Involvement of basolateral amygdala dopamine D1 receptors in the acquisition and expression of morphine-induced place preference in rats

Authors

Department of Physiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

Abstract

Background: In the present study, the effects of intra-basolateral amygdala (BLA) blockade of dopamine D1 receptor on morphine-induced conditioned place preference (CPP) were investigated in male Wistar rats. Materials and Methods: A 5-day CPP paradigm was used. Morphine was injected subsequently at effective (5 mg/kg) and ineffective (0.5 mg/kg) doses. SCH 23390 (0.5– μg/rat), as a selective D1 receptor antagonist, was microinjected bilaterally into the BLA. Results: Effective dose of morphine induced a significant CPP, and increased the locomotor activity during the testing phase. The results showed that morphine-induced CPP was significantly suppressed by D1 receptors antagonist in BLA in the acquisition phase and caused an aversion even at high doses. The antagonist also significantly prevented CPP expression. Morphine increased the motor activity, but the D1 receptors blockade, significantly reduced it. Conclusions: The findings of this study suggest a possible role for BLA dopamine D1 receptors in reward responses in morphine dependency.

Keywords

1.
Fischer B, Jones W, Urbanoski K, Skinner R, Rehm J. Correlations between prescription opioid analgesic dispensing levels and related mortality and morbidity in Ontario, Canada, 2005-2011. Drug Alcohol Rev 2014;33:19-26.  Back to cited text no. 1
    
2.
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;20:4302.  Back to cited text no. 2
    
3.
Kumar K, Kelly M, Pirlot T. Continuous intrathecal morphine treatment for chronic pain of nonmalignant etiology: Long-term benefits and efficacy. Surg Neurol 2001;55:79-86.  Back to cited text no. 3
    
4.
LeResche L, Saunders K, Dublin S, Thielke S, Merrill JO, Shortreed SM, et al. Sex and age differences in global pain status among patients using opioids long term for chronic noncancer pain. J Womens Health (Larchmt) 2015;24:629-35.  Back to cited text no. 4
    
5.
Powledge TM. Addiction and the brain: The dopamine pathway is helping researchers find their way through the addiction maze. BioScience 1999;49:513-9.  Back to cited text no. 5
    
6.
Ayano G. Dopamine: Receptors, functions, synthesis, pathways, locations and mental disorders: Review of literatures. J Ment Disord Treat 2016;2:2.  Back to cited text no. 6
    
7.
Wassum KM, Izquierdo A. The basolateral amygdala in reward learning and addiction. Neurosci Biobehav Rev 2015;57:271-83.  Back to cited text no. 7
    
8.
Babaev O, Piletti Chatain C, Krueger-Burg D. Inhibition in the amygdala anxiety circuitry. Exp Mol Med 2018;50:1-16.  Back to cited text no. 8
    
9.
Hiroi N, White NM. The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference. J Neurosci 1991;11:2107-16.  Back to cited text no. 9
    
10.
Hatfield T, Han JS, Conley M, Gallagher M, Holland P. Neurotoxic lesions of basolateral, but not central, amygdala interfere with pavlovian second-order conditioning and reinforcer devaluation effects. J Neurosci 1996;16:5256-65.  Back to cited text no. 10
    
11.
Cai YQ, Wang W, Paulucci-Holthauzen A, Pan ZZ. Brain circuits mediating opposing effects on emotion and pain. J Neurosci 2018;38:6340-9.  Back to cited text no. 11
    
12.
Ambroggi F, Ishikawa A, Fields HL, Nicola SM. Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron 2008;59:648-61.  Back to cited text no. 12
    
13.
Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 2012;76:790-803.  Back to cited text no. 13
    
14.
Speranza L, di Porzio U, Viggiano D, de Donato A, Volpicelli F. Dopamine: The neuromodulator of long-term synaptic plasticity, reward and movement control. Cells 2021;10:735.  Back to cited text no. 14
    
15.
Yang H, de Jong JW, Tak Y, Peck J, Bateup HS, Lammel S. Nucleus accumbens subnuclei regulate motivated behavior via direct inhibition and disinhibition of VTA dopamine subpopulations. Neuron 2018;97:434-49.e4.  Back to cited text no. 15
    
16.
Dearry A, Gingrich JA, Falardeau P, Fremeau RT, Bates MD, Caron MG. Molecular cloning and expression of the gene for a human D 1 dopamine receptor. Nature 1990;347:72-6.  Back to cited text no. 16
    
17.
Grandy DK, Zhang YA, Bouvier C, Zhou QY, Johnson RA, Allen L, et al. Multiple human D5 dopamine receptor genes: A functional receptor and two pseudogenes. Proc Natl Acad Sci U S A 1991;88:9175-9.  Back to cited text no. 17
    
18.
Bonifazi A, Yano H, Guerrero AM, Kumar V, Hoffman AF, Lupica CR, et al. Novel and potent dopamine D2 receptor go-protein biased agonists. ACS Pharmacol Transl Sci 2019;2:52-65.  Back to cited text no. 18
    
19.
Guitart X, Moreno E, Rea W, Sánchez-Soto M, Cai NS, Quiroz C, et al. Biased G protein-independent signaling of dopamine D1-D3 receptor heteromers in the nucleus accumbens. Mol Neurobiol 2019;56:6756-69.  Back to cited text no. 19
    
20.
Van Tol HH, Bunzow JR, Guan HC, Sunahara RK, Seeman P, Niznik HB, et al. Cloning of the gene for a human dopamine D4 receptor with high affinity for the antipsychotic clozapine. Nature 1991;350:610-4.  Back to cited text no. 20
    
21.
Tritsch NX, Sabatini BL. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 2012;76:33-50.  Back to cited text no. 21
    
22.
Baker DA, Fuchs RA, Specio SE, Khroyan TV, Neisewander JL. Effects of intraaccumbens administration of SCH-23390 on cocaine-induced locomotion and conditioned place preference. Synapse 1998;30:181-93.  Back to cited text no. 22
    
23.
Zarrindast MR, Rezayof A, Sahraei H, Haeri-Rohani A, Rassouli Y. Involvement of dopamine D1 receptors of the central amygdala on the acquisition and expression of morphine-induced place preference in rat. Brain Res 2003;965:212-21.  Back to cited text no. 23
    
24.
Rezayof A, Zarrindast MR, Sahraei H, Haeri-Rohani A. Involvement of dopamine receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. J Psychopharmacol 2003;17:415-23.  Back to cited text no. 24
    
25.
Shippenberg TS, Bals-Kubik R, Huber A, Herz A. Neuroanatomical substrates mediating the aversive effects of D-1 dopamine receptor antagonists. Psychopharmacology (Berl) 1991;103:209-14.  Back to cited text no. 25
    
26.
Esmaeili MH, Kermani M, Parvishan A, Haghparast A. Role of D1/D2 dopamine receptors in the CA1 region of the rat hippocampus in the rewarding effects of morphine administered into the ventral tegmental area. Behav Brain Res 2012;231:111-5.  Back to cited text no. 26
    
27.
Assar N, Mahmoudi D, Farhoudian A, Farhadi MH, Fatahi Z, Haghparast A. D1- and D2-like dopamine receptors in the CA1 region of the hippocampus are involved in the acquisition and reinstatement of morphine-induced conditioned place preference. Behav Brain Res 2016;312:394-404.  Back to cited text no. 27
    
28.
Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates: Fifth ed. San Diego: Academic Press; 2005; 46-61.  Back to cited text no. 28
    
29.
Haghparast A, Esmaeili MH, Taslimi Z, Kermani M, Yazdi-Ravandi S, Alizadeh AM. Intrahippocampal administration of D2 but not D1 dopamine receptor antagonist suppresses the expression of conditioned place preference induced by morphine in the ventral tegmental area. Neurosci Lett 2013;541:138-43.  Back to cited text no. 29
    
30.
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;198:466-71.  Back to cited text no. 30
    
31.
Bariselli S, Glangetas C, Tzanoulinou S, Bellone C. Ventral tegmental area subcircuits process rewarding and aversive experiences. J Neurochem 2016;139:1071-80.  Back to cited text no. 31
    
32.
Lintas A, Chi N, Lauzon NM, Bishop SF, Gholizadeh S, Sun N, et al. Identification of a dopamine receptor-mediated opiate reward memory switch in the basolateral amygdala-nucleus accumbens circuit. J Neurosci 2011;31:11172-83.  Back to cited text no. 32
    
33.
Rosenkranz JA, Grace AA. Modulation of basolateral amygdala neuronal firing and afferent drive by dopamine receptor activation in vivo. J Neurosci 1999;19:11027-39.  Back to cited text no. 33
    
34.
McDonald RJ, White NM. A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum. Behav Neurosci 1993;107:3-22.  Back to cited text no. 34
    
35.
Gallagher M, Graham PW, Holland PC. The amygdala central nucleus and appetitive Pavlovian conditioning: Lesions impair one class of conditioned behavior. J Neurosci 1990;10:1906-11.  Back to cited text no. 35
    
36.
Mogenson GJ, Jones DL, Yim CY. From motivation to action: Functional interface between the limbic system and the motor system. Prog Neurobiol 1980;14:69-97.  Back to cited text no. 36
    
37.
Cuomo V, Cagiano R, Colonna M, Renna G, Racagni G. Influence of SCH 23390, a DA1-receptor antagonist, on the behavioural responsiveness to small and large doses of apomorphine in rats. Neuropharmacology 1986;25:1297-300.  Back to cited text no. 37
    
38.
Carlsson A. On the neuronal circuitries and neurotransmitters involved in the control of locomotor activity. J Neural Transm Suppl 1993;40:1-12.  Back to cited text no. 38
    
39.
Pettersson I, Gundertofte K, Palm J, Liljefors T. A study on the contribution of the 1-phenyl substituent to the molecular electrostatic potentials of some benzazepines in relation to selective dopamine D-1 receptor activity. J Med Chem 1992;35:502-7.  Back to cited text no. 39
    
40.
Tobin S, Sedki F, Abbas Z, Shalev U. Antagonism of the dopamine D1-like receptor in mesocorticolimbic nuclei attenuates acute food deprivation-induced reinstatement of heroin seeking in rats. Eur J Neurosci 2013;37:972-81.  Back to cited text no. 40
    
41.
Andrzejewski ME, Spencer R, Kelley A. Instrumental learning, but not performance, requires dopamine D1-receptor activation in the amygdala. Neuroscience 2005;135:335-45.  Back to cited text no. 41
    
42.
Young EA, Dreumont SE, Cunningham CL. Role of nucleus accumbens dopamine receptor subtypes in the learning and expression of alcohol-seeking behavior. Neurobiol Learn Mem 2014;108:28-37.  Back to cited text no. 42
    
43.
Gao J, Li Y, Zhu N, Brimijoin S, Sui N. Roles of dopaminergic innervation of nucleus accumbens shell and dorsolateral caudate-putamen in cue-induced morphine seeking after prolonged abstinence and the underlying D1- and D2-like receptor mechanisms in rats. J Psychopharmacol 2013;27:181-91.  Back to cited text no. 43
    
44.
Hiroi N, White NM. The amphetamine conditioned place preference: Differential involvement of dopamine receptor subtypes and two dopaminergic terminal areas. Brain Res 1991;552:141-52.  Back to cited text no. 44
    
45.
Khroyan TV, Barrett-Larimore RL, Rowlett JK, Spealman RD. Dopamine D1- and D2-like receptor mechanisms in relapse to cocaine-seeking behavior: Effects of selective antagonists and agonists. J Pharmacol Exp Ther 2000;294:680-7.  Back to cited text no. 45
    
46.
Khroyan TV, Platt DM, Rowlett JK, Spealman RD. Attenuation of relapse to cocaine seeking by dopamine D1 receptor agonists and antagonists in non-human primates. Psychopharmacology (Berl) 2003;168:124-31.  Back to cited text no. 46
    
47.
Adams JU, Careri JM, Efferen TR, Rotrosen J. Differential effects of dopamine antagonists on locomotor activity, conditioned activity and conditioned place preference induced by cocaine in rats. Behav Pharmacol 2001;12:603-11.  Back to cited text no. 47
    
48.
Shimosato K, Ohkuma S. Simultaneous monitoring of conditioned place preference and locomotor sensitization following repeated administration of cocaine and methamphetamine. Pharmacol Biochem Behav 2000;66:285-92.  Back to cited text no. 48
    
49.
Mucha RF, Volkovskis C, Kalant H. Conditioned increases in locomotor activity produced with morphine as an unconditioned stimulus, and the relation of conditioning to acute morphine effect and tolerance. J Comp Physiol Psychol 1981;95:351-62.  Back to cited text no. 49
    
50.
O'Neill MF, Shaw G. Comparison of dopamine receptor antagonists on hyperlocomotion induced by cocaine, amphetamine, MK-801 and the dopamine D1 agonist C-APB in mice. Psychopharmacology (Berl) 1999;145:237-50.  Back to cited text no. 50
    
51.
Waelti P, Dickinson A, Schultz W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 2001;412:43-8.  Back to cited text no. 51
    
52.
Everitt BJ, Wolf ME. Psychomotor stimulant addiction: A neural systems perspective. J Neurosci 2002;22:3312-20.  Back to cited text no. 52
    
53.
Finch DM. Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus 1996;6:495-512.  Back to cited text no. 53
    
54.
Floresco SB, Blaha CD, Yang CR, Phillips AG. Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala-evoked firing of nucleus accumbens neurons. J Neurosci 2001;21:6370-6.  Back to cited text no. 54