Positive reinforcing effect of oxytocin microinjection in the rat central nucleus of amygdala

Behavioural Brain Research

Volumn 296, Issue , 2016, Pages 279-285

  Laszlo K ^a   Kovacs A ^a   Zagoracz, O ^a   Ollmann, T ^a   Peczely L ^a   Kertes, E ^a   Lacy, D G ^c   Lenard L ^a,b  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Amygdala; Anxiety; Oxytocin; Place preference; Poistive reinforcement; Rat

Indexed keywords

L 2540; OXYTOCIN; OXYTOCIN RECEPTOR ANTAGONIST; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; ANXIOLYTIC AGENT; OXYTOCIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; DRUG EFFECT; ELEVATED PLUS MAZE TEST; MALE; MICROINJECTION; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; REINFORCEMENT; TRANQUILIZING ACTIVITY; WISTAR RAT; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; CONDITIONING; DRUG EFFECTS; DRUG THERAPY; MAZE TEST;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; CENTRAL AMYGDALOID NUCLEUS; CONDITIONING (PSYCHOLOGY); MALE; MAZE LEARNING; MICROINJECTIONS; OXYTOCIN; RATS; RATS, WISTAR; RECEPTORS, OXYTOCIN; REINFORCEMENT (PSYCHOLOGY);

EID: 84942543833     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.09.021     Document Type: Article

References (56)

1. Insel T.R. Oxytocin-a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology 1992, 17:3-35.
2. Stoop R. Neuromodulation by oxytocin and vasopressin. Neuron 2012, 76:142-159.
3. Love T.M. Oxytocin motivation and the role of dopamine. Pharmacol. Biochem. Behav. 2014, 119:49-60.
4. Sarnyai Z., Kovacs G.L. Oxytocin in learning and addiction: from early discoveries to the present. Pharmacol. Biochem. Behav. 2014, 119:3-9.
5. Han Y., Yu L.C. Involvement of oxytocin and its receptor in nociceptive modulation in the central nucleus of amygdala of rats. Neurosci. Lett. 2009, 454:101-104.
6. Bartz J.A., Hollander E. The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior. Horm. Behav. 2006, 50:518-528.
7. Heinrichs M., von Dawans B., Domes G. Oxytocin, vasopressin, and human social behavior. Front. Neuroendocrinol. 2009, 30:548-557.
8. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
9. Bale T.L., Davis A.M., Auger A.P., Dorsa D.M., McCarthy M.M. CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J. Neurosci. 2001, 21:2546-2552.
10. Huber D., Veinante P., Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 2005, 308:245-248.
11. Dumais K.M., Veenema A.H. Vasopressin and oxytocin receptor systems in the brain: sex differences and sex-specific regulation of social behavior. Front. Neuroendocrinol. 2015, 807.
12. Gimpl G., Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 2001, 81:629-683.
13. Freeman S.M., Inoue K., Smith A.L., Goodman M.M., Young L.J. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Psychoneuroendocrinology 2014, 45:128-141.
14. Toloczko D.M., Young L., Insel T.R. Are there oxytocin receptors in the primate brain. Integr. Neurobiol. Affiliation 1997, 807:506-509.
15. Barberis C., Audigier S., Durroux T., Elands J., Schmidt A., Jard S. Pharmacology of oxytocin and vasopressin receptors in the central and peripheral nervous-system. Ann. N. Y. Acad. Sci. 1992, 652:39-45.
16. McGaugh J.L., Introini-Collison I.B., Cahill L.F., Castellano C., Dalmaz C., Parent M.B., Williams C.L. Neuromodulatory systems and memory storage: role of the amygdala. Behav. Brain Res. 1993, 58:81-90.
17. Murray E.A. The amygdala, reward and emotion. Trends Cogn. Sci. 2007, 11:489-497.
18. Watanabe N., Sakagami M., Haruno M. Reward prediction error signal enhanced by striatum-amygdala interaction explains the acceleration of probabilistic reward learning by emotion. J. Neurosci. 2013, 33:4487-4493.
19. Laszlo K., Toth K., Kertes E., Peczely L., Lenard L. The role of neurotensin in positive reinforcement in the rat central nucleus of amygdala. Behav. Brain Res. 2010, 208:430-435.
20. Lenard L., Kovacs A., Ollmann T., Peczely L., Zagoracz O., Galosi R., Laszlo K. Positive reinforcing effects of RFamide-related peptide-1 in the rat central nucleus of amygdala. Behav Brain Res. 2014, 275:101-106.
21. Baxter M.G., Murray E.A. The amygdala and reward. Nat. Rev. Neurosci. 2002, 3:563-573.
22. Knobloch H.S., Charlet A., Hoffmann L.C., Eliava M., Khrulev S., Cetin A.H., Osten P., Schwarz M.K., Seeburg P.H., Stoop R., Grinevicht V. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 2012, 73:553-566.
23. Sanna F., Argiolas A., Melis M.R. Oxytocin-induced yawning: sites of action in the brain and interaction with mesolimbic/mesocortical and incertohypothalamic dopaminergic neurons in male rats. Horm. Behav. 2012, 62:505-514.
24. Melis M.R., Succu S., Sanna F., Boi A., Argiolas A. Oxytocin injected into the ventral subiculum or the posteromedial cortical nucleus of the amygdala induces penile erection and increases extracellular dopamine levels in the nucleus accumbens of male rats. Eur. J. Neurosci. 2009, 30:1349-1357.
25. Calcagnoli F., Stubbendorff C., Meyer N., de Boer S.F., Althaus M., Koolhaas J.M. Oxytocin microinjected into the central amygdaloid nuclei exerts anti-aggressive effects in male rats. Neuropharmacology 2015, 90:74-81.
26. Terenzi M.G., Ingram C.D. Oxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei. Neuroscience 2005, 134:345-354.
27. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1986, Academic Press, New York. second ed.
28. Tzschentke T.M. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol. 1998, 56:613-672.
29. Hasenohrl R.U., Oitzl M.S., Huston J.P. Conditioned place preference in the corral-a procedure for measuring reinforcing properties of drugs. J. Neurosci. Methods 1989, 30:141-146.
30. Huston J.P., Hasenohrl R.U., Boix F., Gerhardt P., Schwarting R.K.W. Sequence-specific effects of Neurokinin Substance-P on memory, reinforcement, and brain dopamine activity. Psychopharmacology (Berl) 1993, 112:147-162.
31. Oitzl M.S., Hasenohrl R.U., Huston J.P. Reinforcing effects of peripherally administered substance P and its C-terminal sequence pGlu6-SP 6-11 in the rat. Psychopharmacology (Berl) 1990, 100:308-315.
32. Laszlo K., Toth K., Kertes E., Peczely L., Ollmann T., Madarassy-Szucs A., Lenard L. The role of neurotensin in passive avoidance learning in the rat central nucleus of amygdala. Behav. Brain Res. 2012, 226:597-600.
33. Benelli A., Bertolini A., Poggioli R., Menozzi B., Basaglia R., Arletti R. Polymodal dose-response curve for oxytocin in the social recognition test. Neuropeptides 1995, 28:251-255.
34. Boccia M.M., Kopf S.R., Baratti C.M. Effects of a single administration of oxytocin or vasopressin and their interactions with two selective receptor antagonists on memory storage in mice. Neurobiol. Learn. Mem. 1998, 69:136-146.
35. de Oliveira L.F., Camboim C., Diehl F., Consiglio A.R., Quillfeldt J.A. Glucocorticoid-mediated effects of systemic oxytocin upon memory retrieval. Neurobiol. Learn. Mem. 2007, 87:67-71.
36. Popik P., Vetulani J., Vanree J.M. Low-doses of oxytocin facilitate social recognition in rats. Psychopharmacology (Berl) 1992, 106:71-74.
37. Popik P., Vetulani J., VanRee J.M. Facilitation and attenuation of social recognition in rats by different oxytocin-related peptides. Eur. J. Pharmacol. 1996, 308:113-116.
38. Sala M., Braida D., Donzelli A., Martucci R., Busnelli M., Bulgheroni E., Rubino T., Parolaro D., Nishimori K., Chini B. Mice heterozygous for the oxytocin receptor gene (Oxtr(+/-)) show impaired social behavior but not increased aggression or cognitive inflexibility: evidence of a selective haploinsufficiency gene effect. J. Neuroendocrinol. 2013, 25:107-118.
39. Sala M., Braida D., Lentini D., Busnelli M., Bulgheroni E., Capurro V., Finardi A., Donzelli A., Pattini L., Rubino T., Parolaro D., Nishimori K., Parenti M., Chini B. Pharmacologic rescue of impaired cognitive flexibility, social deficits, increased aggression, and seizure susceptibility in oxytocin receptor null mice: a neurobehavioral model of autism. Biol. Psychiatry 2011, 69:875-882.
40. Rilling J.K., Demarco A.C., Hackett P.D., Chen X., Gautam P., Stair S., Haroon E., Thompson R., Ditzen B., Patel R., Pagnoni G. Sex differences in the neural and behavioral response to intranasal oxytocin and vasopressin during human social interaction. Psychoneuroendocrinology 2014, 39:237-248.
41. Chini B., Leonzino M., Braida D., Sala M. Learning about oxytocin: pharmacologic and behavioral issues. Biol. Psychiatry 2014, 76:360-366.
42. Laszlo K., Toth K., Kertes E., Peczely L., Ollmann T., Lenard L. Effects of neurotensin in amygdaloid spatial learning mechanisms. Behav. Brain Res. 2010, 210:280-283.
43. Jirikowski G.F. Oxytocinergic neuronal systems during mating pregnancy, parturition, and lactation. Ann. N. Y. Acad. Sci. 1992, 652:253-270.
44. Oldenburger W.P., Everitt B.J., de Jonge F.H. Conditioned place preference induced by sexual interaction in female rats. Horm. Behav. 1992, 26:214-228.
45. Liberzon I., Trujillo K.A., Akil H., Young E.A. Motivational properties of oxytocin in the conditioned place preference paradigm. Neuropsychopharmacology 1997, 17:353-359.
46. Baskerville T.A., Allard J., Wayman C., Douglas A.J. Dopamine-oxytocin interactions in penile erection. Eur. J. Neurosci. 2009, 30:2151-2164.
47. 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.
48. Fallon J.H., Koziell D.A., Moore R.Y. Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J. Comp. Neurol. 1978, 180:509-532.
49. 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.
50. Succu S., Sanna F., Argiolas A., Melis M.R. Oxytocin injected into the hippocampal ventral subiculum induces penile erection in male rats by increasing glutamatergic neurotransmission in the ventral tegmental area. Neuropharmacology 2011, 61:181-188.
51. Fibiger H.C., Phillips A.G. Mesocorticolimbic dopamine systems and reward. Ann. N.Y. Acad. Sci. 1988, 537:206-215.
52. Baracz S.J., Cornish J.L. Oxytocin modulates dopamine-mediated reward in the rat subthalamic nucleus. Horm. Behav. 2013, 63:370-375.
53. 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.
54. McGregor I.S., Bowen M.T. Breaking the loop: oxytocin as a potential treatment for drug addiction. Horm. Behav. 2012, 61:331-339.
55. Moaddab M., Hyland B.I., Brown C.H. Oxytocin enhances the expression of morphine-induced conditioned place preference in rats. Psychoneuroendocrinology 2015, 53:159-169.
56. Viviani D., Charlet A., van den Burg E., Robinet C., Hurni N., Abatis M., Magara F., Stoop R. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 2011, 333:104-107.