Role of the oxytocin system in amygdala subregions in the regulation of social interest in male and female rats

Neuroscience

Volumn 330, Issue , 2016, Pages 138-149

  Dumais, Kelly M ^a   Alonso, Andrea G ^a   Bredewold, Remco ^a   Veenema, Alexa H ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

Central amygdala; Medial amygdala; Oxytocin; Oxytocin receptor; Sex differences; Social interest

Indexed keywords

OXYTOCIN RECEPTOR; OXYTOCIN; OXYTOCIN RECEPTOR, RAT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; CORRELATIONAL STUDY; ELEVATED PLUS MAZE TEST; ESTRUS; EXTRACELLULAR SPACE; FEMALE; IN VIVO STUDY; MALE; MEDIAL AMYGDALA; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; RECEPTOR BLOCKING; REGULATORY MECHANISM; SEX DIFFERENCE; SOCIAL INTERACTION; AGONISTS; AMYGDALA; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ESTRUS CYCLE; EXPLORATORY BEHAVIOR; INDWELLING CATHETER; METABOLISM; PHYSIOLOGY; RANDOMIZATION; SEXUAL DEVELOPMENT; SOCIAL BEHAVIOR; WISTAR RAT;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CATHETERS, INDWELLING; ESTROUS CYCLE; EXPLORATORY BEHAVIOR; FEMALE; MALE; MICRODIALYSIS; OXYTOCIN; RANDOM ALLOCATION; RATS, WISTAR; RECEPTORS, OXYTOCIN; SEX CHARACTERISTICS; SOCIAL BEHAVIOR;

EID: 84973495183     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.05.036     Document Type: Article

References (71)

1. Arakawa H., Arakawa K., Deak T. Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor. Neuroscience 2010, 171(4):1141-1151.
2. 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.
3. Balleine B.W., Killcross S. Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 2006, 29(5):272-279.
4. Baron-Cohen S., Ring H.A., Bullmore E.T., Wheelwright S., Ashwin C., Williams S.C. The amygdala theory of autism. Neurosci Biobehav Rev 2000, 24(3):355-364.
5. Bergan J.F., Ben-Shaul Y., Dulac C. Sex-specific processing of social cues in the medial amygdala. Elife 2014, 10.7554/eLife. 02743.
6. Bertsch K., Gamer M., Schmidt B., Schmidinger I., Walther S., Kastel T., Schnell K., Buchel C., Domes G., Herpertz S.C. Oxytocin and reduction of social threat hypersensitivity in women with borderline personality disorder. Am J Psychiatry 2013, 170(10):1169-1177.
7. Bluthe R.M., Dantzer R. Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res 1990, 535(2):301-304.
8. Bosch O.J., Meddle S.L., Beiderbeck D.I., Douglas A.J., Neumann I.D. Brain oxytocin correlates with maternal aggression: link to anxiety. J Neurosci 2005, 25(29):6807-6815.
9. Bredewold R., Smith C.J., Dumais K.M., Veenema A.H. Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context. Front Behav Neurosci 2014, 8(216):1-11.
10. Brühl A.B., Delsignore A., Komossa K., Weidt S. Neuroimaging in social anxiety disorder - a meta-analytic review resulting in a new neurofunctional model. Neurosci Behav Rev 2014, 47:260-280.
11. 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.
12. Consiglio A.R., Borsoi A., Pereira G.A., Lucion A.B. Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol Behav 2005, 85(3):354-362.
13. Domes G., Heinrichs M., Glascher J., Buchel C., Braus D., Herpertz S. Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 2007, 62(10):1187-1190.
14. Domes G., Lischke A., Berger C., Grossman A., Hauenstein K., Heinrichs M., Herpertz S.C. Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 2010, 35(1):83-93.
15. Domes G., Heinrichs M., Kumbier E., Grossmann A., Hauenstein K., Herpertz S.C. Effects of intranasal oxytocin on the neural basis of face processing in autism spectrum disorder. Biol Psychiatry 2013, 74(3):164-171.
16. Donegan N.H., Sanislow C.A., Blumberg H.P., Filbright R.K., Lacadie C., Skudlarski P., Gore J.C., Olson I.R., McGlashan T.H., Wexler B.E. Amygdala hyperreactivity in borderline personality disorder: implications for emotional dysregulation. Biol Psychiatry 2003, 54(11):1284-1293.
17. Dong H.W., Petrovich G.D., Swanson L.W. Topography of projections from amygdala to bed nucleus of the stria terminalis. Brain Res Rev 2001, 38(1-2):192-246.
18. 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, 40:1-23.
19. Dumais K.M., Veenema A.H. Presence and absence of sex differences in structure and function of the brain oxytocin system: implications for understanding social behavior. Sex differences in the central nervous system 2016, 247-284. Elsevier. R. Shansky, J. Johnson (Eds.).
20. Dumais K.M., Bredewold R., Mayer T.E., Veenema A.H. Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region- and sex- specific ways. Horm Behav 2013, 64(4):693-701.
21. Dumais K.M., Alonso A.G., Immormino M.A., Bredewold R., Veenema A.H. Involvement of the oxytocin system in the bed nucleus of the stria terminalis in the sex-specific regulation of social recognition. Psychoneuroendocrinology 2016, 64:79-88.
22. Evans K.C., Wright C.I., Wedig M.M., Gold A.L., Pollack M.H., Rauch S.L. A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder. Depress Anxiety 2008, 25(6):496-505.
23. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 2001, 21(20):8278-8285.
24. Gimpl G., Fahrenholz F. The oxytocin receptor system: Structure, function, and regulation. Physiol Rev 2001, 81(2):630-683.
25. Goldin P.R., Manber-Ball T., Werner K., Heimberg R., Gross J.J. Neural mechanisms of cognitive reappraisal of negative self-beliefs in social anxiety disorder. Biol Psychiatry 2009, 66(12):1091-1099.
26. Goldman J.M., Murr A.S., Cooper R.L. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol 2007, 80:84-97.
27. Guastella A.J., MacLeod C. A critical review of the influence of oxytocin nasal spray on social cognition in humans: evidence and future directions. Horm Behav 2012, 61(3):410-418.
28. Guthman E.M., Vera J. A cellular mechanism for main and accessory olfactory integration at the medial amygdala. J Neurosci 2016, 36(7):2083-2085.
29. Guzmán Y.F., Tronson N.C., Jovasevic V., Sato K., Guedea A.L., Mizukami H., Nishimori K., Radulovic J. Fear-enhancing effects of septal oxytocin receptors. Nat Neurosci 2013, 16(9):1185-1187.
30. Guzmán Y.F., Tronson N.C., Sato K., Mesic I., Guedea A.L., Nishimori K., Radulovic J. Role of oxytocin receptors in modulation of fear by social memory. Psychopharmacology 2014, 231(10):2097-2105.
31. Halpern M., Martinez-Marcos A. Structure and function of the vomeronasal system: an update. Prog Neurobiol 2003, 70(3):245-318.
32. Herpertz S.C., Dietrich T.M., Wenning B., Krings T., Erberich S.G., Willmes K., Thron A., Sass H. Evidence of abnormal amygdala functioning in borderline personality disorder: a functional MRI study. Biol Psychiatry 2001, 50(4):292-298.
33. Horn T.F., Engelmann M. In vivo microdialysis for nonapeptides in rat brain- a practical guide. Methods 2001, 23(1):41-53.
34. Huber D., Veinante P., Stoop R. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 2005, 308(5719):245-248.
35. Insel T.R., Hulihan T.J. A gender-specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behav Neurosci 1995, 109(4):782-789.
36. Joëls M. Modulatory actions of steroid hormones and neuropeptides on electrical activity in brain. Eur J Pharmacol 2000, 405:207-216.
37. Johnston A.L., File S.E. Sex differences in animal tests of anxiety. Physiol Behav 1991, 49:245-250.
38. Kim S.Y., Choi U.S., Park S.Y., Oh S.H., Yoon H.W., Koh Y.J., Im W.Y., Park J.I., Song D.H., Cheon K.A., Lee C.U. Abnormal activation of the social brain network in children with autism spectrum disorder: an FMRI study. Psychiatry Investig 2015, 12(1):37-45.
39. Kleinhans N.M., Richards T., Greenson J., Dawson G., Aylward E. Altered dynamics of the fMRI response to faces in individuals with autism. J Autism Dev Disord 2016, 46(1):232-241.
40. Knobloch S.H., Charlet A., Hoffmann L.C., Eliava M., Khrulev S., Cetin A.H., Osten P., Schwarz M.K., Seeburg P.H., Stoop R., Grinevich V. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 2012, 73:553-566.
41. Labuschagne I., Phan K.L., Wood A., Angstadt M., Chua P., Heinrichs M., Stout J.C., Nathan P.J. Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 2010, 35(12):2403-2413.
42. Lahoud N., Maroun M. Oxytocinergic manipulations in corticolimbic circuit differentially affect fear acquisition and extinction. Psychoneuroendocrinology 2013, 38(10):2184-2195.
43. László K., Kovacs A., Zagoracz O., Ollmann T., Peczely L., Kertes E., Lacy D.G., Lenard L. Positive reinforcing effect of oxytocin microinjection in the rat central nucleus of amygdala. Behav Brain Res 2016, 296:279-285.
44. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184.
45. Lubin D.A., Elliott J.C., Black M.C., Johns J.M. An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav Neurosci 2003, 117(2):195-201.
46. Lukas M., Toth I., Veenema A.H., Neumann I.D. Oxytocin mediates rodent social memory within the lateral septum and the medial amygdala depending on the relevance of the social stimulus: male juvenile versus female adult conspecifics. Psychoneuroendocrinology 2013, 38(6):916-926.
47. Manning M., Kruszynski M., Bankowski K., Olma A., Lammek B., Cheng L.L., Klis W.A., Seto J., Haldar J., Sawyer W.H. Solid-phase synthesis of 16 potent (selective and nonselective) in vivo antagonists of oxytocin. J Med Chem 1989, 32(2):382-391.
48. 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.
49. Murakami G., Hunter R.G., Fontaine C., Ribeiro A., Pfaff D. Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice. Eur J Neurosci 2011, 34(3):469-477.
50. Neumann I.D., Torner L., Wigger A. Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience 2000, 95(2):567-575.
51. Noack J., Murau R., Engelmann M. Consequences of temporary inhibition of the medial amygdala on social recognition memory performance in mice. Front Neurosci 2015, 9(15). 10.3389/fnins.2015.00152.
52. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. 4th ed.
53. Petrovich G.D., Swanson L.W. Projections from the lateral part of the central amygdalar nucleus to the postulated fear conditioning circuit. Brain Res 1997, 763(2):247-254.
54. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Rev 2001, 38(1-2):247-289.
55. Qiu F., Qiu C.Y., Cai H., Liu T.T., Qu Z.W., Yang Z., Li J.D., Zhou Q.Y., Hu W.P. Oxytocin inhibits the activity of acid-sensing ion channels through the vasopressin, V1A receptor in primary sensory neurons. Br J Pharmacol 2014, 171(12):3065-3076.
56. Ramos L., Hicks C., Kevin R., Caminer A., Narlawar R., Kassiou M., McGregor I.S. Acute prosocial effects of oxytocin and vasopressin when given alone or in combination with 3,4-methylenedioxymethamphetamine in rats: involvement of the V1A receptor. Neuropsychopharmacology 2013, 38(11):2249-2259.
57. Rilling J.K., DeMarco A.C., Hackett P.D., Thompson R., Ditzen B., Patel R., Pagnoni G. Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology 2012, 37(4):447-461.
58. 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.
59. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 2009, 30:534-547.
60. 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. Pharmacological 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(9):875-882.
61. Schorscher-Petcu A., Sotocinal S., Ciura S., Dupre A., Ritchie J., Sorge R.E., Crawley J.N., Hu S.B., Nishimori K., Young L.J., Tribollet E., Quirion R., Mogil J.S. Oxytocin-induced analgesia and scratching are mediated by the vasopressin-1A receptor in the mouse. J Neurosci 2010, 30(24):8274-8284.
62. Slattery D.A., Neumann I.D. Chronic icv oxytocin attenuates the pathological high anxiety state of selectively bred Wistar rats. Neuropharmacology 2010, 58(1):56-61.
63. Song Z., McCann K.E., McNeill J.K., Larkin T.E., Huhman K.L., Albers H.E. Oxytocin induces social communication by activating arginine-vasopressin V1a receptors and not oxytocin receptors. Psychoneuroendocrinology 2014, 50:14-19.
64. Stefanova N. Gamma-aminobutyric acid-immunoreactive neurons in the amygdala of the rat - sex differences and effect of early postnatal castration. Neurosci Lett 1998, 255(3):175-177.
65. Thor D.H. Testosterone and persistence of social investigation in laboratory rats. J Comp Physiol Psychol 1980, 94(5):970-976.
66. Varlinskaya E.I., Vogt B.A., Spear L.P. Social context induces two unique patterns of c-Fos expression in adolescent and adult rats. Dev Psychobiol 2013, 55(7):684-697.
67. Veenema A.H., Neumann I.D. Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res 2008, 170:260-276.
68. Viviani D., Stoop R. Opposite effects of oxytocin and vasopressin on the emotional expression of the fear response. Prog Brain Res 2008, 170:207-218.
69. 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(6038):104-107.
70. Wallace D.M., Magnuson D.J., Gray T.S. Organization of amygdaloid projections to brainstem dopamine, noradrenergic, and adrenergic cell groups in the rat. Brain Res Bull 1992, 28(3):447-454.
71. Zahm D.S., Jensen S.L., Williams E.S., Martin J.R. Direct comparison of projections from the central amygdaloid region and nucleus accumbens shell. Eur J Neurosci 1999, 11(4):1119-1126.