Systemically administered oxytocin decreases methamphetamine activation of the subthalamic nucleus and accumbens core and stimulates oxytocinergic neurons in the hypothalamus

Addiction Biology

Volumn 15, Issue 4, 2010, Pages 448-463

  Carson, Dean S ^a   Hunt, Glenn E ^b   Guastella, Adam J ^a   Barber, Lachlan ^a   Cornish, Jennifer L ^a   Arnold, Jonathon C ^a,c   Boucher, Aurelie A ^a   McGregor, Iain S ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b Discipline of Psychiatry   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

Accumbens core; addiction; hyperactivity; methamphetamine; oxytocin; subthalamic nucleus

Indexed keywords

METHAMPHETAMINE; OXYTOCIN; OXYTOCIN RECEPTOR; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; LOCOMOTION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PERFUSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUBTHALAMIC NUCLEUS; SUPRAOPTIC NUCLEUS; THALAMUS MIDLINE NUCLEUS;

AMPHETAMINE-RELATED DISORDERS; ANIMALS; COMPULSIVE BEHAVIOR; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; HYPOTHALAMUS; MALE; METHAMPHETAMINE; MOTOR ACTIVITY; NERVE NET; NEURONS; NUCLEUS ACCUMBENS; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; STIMULATION, CHEMICAL; SUBTHALAMIC NUCLEUS; SUPRAOPTIC NUCLEUS;

EID: 78649485743     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/j.1369-1600.2010.00247.x     Document Type: Article

References (78)

1. Akerlund M, Bossmar T, Brouard R, Kostrzewska A, Laudanski T, Lemancewicz A, Serradeil-Le Gal C, Steinwall M, (1999) Receptor binding of oxytocin and vasopressin antagonists and inhibitory effects on isolated myometrium from preterm and term pregnant women. Br J Obstet Gynaecol 106: 1047-1053.
2. Andrade-Franze GMF, Andrade CAF, De Luca LA Jr, De Paula PM, Menani JV, (2010) Lateral parabrachial nucleus and central amygdala in the control of sodium intake. Neuroscience 165: 633-641.
3. Antunes-Rodrigues J, De Castro M, Elias LLK, Valenca MM, McCann SM, (2004) Neuroendocrine control of body fluid metabolism. Physiol Rev 84: 169-208.
4. Baskerville TA, Douglas AJ, (2008) Interactions between dopamine and oxytocin in the control of sexual behaviour. Prog Brain Res 170: 277-290.
5. Bassareo V, Di Chiara G, (1999) Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89: 637-641.
6. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E, (2008) Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58: 639-650.
7. Baunez C, Amalric M, Robbins TW, (2002) Enhanced food-related motivation after bilateral lesions of the subthalamic nucleus. J Neurosci 22: 562-568.
8. Baunez C, Dias C, Cador M, Amalric M, (2005) The subthalamic nucleus exerts opposite control on cocaine and 'natural' rewards. Nat Neurosci 8: 484-489.
9. Benabid AL, Koudsie A, Benazzouz A, Vercueil L, Fraix V, Chabardes S, Lebas JF, Pollak P, (2001) Deep brain stimulation of the corpus luysi (subthalamic nucleus) and other targets in Parkinson's disease. Extension to new indications such as dystonia and epilepsy. J Neurol 248 (Suppl. 3): III37-III47.
10. Bergman H, Wichmann T, DeLong MR, (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249: 1436-1438.
11. Bergmann O, Winter C, Meissner W, Harnack D, Kupsch A, Morgenstern R, Reum T, (2004) Subthalamic high frequency stimulation induced rotations are differentially mediated by D1 and D2 receptors. Neuropharmacology 46: 974-983.
12. Canales JJ, Graybiel AM, (2000) A measure of striatal function predicts motor stereotypy. Nat Neurosci 3: 377-383.
13. Carson DS, Cornish JL, Guastella AJ, Hunt GE, McGregor IS, (2010) Oxytocin decreases methamphetamine self-administration, methamphetamine hyperactivity, and relapse to methamphetamine-seeking behaviour in rats. Neuropharmacology 58: 38-43.
14. Catheline G, Touquet B, Lombard MC, Poulain DA, Theodosis DT, (2006) A study of the role of neuro-glial remodeling in the oxytocin system at lactation. Neuroscience 137: 309-316.
15. Chiang C-Y, Cherng CG, Lai Y-T, Fan H-Y, Chuang J-Y, Kao G-S, Chang W-T, Yu L, (2009) Medial prefrontal cortex and nucleus accumbens core are involved in retrieval of the methamphetamine-associated memory. Behav Brain Res 197: 24-30.
16. Cooper AJ, Mitchell IJ, (1995) Fos immuno-positive neurons in the subthalamic nucleus following reversal of parkinsonian symptoms by antagonism of excitatory amino acid transmission in the entopeduncular nucleus of the monoamine depleted rat. Neurosci Lett 201: 251-254.
17. Cruickshank CS, Dyer KR, (2009) A review of the clinical pharmacology of methamphetamine. Addiction 104: 1085-1099.
18. Cui SS, Bowen RC, Gu GB, Hannesson DK, Yu PH, Zhang X, (2001) Prevention of cannabinoid withdrawal syndrome by lithium: involvement of oxytocinergic neuronal activation. J Neurosci 21: 9867-9876.
19. Cushing BS, Yamamoto Y, Hoffman GE, Carter CS, (2003) Central expression of c-Fos in neonatal male and female prairie voles in response to treatment with oxytocin. Dev Brain Res 143: 129-136.
20. Di Chiara G, (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137: 75-114.
21. Dielenberg RA, Hunt GE, McGregor IS, (2001) 'When a rat smells a cat': the distribution of Fos immunoreactivity in rat brain following exposure to a predatory odor. Neuroscience 104: 1085-1097.
22. Domes G, Heinrichs M, Glascher J, Buchel C, Braus DF, Herpertz SC, (2007) Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62: 1187-1190.
23. Dusunceli F, Iseri SO, Ercan F, Gedik N, Yegen C, Yegen BC, (2008) Oxytocin alleviates hepatic ischemia-reperfusion injury in rats. Peptides 29: 1216-1222.
24. Elkashef A, Vocci F, Hanson G, White J, Wickes W, Tiihonen J, (2008) Pharmacotherapy of methamphetamine addiction: an update. Subst Abus 29: 31-49.
25. Engleman EA, Ding ZM, Oster SM, Toalston JE, Bell RL, Murphy JM, McBride WJ, Rodd ZA, (2009) Ethanol is self-administered into the nucleus accumbens shell, but not the core: evidence of genetic sensitivity. Alcohol Clin Exp Res 33: 2162-2171.
26. Ermisch A, Barth T, Ruhle HJ, Skopkova J, Hrbas P, Landgraf R, (1985) On the blood-brain barrier to peptides: accumulation of labelled vasopressin, DesGlyNH2-vasopressin and oxytocin by brain regions. Endocrinol Exp 19: 29-37.
27. Febo M, Numan M, Ferris CF, (2005) Functional magnetic resonance imaging shows oxytocin activates brain regions associated with mother-pup bonding during suckling. J Neurosci 25: 11637-11644.
28. Febo M, Shields J, Ferris CF, King JA, (2009) Oxytocin modulates unconditioned fear response in lactating dams: an fMRI study. Brain Res 1302: 183-193.
29. Grindstaff RJ, Grindstaff RR, Sullivan MJ, Cunningham JT, (2000) Role of the locus ceruleus in baroreceptor regulation of supraoptic vasopressin neurons in the rat. Am J Physiol Regul Integr Comp Physiol 279: R306-R319.
30. Gross NB, Marshall JF, (2009) Striatal dopamine and glutamate receptors modulate methamphetamine-induced cortical Fos expression. Neuroscience 161: 1114-1125.
31. Guastella AJ, Howard AL, Dadds MR, Mitchell P, Carson DS, (2009) A randomized controlled trial of intranasal oxytocin as an adjunct to exposure therapy for social anxiety disorder. Psychoneuroendocrinology 34: 917-923.
32. Guastella AJ, Einfeld SL, Gray KM, Rinehart NJ, Tonge BJ, Lambert TJ, Hickie IB, (2010) Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry 67: 692-694.
33. Holder MK, Hadjimarkou MM, Zup SL, Blutstein T, Benham RS, McCarthy MM, Mong JA, (2010) Methamphetamine facilitates female sexual behavior and enhances neuronal activation in the medial amygdala and ventromedial nucleus of the hypothalamus. Psychoneuroendocrinology 35: 197-208.
34. Hollander E, Bartz J, Chaplin W, Phillips A, Sumner J, Soorya L, Anagnostou E, Wasserman S, (2007) Oxytocin increases retention of social cognition in autism. Biol Psychiatry 61: 498-503.
35. Hull EM, Dominguez JM, (2007) Sexual behavior in male rodents. Horm Behav 52: 45-55.
36. Jin D, Liu H-X, Hirai H, Torashima T, Nagai T, Lopatina O, Shnayder NA, Yamada K, Noda M, Seike T, Fujita K, Takasawa S, Yokoyama S, Koizumi K, Shiraishi Y, Tanaka S, Hashii M, Yoshihara T, Higashida K, Islam MS, Yamada N, Hayashi K, Noguchi N, Kato I, Okamoto H, Matsushima A, Salmina A, Munesue T, Shimizu N, Mochida S, Asano M, Higashida H, (2007) CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446: 41-45.
37. Joo KW, Jeon US, Kim G-H, Park J, Oh YK, Kim YS, Ahn C, Kim S, Kim SY, Lee JS, Han JS, (2004) Antidiuretic action of oxytocin is associated with increased urinary excretion of aquaporin-2. Nephrol Dial Transplant 19: 2480-2486.
38. Kita I, Yoshida Y, Nishino S, (2006) An activation of parvocellular oxytocinergic neurons in the paraventricular nucleus in oxytocin-induced yawning and penile erection. Neurosci Res 54: 269-275.
39. Klavir O, Flash S, Winter C, Joel D, (2009) High frequency stimulation and pharmacological inactivation of the subthalamic nucleus reduces 'compulsive' lever-pressing in rats. Exp Neurol 215: 101-109.
40. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E, (2005) Oxytocin increases trust in humans. Nature 435: 673-676.
41. Kovacs GL, Telegdy G, (1987) Beta-endorphin tolerance is inhibited by oxytocin. Pharmacol Biochem Behav 26: 57-60.
42. Kovacs GL, Sarnyai Z, Szabo G, (1998) Oxytocin and addiction: a review. Psychoneuroendocrinology 23: 945-962.
43. Kramer KM, Cushing BS, Carter CS, (2003) Developmental effects of oxytocin on stress response: single versus repeated exposure. Physiol Behav 79: 775-782.
44. Krasnova IN, Cadet JL, (2009) Methamphetamine toxicity and messengers of death. Brain Res Rev 60: 379-407.
45. Landgraf R, Ermisch A, Hess J, (1979) Indications for a brain uptake of labelled vasopressin and ocytocin and the problem of the blood-brain barrier. Endokrinologie 73: 77-81.
46. Lardeux S, Baunez C, (2008) Alcohol preference influences the subthalamic nucleus control on motivation for alcohol in rats. Neuropsychopharmacology 33: 634-642.
47. Lardeux S, Pernaud R, Paleressompoulle D, Baunez C, (2009) Beyond the reward pathway: coding reward magnitude and error in the rat subthalamic nucleus. J Neurophysiol 102: 2526-2537.
48. Lee NK, Rawson RA, (2008) A systematic review of cognitive and behavioural therapies for methamphetamine dependence. Drug Alcohol Rev 27: 309-317.
49. Lee Y, Hamamura T, Ohashi K, Fujiwara Y, Kuroda S, (1999) The effect of lithium on methamphetamine-induced regional Fos protein expression in the rat brain. Neuroreport 10: 895-900.
50. McGregor IS, Hargreaves GA, Apfelbach R, Hunt GE, (2004) Neural correlates of cat odor-induced anxiety in rats: region-specific effects of the benzodiazepine midazolam. J Neurosci 24: 4134-4144.
51. McGregor IS, Callaghan PD, Hunt GE, (2008) From ultrasocial to antisocial: a role for oxytocin in the acute reinforcing effects and long-term adverse consequences of drug use? Br J Pharmacol 154: 358-368.
52. McKinley MJ, Johnson AK, (2004) The physiological regulation of thirst and fluid intake. News Physiol Sci 19: 1-6.
53. Maurice N, Deniau JM, Glowinski J, Thierry AM, (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 18: 9539-9546.
54. Moody KM, Adler NT, (1995) The role of the uterus and cervix in systemic oxytocin-PGE2 facilitated lordosis behavior. Horm Behav 29: 571-580.
55. Van Nieuwenhuijzen PS, McGregor IS, Hunt GE, (2009) The distribution of gamma-hydroxybutyrate-induced Fos expression in rat brain: comparison with baclofen. Neuroscience 158: 441-455.
56. Paxinos G, Watson C, (1997) The Rat Brain in Stereotaxic Coordinates, 3rd edn Sydney: Academic Press.
57. Pontieri FE, Crane AM, Seiden LS, Kleven MS, Porrino LJ, (1990) Metabolic mapping of the effects of intravenous methamphetamine administration in freely moving rats. Psychopharmacology 102: 175-182.
58. Popeski N, Woodside B, (2001) Effect of nitric oxide synthase inhibition on fos expression in the hypothalamus of female rats following central oxytocin and systemic urethane administration. J Neuroendocrinol 13: 596-607.
59. Popik P, Vetulani J, Van Ree JM, (1992) Low doses of oxytocin facilitate social recognition in rats. Psychopharmacology 106: 71-74.
60. Qi J, Yang JY, Song M, Li Y, Wang F, Wu CF, (2008) Inhibition by oxytocin of methamphetamine-induced hyperactivity related to dopamine turnover in the mesolimbic region in mice. Naunyn-Schmiedebergs. Arch Pharmacol 376: 441-448.
61. Qi J, Yang J-Y, Wang F, Zhao Y-N, Song M, Wu C-F, (2009) 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 56: 856-865.
62. Ring RH, Malberg JE, Potestio L, Ping J, Boikess S, Luo B, Schechter LE, Rizzo S, Rahman Z, Rosenzweig-Lipson S, (2006) Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology 185: 218-225.
63. Rose ME, Grant JE, (2008) Pharmacotherapy for methamphetamine dependence: a review of the pathophysiology of methamphetamine addiction and the theoretical basis and efficacy of pharmacotherapeutic interventions. Ann Clin Psychiatry 20: 145-155.
64. Rossoni E, Feng J, Tirozzi B, Brown D, Leng G, Moos F, (2008) Emergent synchronous bursting of oxytocin neuronal network. Plos Comput Biol 4: e1000123.
65. Smeding HMM, Goudriaan AE, Foncke EMJ, Schuurman PR, Speelman JD, Schmand B, (2007) Pathological gambling after bilateral subthalamic nucleus stimulation in Parkinson disease. J Neurol Neurosurg Psychiatry 78: 517-519.
66. Smith-Roe SL, Kelley AE, (2000) Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20: 7737-7742.
67. Swanson LW, Sawchenko PE, (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6: 269-324.
68. Szabo G, Kovacs GL, Telegdy G, (1987) Effects of neurohypophyseal peptide hormones on alcohol dependence and withdrawal. Alcohol Alcohol 22: 71-74.
69. Temel Y, Blokland A, Steinbusch HWM, Visser-Vandewalle V, (2005) The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol 76: 393-413.
70. Thompson MR, Callaghan PD, Hunt GE, Cornish JL, McGregor IS, (2007) A role for oxytocin and 5-HT(1A) receptors in the prosocial effects of 3,4 methylenedioxymethamphetamine ('ecstasy'). Neuroscience 146: 509-514.
71. Uslaner JM, Yang P, Robinson TE, (2005) Subthalamic nucleus lesions enhance the psychomotor-activating, incentive motivational, and neurobiological effects of cocaine. J Neurosci 25: 8407-8415.
72. Uvnas-Moberg K, Ahlenius S, Hillegaart V, Alster P, (1994) High doses of oxytocin cause sedation and low doses cause an anxiolytic-like effect in male rats. Pharmacol Biochem Behav 49: 101-106.
73. Vaccari C, Lolait SJ, Ostrowski NL, (1998) Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 139: 5015-5033.
74. Veenema AH, Neumann ID, (2008) Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res 170: 261-276.
75. Viviani D, Stoop R, (2008) Opposite effects of oxytocin and vasopressin on the emotional expression of the fear response. Prog Brain Res 170: 207-218.
76. Winter C, Flash S, Klavir O, Klein J, Sohr R, Joel D, (2008a) The role of the subthalamic nucleus in 'compulsive' behavior in rats. Eur J Neurosci 27: 1902-1911.
77. Winter C, Lemke C, Sohr R, Meissner W, Harnack D, Juckel G, Morgenstern R, Kupsch A, (2008b) High frequency stimulation of the subthalamic nucleus modulates neurotransmission in limbic brain regions of the rat. Exp Brain Res 185: 497-507.
78. Yoshimura R, Kiyama H, Kimura T, Araki T, Maeno H, Tanizawa O, Tohyama M, (1993) Localization of oxytocin receptor messenger ribonucleic acid in the rat brain. Endocrinology 133: 1239-1246.