Oxytocin modulates dopamine-mediated reward in the rat subthalamic nucleus

Hormones and Behavior

Volumn 63, Issue 2, 2013, Pages 370-375

  Baracz, Sarah J ^a   Cornish, Jennifer L ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Conditioned place preference; Dopamine; Oxytocin; Reward; Subthalamic nucleus

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; FLUPHENAZINE; OXYTOCIN; OXYTOCIN ANTAGONIST; OXYTOCIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONDITIONING; CONTROLLED STUDY; HISTOLOGY; HORMONE ACTION; LOCOMOTION; MALE; NEUROTRANSMISSION; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; REWARD; SUBTHALAMIC NUCLEUS;

ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; CONDITIONING (PSYCHOLOGY); DOPAMINE; DOPAMINE ANTAGONISTS; DRUG ANTAGONISM; MALE; MOTOR ACTIVITY; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OXYTOCIN; REWARD; SUBTHALAMIC NUCLEUS;

EID: 84872869047     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.12.003     Document Type: Article

References (65)

1. Abrahams B.S., Rutherford J.D., Mallet P.E., Beninger R.J. Place conditioning with the dopamine D1-like receptor agonist SKF 82958 but not SKF 81297 or SKF 77434. Eur. J. Pharmacol. 1998, 343:111-118.
2. Adan R.A.H., Van Leeuwen F.W., Sonnemans M.A.F., Brouns M., Hoffman G., Verbalis J.G., Burbach J.P.H. Rat oxytocin receptor in brain, pituitary, mammary gland, and uterus: partial sequence and immunocytochemical localisation. Endocrinology 1995, 136:4022-4028.
3. Baracz S.J., Rourke P.I., Pardey M.C., Hunt G.E., McGregor I.S., Cornish J.L. Oxytocin directly administered into the nucleus accumbens core or subthalamic nucleus attenuates methamphetamine-induced conditioned place preference. Behav. Brain Res. 2012, 228:185-193. 10.1016/j.bbr.2011.11.038.
4. Bardo M.T., Valone J.M., Bevins R.A. Locomotion and conditioned place preference produced by acute intravenous amphetamine: role of dopamine receptors and individual differences in amphetamine self-administration. Psychopharmacology 1999, 143:39-46.
5. Baskerville T.A., Douglas A.J. Dopamine and oxytocin interactions underlying behaviors: potential contributions to behavioral disorders. CNS Neurosci. Ther. 2010, 16:e92-e123. 10.1111/j.1755-5949.2010.00154.x.
6. Baskerville T.A., Allard J., Wayman C., Douglas A.J. Dopamine-oxytocin interactions in penile erection. Eur. J. Neurosci. 2009, 30:2151-2164. 10.1111/j.1460-9568.2009.06999.x.
7. Baunez C., Lardeux S. Frontal cortex-like functions of the subthalamic nucleus. Front. Syst. Neurosci. 2011, 5:83-95. 10.3389/fnsys.2011.00083.
8. Baunez C., Dias C., Cador M., Amalric M. The subthalamic nucleus exerts opposite control on cocaine and 'natural' rewards. Nat. Neurosci. 2005, 8:484-489. 10.1038/nn1429.
9. Boyson S.J., McGonigle P., Molinoff P.B. Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J. Neurosci. 1986, 6:3177-3188.
10. Carson D.S., Cornish J.L., Guastella A.J., Hunt G.E., McGregor I.S. Oxytocin decreases methamphetamine self-administration, methamphetamine hyperactivity, and relapse to methamphetamine-seeking behaviour in rats. Neuropharmacology 2010, 58:38-43. 10.1016/j.neuropharm.2009.06.018.
11. Carson D.S., Hunt G.E., Guastella A.J., Barber L.L., Cornish J.L., Arnold J.C., Boucher A.A., McGregor I.S. Systemically administered oxytocin decreases methamphetamine activation of the subthalamic nucleus and accumbens core and stimulates oxytocinergic neurons in the hypothalamus. Addict. Biol. 2010, 15:448-463.
12. Chan W.Y., Wo N.C., Stoev S., Cheng L.L., Manning M. Discovery and design of novel and selective vasopressin and oxytocin agonists and antagonists: the role of bioassays. Exp. Physiol. 2003, 85S:7-18.
13. Cornish J.L., Kalivas P.W. Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction. J. Neurosci. 2000, 20:1-5.
14. Coyle J.T., Snyder S.H. Antiparkinsonian drugs: inhibition of dopamine uptake in the corpus striatum as a possible mechanism of action. Science 1969, 166:899-901.
15. Cruickshank C.C., Dyer K.R. A review of the clinical pharmacology of methamphetamine. Addiction 2009, 104:1085-1099.
16. Cui S.-S., Bowen R.C., Gu G.-B., Hanneson D.K., Yu P.H., Zhang X. Prevention of cannabinoid withdrawal syndrome by lithium: involvement of oxytocinergic neuronal activation. J. Neurosci. 2001, 21:9867-9876.
17. Darbaky Y., Baunez C., Arecchi P., Legallet E., Apicella P. Reward-related neuronal activity in the subthalamic nucleus of the monkey. NeuroReport 2005, 16:1241-1244.
18. Di Chiara G. The role of dopamine in drug abuse viewed from the perspective of its role in motivation. Drug Alcohol Depend. 1995, 38:95-137.
19. Elkashef A., Vocci F., Hanson G., White J., Wickes W., Tiihonen J. Pharmacotherapy of methamphetamine addiction: an update. Subst. Abuse 2008, 29:31-49. 10.1080/08897070802218554.
20. Ferguson J.N., Young L.J., Hearn E.F., Matzuk M.M., Insel T.R., Winslow J.T. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 2000, 25:284-288.
21. Figueira R.J., Peabody M.F., Lonstein J.S. Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. Behav. Neurosci. 2008, 122:618-628.
22. Freund-Mercier M.J., Stoeckel M.E., Dietl M.M., Palacios J.M., Richard P. Quantitative autoradiographic mapping of neurophypohysial hormone binding sites in the rat forebrain and pituitary gland-I. Characterisation of different types of binding sites and their distribution in the Long-Evans strain. Neuroscience 1988, 26:261-272.
23. Gordon I., Zagoory-Sharon O., Leckman J.F., Feldman R. Oxytocin and the development of parenting in humans. Biol. Psychiatry 2010, 68:377-382. 10.1016/j.biopsych.2010.02.005.
24. Gordon I., Martin C., Feldman R., Leckman J.F. Oxytocin and social motivation. Dev. Cogn. Neurosci. 2011, 1:471-493. 10.1016/j.dcn.2011.07.007.
25. Greer M., Williams C.M. Dopamine metabolism in Parkinson's disease. Neurology 1963, 13:73-76.
26. Hassani O.-K., Feger J. Effects of intrasubthalamic injection of dopamine receptor agonists on subthalamic neurons in normal and 6-hydroxydopamine-lesioned rats: an electrophysiological and c-fos study. Neuroscience 1999, 92:533-543.
27. Hassani O.-K., Francois C., Yelnik J., Feger J. Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat. Brain Res. 1997, 749:88-94.
28. Herzig V., Schmidt W.J. Effects of MPEP on locomotion, sensitization and conditioned reward induced by cocaine or morphine. Neuropharmacology 2004, 47:973-984.
29. Hyman S.E., Malenka R.C., Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 2006, 29:565-598. 10.1146/.
30. Ikemoto S. Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. Neurosci. Biobehav. Rev. 2010, 35:129-150. 10.1016/j.neubiorev.2010.02.001.
31. Izzo E., Orsini C., Koob G.F., Pulvirenti L. A dopamine partial agonist and antagonist block amphetamine self-administration in a progressive ratio schedule. Pharmacol. Biochem. Behav. 2001, 68:701-708.
32. Janssen M.L., Zwartjes D.G., Tan S.K., Vlamings R., Jahanshahi A., Heida T., Hoogland G., Steinbusch H.W.M., Visser-Vandewalle V., Temel Y. Mild dopaminergic lesions are accompanied by robust changes in subthalamic nucleus activity. Neurosci. Lett. 2012, 508:101-105. 10.1016/j.neulet.2011.12.027.
33. Johnson A.E., Coirini H., Kallstrom L., Wiesel F.-A. Characterization of dopamine receptor binding sites in the subthalamic nucleus. NeuroReport 1994, 5:1836-1838.
34. Koob G.F. Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 2009, 56(Suppl. 1):18-31. 10.1016/j.neuropharm.2008.07.043.
35. Kovacs G.L., Borthaiser Z., Telegdy G. Oxytocin reduces intravenous heroin self-administration in heroin-tolerant rats. Life Sci. 1985, 37:17-26.
36. Kovacs G.L., Horvath Z., Sarnyai Z., Faludi M., Telegdy G. Oxytocin and a c-terminal derivative (z-prolyl-d-leucine) attenuate tolerance to and dependence on morphine and interact with dopaminergic neurotransmission in the mouse brain. Neuropharmacology 1985, 24:413-419.
37. Kovacs G.L., Sarnyai Z., Babarczi E., Szabo G., Telegdy G. The role of oxytocin-dopamine interactions in cocaine-induced locomotor hyperactivity. Neuropharmacology 1990, 29:365-368.
38. Kreiss D.S., Mastropietro C.W., Rawji S.S., Walters J.R. The response of subthalamic nucleus neurons to dopamine receptor stimulation in a rodent model of Parkinson's disease. J. Neurosci. 1997, 17:6807-6819.
39. Lardeux S., Baunez C. Alcohol preference influences the subthalamic nucleus control on motivation for alcohol in rats. Neuropsychopharmacology 2008, 33:634-642. 10.1038/sj.npp. 1301432.
40. Lardeux S., Pernaud R., Paleressompoulle D., Baunez C. Beyond the reward pathway: coding reward magnitude and error in the rat subthalamic nucleus. J. Neurophysiol. 2009, 102:2526-2537. 10.1152/jn.91009.2008.
41. Lintas A., Silkis I.G., Alberi L., Villa A.E. Dopamine deficiency increases synchronized activity in the rat subthalamic nucleus. Brain Res. 2012, 1434:142-151. 10.1016/j.brainres.2011.09.005.
42. Liu Y., Wang Z.-X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 2003, 121:537-544.
43. Manning M., Stoev S., Chini B., Durroux T., Mouillac B., Guillon G. Peptide and non-peptide agonists and antagonists for the vasopressin and oxytocin V1a, V1b, V2 and OT receptors: research tools and potential therapeutic agents. Prog. Brain Res. 2008, 170:473-512. 10.1016/S0079-6123(08)00437-8.
44. McGregor I.S., Bowen M.T. Breaking the loop: oxytocin as a potential treatment for drug addiction. Horm. Behav. 2012, 61:331-339. 10.1016/j.yhbeh.2011.12.001.
45. McGregor I.S., Callaghan P.D., Hunt G.E. From ultrasocial to antisocial: a role for oxytocin in the acute reinforcing effects and long-term adverse consequences of drug use?. Br. J. Pharmacol. 2008, 154:358-368. 10.1038/bjp. 2008.132.
46. Melis M.R., Argiolas A. Central control of penile erection: a re-visitation of the role of oxytocin and its interaction with dopamine and glutamic acid in male rats. Neurosci. Biobehav. Rev. 2011, 35:939-955. 10.1016/j.neubiorev.2010.10.014.
47. Mintz I., Hammond C., Feger J. Excitatory effect of iontophoretically applied dopamine on identified neurons of the rat subthalamic nucleus. Brain Res. 1986, 375:172-175.
48. Paxinos G., Watson C. The Rat Brain Atlas in Stereotaxic Co-ordinates 1997, Academic Press, San Diego. 4th ed.
49. Qi J., Yang J.Y., Song M., Li Y., Wang F., Wu C.F. Inhibition by oxytocin of methamphetamine-induced hyperactivity related to dopamine turnover in the mesolimbic region in mice. Naunyn-Schmiedeberg's Arch. Pharmacol. 2008, 376:441-448. 10.1007/s00210-007-0245-8.
50. Qi J., Yang J.-Y., Wang F., Zhao Y.-N., Song M., Wu C.F. Effects of oxytocin on methamphetamine-induced conditioned place preference and the possible role of glutamatergic neurotransmission in the medial prefrontal cortex of mice in reinstatement. Neuropharmacology 2009, 56:856-865.
51. Rouand T., Lardeux S., Panayotis N., Paleressompoulle D., Cador M., Baunez C. Reducing the desire for cocaine with subthalamic nucleus deep brain stimulation. Proc. Natl. Acad. Sci. 2010, 107:1196-1200.
52. Sarnyai Z., Babarczy E., Krivan M., Szabo G., Kovacs G.L., Barth T., Telegdy G. Selective attenuation of cocaine-induced stereotyped behaviour by oxytocin: putative role of basal forebrain target sites. Neuropeptides 1991, 19:51-56.
53. Schultz W. Multiple reward signals in the brain. Nat. Rev. Neurosci. 2000, 1:199-207.
54. Self D.W., Stein L. The D1 agoists SKF 82958 and SKF 77434 are self-administered by rats. Brain Res. 1992, 582:349-352.
55. Shahrokh D.K., Zhang T.-Y., Diorio J., Gratton A., Meaney M.J. Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Neuroendocrinology 2010, 151:2276-2286.
56. Sinnott R.S., Mach R.H., Nader M.A. Dopamine D2/D3 receptors modulate cocaine's reinforcing and discriminative stimulus effects in rhesus monkeys. Drug Alcohol Depend. 1999, 54:97-110.
57. Succu S., Sanna F., Melis T., Boi A., Argiolas A., Melis M.R. Stimulation of dopamine receptors in the paraventricular nucleus of the hypothalamus of male rats induces penile erection and increases extra-cellular dopamine in the nucleus accumbens: involvement of central oxytocin. Neuropharmacology 2007, 52:1034-1043. 10.1016/j.neuropharm.2006.10.019.
58. Tofighy A., Abbott A., Centonze D., Cooper A.J., Noor E., Pearce S.M., Stanford I.M., Wigmore M.A., Lacey M.G. Excitation by dopamine of rat subthalamic nucleus neurones in vitro - a direct action with unconventional pharmacology. Neuroscience 2003, 116:157-166.
59. Tzschentke T.M. Reassessment of buprenorphine in conditioned place preference: temporal and pharmacological considerations. Psychopharmacology 2004, 172:58-67. 10.1007/s00213-003-1626-4.
60. Vaccari C., Lolait S.J., Ostrowski N.L. Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 1998, 139:5015-5033.
61. Velazquez-Sanchez C., Ferragud A., Renau-Piqueras J., Canales J.J. Therapeutic-like properties of a dopamine uptake inhibitor in animal models of amphetamine addiction. Int. J. Neuropsychopharmacol. 2011, 14:655-665. 10.1017/S1461145710000969.
62. Wilson C.J., Bevan M.D. Intrinsic dynamics and synaptic inputs control the activity patterns of subthalamic nucleus neurons in health and in Parkinson's disease. Neuroscience 2011, 198:54-68. 10.1016/j.neuroscience.2011.06.049.
63. Woolverton W.L., Goldberg L.I., Ginos J.Z. Intravenous self-administration of dopamine receptor agonists by rhesus monkeys. J. Pharmacol. Exp. Ther. 1984, 230:678-683.
64. Yang J.Y., Qi J., Han W.Y., Wang F., Wu C.F. Inhibitory role of oxytocin in psychostimulant-induced psychological dependence and its effects on dopaminergic and glutaminergic transmission. Acta Pharmacol. Sin. 2010, 31:1071-1074. 10.1038/aps.2010.140.
65. Yang J., Pan Y.-J., Zhao Y., Qiu P.-Y., Lu L., Li P., Chen F., Yan X.-Q., Yan X.-Q. Oxytocin in the rat caudate nucleus influences pain modulation. Peptides 2011, 32(10):2104-2107. 10.1016/j.peptides.2011.08.021.