or 5 mg/kg) injections, in the conditioned place preference apparatus, followed by four-day forced abstinence, which altered their conditioning response to a morphine (0.5 mg/kg) priming dose on the ninth day. On that day, rats were given high- or low-intensity electrical stimulation or reversible inactivation with lidocaine (0.5 μL/site) in the VTA.

Findings/Results: Results showed that the electrical stimulation of the VTA with the high intensity                         (150 μA/rat), had a minimal effect on the expression of morphine-induced place conditioning in rats treated with a high dose (5 mg/kg) of morphine. However, the reversible inactivation of the VTA with lidocaine       greatly increased place preference in rats treated with a low dose (0.5 mg/kg) of morphine. Additionally, the reinstatement of 0.5 mg/kg morphine-treated rats was observed after lidocaine infusion into the VTA.

Conclusion and implications: These results suggest that VTA electrical stimulation suppresses neuronal activation, but the priming dose causes reinstatement. The VTA may be a potential target for deep brain stimulation-based treatment of intractable disorders induced by substance abuse.


Keywords


Deep brain stimulation; Dopamine; Drug addiction; Rat; Ventral tegmental area.

Full Text:

PDF

References


Allichon MC, Ortiz V, Pousinha P, Andrianarivelo A, Petitbon A, Heck N, et al. Cell-type-specific adaptions in striatal medium-sized spiny neurons and their roles in behavioral responses to drugs of abuse. Front Synaptic Neurosci. 2021;13:799274,1-17. DOI: 10.3389/fnsyn.2021.799274.

Ryan SA. Substance abuse in pregnancy. Clin Obstet Gynecol. 2019;62(1):112-117. DOI: 10.1097/GRF.0000000000000427.

Veeneman MMJ, Boleij H, Broekhoven MH, Snoeren EMS, Guitart Masip M, Cousijn J, et al. Dissociable roles of mGlu5 and dopamine receptors in the rewarding and sensitizing properties of morphine and cocaine. Psychopharmacology (Berl). 2011;214(4):863-876. DOI: 10.1007/s00213-010-2095-1.

Motahari AA, Sahraei H, Meftahi GH. Role of nitric oxide on dopamine release and morphine-dependency. Basic Clin Neurosci. 2016;7(4): 283-290. DOI: 10.15412/J.BCN.03070401.

Gordon-Fennell A, Stuber GD. Illuminating subcortical GABAergic and glutamatergic circuits for reward and aversion. Neuropharmacology. 2021;198:108725,1-42. DOI: 10.1016/j.neuropharm.2021.108725.

Listos J, Łupina M, Talarek S, Mazur A, Orzelska-Górka J, Kotlińska J. The mechanisms involved in morphine addiction: an overview. Int J Mol Sci. 2019;20(17):4302,1-23. DOI: 10.3390/ijms20174302.

Kuhn BN, Kalivas PW, Bobadilla AC. Understanding addiction using animal models. Front. Behav. Neurosci. 2019;13:262,1-24. DOI: 10.3389/fnbeh.2019.00262

Polter AM, Barcomb K, Tsuda AC, Kauer JA. Synaptic function and plasticity in identified inhibitory inputs onto VTA dopamine neurons. Eur J Neurosci. 2018;47(10):1208-1218. DOI: 10.1111/ejn.13879.

Jokar Z, Khatamsaz S, Alaei H, Shariati M. Effect of electrical stimulation of central nucleus of the amygdala on morphine conditioned place preference in male rats. Iran J Basic Med Sci.. 2022;25(5):604-610. DOI: 10.22038/IJBMS.2022.62133.13751.

Moaddab M, Haghparast A, Hassanpour-Ezatti M. Effects of reversible inactivation of the ventral tegmental area on the acquisition and expression of morphine-induced conditioned place preference in the rat. Behav Brain Res. 2009;198(2):466-471. DOI: 10.1016/j.bbr.2008.11.030.

Sun GL, Song ZJ, Peng XH, Chen PP, Song Y, Qin X, et al. Projection-specific dopamine neurons in the ventral tegmental area participated in morphine-induced hyperalgesia and anti-nociceptive tolerance in male mice. J Psychopharmacol. 2021;35(5):591-605. DOI: 10.1177/0269881120985183.

Ji NN, Kang J, Hua R, Zhang YM. Involvement of dopamine system in the regulation of the brain corticotropin-releasing hormone in paraventricular nucleus in a rat model of chronic visceral pain. Neurol Res. 2018;40(8):650-657. DOI: 10.1080/01616412.2018.1460702.

Mortazaei S, Sahraei H, Bahari Z, Meftahi GH, Pirzad Jahromi G, Hatef B. Ventral tegmental area inactivation alters hormonal, metabolic, and locomotor responses to inescapable stress. Arch Physiol Biochem. 2019;125(4):293-301. DOI: 10.1080/13813455.2018.1455711.

Chalabi-Yani D, Sahraei H, Meftahi GH, Hosseini SB, Sadeghi-Gharajehdaghi S, Ali Beig H, et al. Effect of transient inactivation of ventral tegmental area on the expression and acquisition of nicotine-induced conditioned place preference in rats. Iran Biomed J. 2015;19(4):214-219. DOI: 10.6091/ibj.1402.2015.

Rogers TD, Dickson PE, McKimm E, Heck DH, Goldowitz D, Blaha CD, et al. Reorganization of circuits underlying cerebellar modulation of prefrontal cortical dopamine in mouse models of autism spectrum disorder. Cerebellum. 2013;12(4):547-556. DOI: 10.1007/s12311-013-0462-2

Aum DJ, Tierney TS. Deep brain stimulation: foundations and future trends. Front Biosci (Landmark Ed). 2018;23(1):162-182. DOI: 10.2741/4586

Fattahi M, Ashabi G, Karimian SM, Riahi E. Preventing morphine reinforcement with high‐frequency deep brain stimulation of the lateral hypothalamic area. Addict Biol. 2019;24(4):685-695. DOI: 10.1111/adb.12634.

Yan N, Chen N, Zhu H, Zhang J, Sim M, Ma Y, et al. High-frequency stimulation of nucleus accumbens changes in dopaminergic reward circuit. PloS one. 2013;8(11):e79318,1-8. DOI: 10.1371/journal.pone.0079318.

Wang TR, Moosa S, Dallapiazza RF, Elias WJ, Lynch WJ. Deep brain stimulation for the treatment of drug addiction. Neurosurg Focus 2018;45(2):E11,1-19. DOI: 10.3171/2018.5.FOCUS18163.

Fakhrieh‐Asl G, Sadr SS, Karimian SM, Riahi E. Deep brain stimulation of the orbitofrontal cortex prevents the development and reinstatement of morphine place preference. Addict Biol. 2020;25(4):e12780,1-12. DOI: 10.1111/adb.12780.

Albus U. Guide for the Care and Use of Laboratory Animals (8th ed.). Laboratory Animals. 2012;46(3):267-268. DOI: 10.1258/la.2012.150312.20. Alaei H, Ghobadi Pour M. Stimulation and transient inactivation of ventral tegmental area modify reinstatement of acquisition phase of morphine-induced conditioned place preference in male rats. Brain Res Bull. 2021;176:130-141. DOI: 10.1016/j.brainresbull.2021.08.014.

Paxinos G, Watson C. The rat brain in stereotaxic coordinates: 6th edition. USA: Elsevier; 2006. P. 112-130.

Alaei H, Ghobadi Pour M. Stimulation and transient inactivation of ventral tegmental area modify reinstatement of acquisition phase of morphine-induced conditioned place preference in male rats. Brain Res Bull. 2021;176:130-141. DOI: 10.1016/j.brainresbull.2021.08.014.

Kunori N, Kajiwara R, Takashima I. Voltage-sensitive dye imaging of primary motor cortex activity produced by ventral tegmental area stimulation. J Neurosci. 2014;34(26):8894-8903. DOI: 10.1523/JNEUROSCI.5286-13.2014.

Majkutewicz I, Cecot T, Jerzemowska G, Myślińska D, Plucińska K, Trojniar W, et al. Lesion of the ventral tegmental area amplifies stimulation-induced Fos expression in the rat brain. Brain Res. 2010;1320:95-105. DOI: 10.1016/j.brainres.2010.01.009.

Ghavipanjeh GR, Pourshanazari AA, Alaei H, Karimi S, Nejad MA. Effects of temporary inactivation and electrical stimulation of the dorsal raphe nucleus on morphine-induced conditioned place preference. Malays J Med Sci. 2015;22(2):33-40. PMID: 26023293.

Narita M, Matsushima Y, Niikura K, Narita M, Takagi S, Nakahara K, et al. Implication of dopaminergic projection from the ventral tegmental area to the anterior cingulate cortex in μ‐opioid‐induced place preference. Addict Biol. 2010;15(4):434-447. DOI: 10.1111/j.1369- 1600.2010.00249.x.

Gretenkord S, Olthof BMJ, Stylianou M, Rees A, Gartside SE, LeBeau FEN. Electrical stimulation of the ventral tegmental area evokes sleep‐like state transitions under urethane anaesthesia in the rat medial prefrontal cortex via dopamine D1‐like receptors. Eur J Neurosci. 2020;52(2):2915-2930. DOI: 10.1111/ejn.14665.

Amohashemi E, Alaei H, Reisi P. Effects of GABAB receptor blockade on lateral habenula glutamatergic neuron activity following morphine injection in the rat: an electrophysiological study. Res Pharm Sci. 2023;18(1):16-23. DOI: 10.4103/1735-5362.363592.

Ahmadian SM, Alaei H, Ghahremani P. An Assessment between D1 receptor agonist and D2 receptor antagonist into the ventral tegmental area on conditioned place preference and locomotor activity. Adv Biomed Res. 2019;8:72,1-8. DOI: 10.4103/abr.abr-82-19.

Sahraei H, Zarei F, Eidi A, Oryan S, Shams J, Khoshbaten A, et al. The role of nitric oxide within the nucleus accumbens on the acquisition and expression of morphine-induced place preference in morphine sensitized rats. Eur J Pharmacol 2007;556(1-3):99-106. DOI: 10.1016/j.ejphar.2006.10.044.

Listos J, Talarek S, Listos P, Orzelska J, Łupina M, Fidecka S. Effects of the adenosinergic system on the expression and acquisition of sensitization to conditioned place preference in morphine-conditioned rats. Naunyn Schmiedebergs Arch Pharmacol. 2016;389(2):233-241. DOI: 10.1007/s00210-015-1190-6.

Yang C, Qiu Y, Hu X, Chen J, Wu Y, Wu X. The Effect of High-Frequency Electrical Stimulation of Bilateral Nucleus Accumbens on the Behavior of Morphine-Induced Conditioned Place Preference Rats at Extinction and Reinstatement Phases. Evid Based Complement Alternat Med 2020;2020:8232809,1-8. DOI: 10.1155/2020/8232809.

Jokar Z, Khatamsaz S, Alaei H, Shariati M. The electrical stimulation of the central nucleus of the amygdala in combination with dopamine receptor antagonist reduces the acquisition phase of morphine-induced conditioned place preference in male rat. Res Pharm Sci. 2023;18(4):430-438. DOI: 10.4103/1735-5362.378089.

Koob GF, Volkow ND. Neurocircuitry of Addiction. Neuropsychopharmacology. 2010;35(1):217-238. DOI: 10.1038/npp.2009.110.

Berridge KC, Robinson TE. Liking, wanting, and the incentive-sensitization theory of addiction. Am Psychol. 2016;71(8):670-679. DOI: 10.1037/amp0000059.

Vigano D, Rubino T, Di Chiara G, Ascari I, Massi P, Parolaro D. Mμ opioid receptor signaling in morphine sensitization. Neuroscience. 2003;117(4):921-929. DOI: 10.1016/s0306-4522(02)00825-4.

Reisi Z, Bani-Ardalan M, Zarepour L, Haghparast A. Involvement of D1/D2 dopamine receptors within the nucleus accumbens and ventral tegmental area in the development of sensitization to antinociceptive effect of morphine. Pharmacol Biochem Behav. 2014;118:16-21. DOI: 10.1016/j.pbb.2013.12.023.

Mahmoudi D, Assar N, Mousavi Z, Katebi SN, Azizi P, Haghparast A. The orexin receptors in the ventral tegmental area are involved in the development of sensitization to expression of morphine-induced preference in rats. Behav Pharmacol. 2020;31(8):759-767. DOI: 874 10.1097/FBP.0000000000000587.

Azizi P, Haghparast A, Hassanpour-Ezatti M. Effects of CB1 receptor antagonist within the nucleus accumbens on the acquisition and expression of morphine-induced conditioned place preference in morphine-sensitized rats. Behav Brain Res. 2009;197(1):119-124. DOI: 10.1016/j.bbr.2008.08.009.

Shi XD, Wang GB, Ma YY, Ren W, Luo F, Cui CL, et al. Repeated peripheral electrical stimulations suppress both morphine-induced CPP and reinstatement of extinguished CPP in rats: accelerated expression of PPE and PPD mRNA in NAc implicated. Brain Res Mol Brain Res. 2004;130(1-2):124-133. DOI: 10.1016/j.molbrainres.2004.07.016.

Brocka M, Helbing C, Vincenz D, Scherf T, Montag D, Goldschmidt J, et al. Contributions of dopaminergic and non-dopaminergic neurons to VTA-stimulation induced neurovascular responses in brain reward circuits. Neuroimage. 2018;177:88-97. DOI: 10.1016/j.neuroimage.2018.04.059.

Lepack AE, Werner CT, Stewart AF, Fulton SL, Zhong P, Farrelly LA, et al. Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking. Science. 2020;368(6487):197-201. DOI: 10.1126/science.aaw8806.

Li Y, Li CY, Xi W, Jin S, Wu ZH, Jiang P, et al. Rostral and caudal ventral tegmental area GABAergic inputs to different dorsal raphe neurons participate in opioid dependence. Neuron. 2019;101(4):748-761.e5. DOI: 10.1016/j.neuron.2018.12.012.

Park JW, Bhimani RV, Park J. Noradrenergic modulation of dopamine transmission evoked by electrical stimulation of the locus coeruleus in the rat brain. ACS Chem Neurosci. 2017;8(9):1913-1924. DOI: 10.1021/acschemneuro.7b00078.

Moncada D. Evidence of VTA and LC control of protein synthesis required for the behavioral tagging process. Neurobiol Learn Mem. 2017;138:226-237.DOI: 10.1016/j.nlm.2016.06.003.


Refbacks

  • There are currently no refbacks.


Creative Commons LicenseThis work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly.