Integrative opioid-GABAergic neuronal mechanisms regulating dopamine efflux in the nucleus accumbens of freely moving animals.
Dopamine release
GABA receptor subtypes
Neuronal interactions
Nucleus accumbens
Opioid receptor subtypes
Journal
Pharmacological reports : PR
ISSN: 2299-5684
Titre abrégé: Pharmacol Rep
Pays: Switzerland
ID NLM: 101234999
Informations de publication
Date de publication:
Aug 2021
Aug 2021
Historique:
received:
13
01
2021
accepted:
11
03
2021
revised:
26
02
2021
pubmed:
21
3
2021
medline:
19
1
2022
entrez:
20
3
2021
Statut:
ppublish
Résumé
The nucleus accumbens (NAc) is a terminal region of mesocorticolimbic dopamine (DA) neuronal projections from the ventral tegmental area. Accumbal DA release is integrated by afferents from other brain regions and by interneurons, which involve a diversity of neurotransmitters and neuropeptides. These integrative processes, implicated in the pathobiology of neuropsychiatric disorders, are mediated via receptor subtypes whose relative roles in the regulation of accumbal DA release are poorly understood. Such complex interactions are exemplified by how selective activation of opioid receptor subtypes enhances accumbal DA efflux in a manner that is modulated by changes in neural activity through GABA receptor subtypes. This review delineates the roles of GABA
Identifiants
pubmed: 33743175
doi: 10.1007/s43440-021-00249-9
pii: 10.1007/s43440-021-00249-9
doi:
Substances chimiques
Receptors, Opioid
0
Dopamine
VTD58H1Z2X
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
971-983Subventions
Organisme : Ministry of Education, Culture, Sports, Science and Technology, Japan
ID : 17K11858
Organisme : Ministry of Education, Culture, Sports, Science and Technology, Japan
ID : 18K09777
Informations de copyright
© 2021. Maj Institute of Pharmacology Polish Academy of Sciences.
Références
Di Chiara G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res. 2002;137:75–114.
pubmed: 12445717
pmcid: 12445717
Nicola SM. The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology. 2007;191:521–50.
pubmed: 16983543
pmcid: 16983543
Floresco SB. The nucleus accumbens: an interface between cognition, emotion, and action. Annu Rev Psychol. 2015;66:25–52.
pubmed: 25251489
pmcid: 25251489
Castro DC, Bruchas MR. A motivational and neuropeptidergic hub: anatomical and functional diversity within the nucleus accumbens shell. Neuron. 2019;102:529–52.
pubmed: 31071288
pmcid: 31071288
Di Chiara G, Bassareo V, Fenu S, De Luca MA, Spina L, Cadoni C, et al. Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology. 2004;47(Suppl 1):227–41.
pubmed: 15464140
pmcid: 15464140
Koob GF, Volkow ND. Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry. 2016;3:760–73.
pubmed: 27475769
pmcid: 27475769
Koob GF. Neurobiology of opioid addiction: opponent process, hyperkatifeia, and negative reinforcement. Biol Psychiatry. 2020;87:44–53.
pubmed: 31400808
pmcid: 31400808
Okutsu H, Watanabe S, Takahashi I, Aono Y, Saigusa T, Koshikawa N, et al. Endomorphin-2 and endomorphin-1 promote the extracellular amount of accumbal dopamine via nonopioid and mu-opioid receptors, respectively. Neuropsychopharmacology. 2006;31:375–83.
pubmed: 16034447
pmcid: 16034447
Saigusa T, Aono Y, Waddington JL. Mechanisms underlying δ- and μ-opioid receptor agonist-induced increases in extracellular dopamine level in the nucleus accumbens of freely moving rats. J Oral Sci. 2017;59:195–200.
pubmed: 28637978
pmcid: 28637978
Aono Y, Saigusa T, Mizoguchi N, Iwakami T, Takada K, Gionhaku N, et al. Role of GABA
pubmed: 18021767
pmcid: 18021767
Aono Y, Kiguchi Y, Watanabe Y, Waddington JL, Saigusa T. Stimulation of accumbal GABA
pubmed: 28923348
pmcid: 28923348
Saigusa T, Aono Y, Mizoguchi N, Iwakami T, Takada K, Oi Y, et al. Role of GABA
pubmed: 18206140
pmcid: 18206140
Watanabe Y, Aono Y, Komiya M, Waddington JL, Saigusa T. Stimulation of accumbal GABA<sub>B</sub> receptors inhibits delta1- and delta2-opioid receptor-mediated dopamine efflux in the nucleus accumbens of freely moving rats. Eur J Pharmacol. 2018;837:88–95.
pubmed: 30086266
pmcid: 30086266
Svingos AL, Clarke CL, Pickel VM. Cellular sites for activation of δ-opioid receptors in the rat nucleus accumbens shell: relationship with Met
pubmed: 9465017
pmcid: 9465017
Svingos AL, Moriwaki A, Wang JB, Uhl GR, Pickel VM. Mu-opioid receptors are localized to extrasynaptic plasma membranes of GABAergic neurons and their targets in the rat nucleus accumbens. J Neurosci. 1997;17:2585–2294.
pubmed: 9065518
pmcid: 9065518
Robinson TG, Beart PM. Excitant amino acid projections from rat amygdala and thalamus to nucleus accumbens. Brain Res Bull. 1988;20:467–71.
pubmed: 3293707
pmcid: 3293707
Blaha CD, Yang CR, Floresco SB, Barr AM, Phillips AG. Stimulation of the ventral subiculum of the hippocampus evokes glutamate receptor-mediated changes in dopamine efflux in the rat nucleus accumbens. Eur J Neurosci. 1997;9:902–11.
pubmed: 9182943
pmcid: 9182943
Christie MJ, James LB, Beart PM. An excitant amino acid projection from the medial prefrontal cortex to the anterior part of nucleus accumbens in the rat. J Neurochem. 1985;45:477–82.
pubmed: 2861249
pmcid: 2861249
Waddington JL, Cross AJ. Neurochemical changes following kainic acid lesions of the nucleus accumbens: implications for a GABAergic accumbal-ventral tegmental pathway. Life Sci. 1978;22:1011–4.
pubmed: 25363
pmcid: 25363
Berendse HW, Groenewegen HJ, Lohman AH. Compartmental distribution of ventral striatal neurons projecting to the mesencephalon in the rat. J Neurosci. 1992;12:2079–103.
pubmed: 1607929
pmcid: 1607929
Zahm DS, Heimer L. Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol. 1993;8:220–32.
Schwarzer C, Berresheim U, Pirker S, Wieselthaler A, Fuchs K, Sieghart W, et al. Distribution of the major gamma-aminobutyric acid(A) receptor subunits in the basal ganglia and associated limbic brain areas of the adult rat. J Comp Neurol. 2001;433:526–49.
pubmed: 11304716
pmcid: 11304716
Chang HT, Kitai ST. Projection neurons of the nucleus accumbens: an intracellular labeling study. Brain Res. 1985;347:112–6.
pubmed: 2996712
pmcid: 2996712
Bolam JP, Clarke DJ, Smith AD, Somogyi P. A type of aspiny neuron in the rat neostriatum accumulates [
pubmed: 6841665
pmcid: 6841665
Kita H, Kitai ST. Glutamate decarboxylase immunoreactive neurons in rat neostriatum: their morphological types and populations. Brain Res. 1988;447:346–52.
pubmed: 3390703
pmcid: 3390703
Xi ZX, Ramamoorthy S, Shen H, Lake R, Samuvel DJ, Kalivas PW. GABA transmission in the nucleus accumbens is altered after withdrawal from repeated cocaine. J Neurosci. 2003;23:3498–505.
pubmed: 12716959
pmcid: 12716959
Bettler B, Kaupmann K, Mosbacher J, Gassmann M. Molecular structure and physiological functions of GABA
pubmed: 15269338
pmcid: 15269338
Davis LL, Trivedi M, Choate A, Kramer GL, Petty F. Growth hormone response to the GABA
pubmed: 9203224
pmcid: 9203224
Mouginot D, Kombian SB, Pittman QJ. Activation of presynaptic GABA
pubmed: 9497428
pmcid: 9497428
Margeta-Mitrovic M, Mitrovic I, Riley RC, Jan LY, Basbaum AI. Immunocytochemical localization of GABA
pubmed: 10076927
pmcid: 10076927
Doherty M, Gratton A. Differential involvement of ventral tegmental GABA(A) and GABA(B) receptors in the regulation of the nucleus accumbens dopamine response to stress. Brain Res. 2007;1150:62–8.
pubmed: 17395162
pmcid: 17395162
Westerink BH, Kwint HF, deVries JB. The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci. 1996;16:2605–11.
pubmed: 8786436
pmcid: 8786436
Ikemoto S, Kohl RR, McBride WJ. GABA(A) receptor blockade in the anterior ventral tegmental area increases extracellular levels of dopamine in the nucleus accumbens of rats. J Neurochem. 1997;69:137–43.
pubmed: 9202304
pmcid: 9202304
Pycock CJ, Horton RW. Dopamine-dependent hyperactivity in the rat following manipulation of GABA mechanisms in the region of the nucleus accumbens. J Neural Trans. 1979;45:17–33.
Wong LS, Eshel G, Dreher J, Ong J, Jackson DM. Role of dopamine and GABA in the control of motor activity elicited from the rat nucleus accumbens. Pharm Biochem Behav. 1991;38:829–35.
Scheel-Krüger J, Arnt J, Magelund G, Olianas M, Przewlocka B, Christensen AV. Behavioural functions of GABA in basal ganglia and limbic system. Brain Res Bull. 1980;5(Suppl 2):261–7.
Rahman S, McBride WJ. Involvement of GABA and cholinergic receptors in the nucleus accumbens on feedback control of somatodendritic dopamine release in the ventral tegmental area. J Neurochem. 2002;80:646–54.
pubmed: 11841572
pmcid: 11841572
Yan Q. Focal bicuculline increases extracellular dopamine concentration in the nucleus accumbens of freely moving rats as measured by in vivo microdialysis. Eur J Pharmacol. 1999;385:7–13.
Ferraro L, Tanganelli S, O’Connor WT, Antonelli T, Rambert F, Fuxe K. The vigilance promoting drug modafinil increases dopamine release in the rat nucleus accumbens via the involvement of a local GABAergic mechanism. Eur J Pharmacol. 1996;306:33–9.
pubmed: 8813612
pmcid: 8813612
Yoshida M, Yokoo H, Nakahara K, Tomita M, Hamada N, Ishikawa M, et al. Local muscimol disinhibits mesolimbic dopaminergic activity as examined by brain microdialysis and Fos immunohistochemistry. Brain Res. 1997;767:356–60.
pubmed: 9367268
pmcid: 9367268
Pijnenburg AJ, van Rossum JM. Stimulation of locomotor activity following injection of dopamine into the nucleus accumbens. J Pharm Pharmacol. 1973;25:1003–5.
pubmed: 4150283
pmcid: 4150283
Ashby CR Jr, Rohatgi R, Ngosuwan J, Borda T, Gerasimov MR, Morgan AE, et al. Implication of the GABA
pubmed: 10024012
pmcid: 10024012
Fadda P, Scherma M, Fresu A, Collu M, Fratta W. Baclofen antagonizes nicotine-, cocaine-, and morphine-induced dopamine release in the nucleus accumbens of rat. Synapse. 2003;50:1–6.
pubmed: 12872287
pmcid: 12872287
Erlander MG, Tobin AJ. The structural and functional heterogeneity of glutamic acid decarboxylase: a review. Neurochem Res. 1991;16:215–26.
pubmed: 1780024
pmcid: 1780024
Buddhala C, Hsu CC, Wu JY. A novel mechanism for GABA synthesis and packaging into synaptic vesicles. Neurochem Int. 2009;55:9–12.
pubmed: 19428801
pmcid: 19428801
Martin DL, Rimvall K. Regulation of gamma-aminobutyric acid synthesis in the brain. J Neurochem. 1993;60:395–407.
pubmed: 8419527
pmcid: 8419527
Waagepetersen HS, Sonnewald U, Schousboe A. The GABA paradox: multiple roles as metabolite, neurotransmitter, and neurodifferentiative agent. J Neurochem. 1999;73:1335–42.
pubmed: 10501176
pmcid: 10501176
Walls AB, Nilsen LH, Eyjolfsson EM, Vestergaard HT, Hansen SL, Schousboe A, et al. GAD65 is essential for synthesis of GABA destined for tonic inhibition regulating epileptiform activity. J Neurochem. 2010;115:1398–408.
pubmed: 21039523
pmcid: 21039523
Bolam JP, Powell JF, Wu JY, Smith AD. Glutamate decarboylase-immunoreactive structures in the rat striatum: a correlated light and electron microscopic study including a combination of Golgi impregnation with immunocytochemistry. J Comp Neurol. 1985;237:1–20.
pubmed: 4044888
pmcid: 4044888
Cowan RL, Wilson CJ, Emson PC, Heizmann CW. Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J Comp Neurol. 1990;302:197–205.
pubmed: 2289971
pmcid: 2289971
Oertel WH, Mugnaini E. Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci Lett. 1984;47:233–8.
pubmed: 6147799
pmcid: 6147799
Lee M, Schwab C, McGeer PL. Astrocytes are GABAergic cells that modulate microglial activity. Glia. 2011;59:152–65.
pubmed: 21046567
pmcid: 21046567
González-Hernández T, Barroso-Chinea P, Acevedo A, Salido E, Rodríguez M. Colocalization of tyrosine hydroxylase and GAD65 mRNA in mesostriatal neurons. Eur J Neurosci. 2001;13:57–67.
pubmed: 11135004
pmcid: 11135004
Saigusa T, Aono Y, Sekino R, Uchida T, Takada K, Oi Y, Koshikawa N, Cools AR. In vivo neurochemical evidence that newly synthesised GABA activates GABA(B), but not GABA(A), receptors on dopaminergic nerve endings in the nucleus accumbens of freely moving rats. Neuropharmacology. 2012;62:907–13.
pubmed: 21964521
pmcid: 21964521
Attwell D, Barbour B, Szatkowski M. Nonvesicular release of neurotransmitter. Neuron. 1993;11:401–7.
pubmed: 8104430
pmcid: 8104430
Rossi DJ, Hamann M, Attwell D. Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J Physiol. 2003;548:97–110.
pubmed: 12588900
pmcid: 12588900
Wall MJ, Usowicz MM. Development of action potential-dependent and independent spontaneous GABA
pubmed: 9104595
pmcid: 9104595
Richerson GB, Wu YM. Dynamic equilibrium of neurotransmitter transportrers; not just for reuptake anymore. J Neurophysiol. 2003;90:1363–74.
pubmed: 12966170
pmcid: 12966170
Kozlov AS, Angulo MC, Audinat E, Charpak S. Target cell-specific modulation of neuronal activity by atrocytes. Proc Natl Acad Sci USA. 2006;103:10058–63.
pubmed: 16782808
pmcid: 16782808
Liu QY, Schaffner AE, Chang YH, Maric D, Barker JL. Persistent activation of GABA
pubmed: 10980012
pmcid: 10980012
Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, et al. The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci. 1998;18:9733–50.
pubmed: 9822734
pmcid: 9822734
Jin H, Wu H, Osterhaus G, Wei J, Davis K, Sha D, et al. Demonstration of functional coupling between gamma-aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci USA. 2003;100:4293–8.
pubmed: 12634427
pmcid: 12634427
Walls AB, Eyjolfsson EM, Smeland OB, Nilsen LH, Schousboe I, Schousboe A, et al. Knockout of GAD65 has major impact on synaptic GABA synthesized from astrocyte-derived glutamine. J Cereb Blood Flow Metab. 2011;31:494–503.
pubmed: 20664610
pmcid: 20664610
Gasnier B. The loading of neurotransmitters into synaptic vesicles. Biochimie. 2000;82:327–37.
pubmed: 10865121
pmcid: 10865121
Galvan A, Hu X, Smith Y, Wichmann T. Localization and pharmacological modulation of GABA-B receptors in the globus pallidus of parkinsonian monkeys. Exp Neurol. 2011;229:429–39.
pubmed: 21419765
pmcid: 21419765
Tepper JM, Lee CR. GABAergic control of substantia nigra dopaminergic neurons. Prog Brain Res. 2007;160:189–208.
pubmed: 17499115
pmcid: 17499115
Azzam AAH, McDonald J, Lambert DG. Hot topics in opioid pharmacology: mixed and biased opioids. Br J Anaesth. 2019;122:e136–45.
pubmed: 31010646
pmcid: 31010646
Narita M, Funada M, Suzuki T. Regulations of opioid dependence by opioid receptor types. Pharmacol Ther. 2001;89:1–15.
pubmed: 11316510
pmcid: 11316510
Fields HL, Margolis EB. Understanding opioid reward. Trends Neurosci. 2015;38:217–25.
pubmed: 25637939
pmcid: 4385443
Yoshida Y, Koide S, Hirose N, Takada K, Tomiyama K, Koshikawa N, et al. Fentanyl increases dopamine release in rat nucleus accumbens: involvement of mesolimbic mu- and delta-2-opioid receptors. Neuroscience. 1999;92:1357–65.
pubmed: 10426490
pmcid: 10426490
Fusa K, Takahashi I, Watanabe S, Aono Y, Ikeda H, Saigusa T, et al. The non-peptidic delta opioid receptor agonist TAN-67 enhances dopamine efflux in the nucleus accumbens of freely moving rats via a mechanism that involves both glutamate and free radicals. Neuroscience. 2005;130:745–55.
pubmed: 15590157
pmcid: 15590157
Hirose N, Murakawa K, Takada K, Oi Y, Suzuki T, Nagase H, et al. Interactions among mu- and delta-opioid receptors, especially putative delta
pubmed: 16111831
pmcid: 16111831
Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ. Autoradiographic differentiation of mu, delta and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci. 1987;7:2445–64.
pubmed: 3039080
pmcid: 3039080
Gouarderes C, Tellez S, Tafani JAM, Zajac J-M. Quantitative autoradiographic mapping of delta-opioid receptors in the rat central nervous system using [
pubmed: 8388577
pmcid: 8388577
Evans CJ, Keith DE, Morrison H, Magendzo K, Edwards RH. Cloning of a delta opioid receptor by functional expression. Science. 1992;258:1952–5.
pubmed: 1335167
pmcid: 1335167
Dietis N, Rowbotham DJ, Lambert DG. Opioid receptor subtypes: fact or artifact? Br J Anaesth. 2011;107:8–18.
pubmed: 21613279
pmcid: 21613279
Pasternak GW, Wood PJ. Multiple mu opiate receptors. Life Sci. 1986;38:1889–98.
pubmed: 2872563
pmcid: 2872563
Saigusa T, Fusa K, Okutsu H, Koshikawa N. Monitoring of extracellular dopamine levels in the dorsal striatum and the nucleus accumbens with 5-minute on-line microdialysis in freely moving rats. J Oral Sci. 2001;43:129–34.