Local oxytocin tempers anxiety by activating GABAA receptors in the hypothalamic paraventricular nucleus

Psychoneuroendocrinology

Volumn 63, Issue , 2016, Pages 50-58

  Smith, Adam S ^a   Tabbaa, Manal ^a   Lei, Kelly ^a   Eastham, Patrick ^a   Butler, Michael J ^a   Linton, Latanya ^a   Altshuler, Randy ^a   Liu, Yan ^a   Wang, Zuoxin ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Corticotrophinreleasing hormone; GABA; Hypothalamic pituitary adrenal axis; Oxytocin; Prairie vole; Retrodialysis

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; BIOLOGICAL MARKER; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; OXYTOCIN; PROTEIN C FOS; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; OXYTOCIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR CHANGE; BRAIN NERVE CELL; CELL ACTIVITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; FEMALE; HORMONE RELEASE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN VIVO STUDY; MICROTUS OCHROGASTER; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ANIMAL BEHAVIOR; ARVICOLINAE; DRUG EFFECTS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOHISTOCHEMISTRY; METABOLISM; MICRODIALYSIS;

ANIMALS; ANXIETY; ARVICOLINAE; BEHAVIOR, ANIMAL; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; FEMALE; GABA-A RECEPTOR AGONISTS; GABA-A RECEPTOR ANTAGONISTS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; IMMUNOHISTOCHEMISTRY; MICRODIALYSIS; OXYTOCICS; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, GABA-A;

EID: 84949786118     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.09.017     Document Type: Article

References (52)

1. Armario A. The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors?. CNS Neurol. Disord. 2006, 5:485-501.
2. Bali B., Kovacs K.J. GABAergic control of neuropeptide gene expression in parvocellular neurons of the hypothalamic paraventricular nucleus. Eur. J. Neurosci. 2003, 18:1518-1526.
3. Bartanusz V., Muller D., Gaillard R.C., Streit P., Vutskits L., Kiss J.Z. Local gamma-aminobutyric acid and glutamate circuit control of hypophyseotrophic corticotropin-releasing factor neuron activity in the paraventricular nucleus of the hypothalamus. Eur. J. Neurosci. 2004, 19:777-782.
4. Blume A., Bosch O.J., Miklos S., Luz T., Wales L., Waldherr M., Neumann I.D. Oxytocin reduces anxiety via ERK1/2 activation: Local effect within the rat hypothalamic paraventricular nucleus. Eur. J. Neurosci. 2008, 27:1947-1956.
5. Bosch O.J., Krömer S.A., Brunton P.J., Neumann I.D. Release of oxytocin in the hypothalamic paraventricular nucleus, but not central amygdala or lateral septum in lactating residents and virgin intruders during maternal defence. Neuroscience 2004, 124:439-448.
6. 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, 25:6807-6815.
7. Bowen M.T., Peters S.T., Absalom N., Chebib M., Neumann I.D., McGregor I.S. Oxytocin prevents ethanol actions at delta subunit-containing GABAA receptors and attenuates ethanol-induced motor impairment in rats. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:3104-3109.
8. Brussaard A.B., Kits K.S., de Vlieger T.A. Postsynaptic mechanism of depression of GABAergic synapses by oxytocin in the supraoptic nucleus of immature rat. J. Physiol. 1996, 497:495-507.
9. A receptors in rats. Brain Res. 2011, 1387:39-45.
10. Churchland P.S., Winkielman P. Modulating social behavior with oxytocin: how does it work? What does it mean?. Horm. Behav. 2012, 61:392-399.
11. Cullinan W.E. GABA(A) receptor subunit expression within hypophysiotropic CRH neurons: a dual hybridization histochemical study. J. Comp. Neurol. 2000, 419:344-351.
12. Curtis J.T., Wang Z. Ventral tegmental area involvement in pair bonding in male prairie voles. Physiol. Behav. 2005, 86:338-346.
13. Dabrowska J., Hazra R., Ahern T.H., Guo J.-D., McDonald A.J., Mascagni F., Muller J.F., Young L.J., Rainnie D.G. Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin systems in the hypothalamus and the bed nucleus of the stria terminalis of the rat: Implications for balancing stress and affect. Psychoneuroendocrinology 2011, 36:1312-1326.
14. Decavel C., Van den Pol A.N. GABA: a dominant neurotransmitter in the hypothalamus. J. Comp. Neurol. 1990, 302:1019-1037.
15. Depino A.M., Tsetsenis T., Gross C. GABA homeostasis contributes to the developmental programming of anxiety-related behavior. Brain Res. 2008, 1210:189-199.
16. Detillion C.E., Craft T.K.S., Glasper E.R., Prendergast B.J., DeVries A.C. Social facilitation of wound healing. Psychoneuroendocrinology 2004, 29:1004-1011.
17. Ebner K., Bosch O.J., Kromer S.A., Singewald N., Neumann I.D. Release of oxytocin in the rat central amygdala modulates stress-coping behaviour and the release of excitatory amino acids. Neuropsychopharmacology 2005, 30:223-230.
18. Engelmann M., Ludwig M., Landgraf R. Microdialysis administration of vasopressin and vasopressin antagonists into the septum during pole-jumping behavior in rats. Behav. Neural. Biol. 1992, 58:51-57.
19. Gobrogge K.L., Liu Y., Jia X., Wang Z. Anterior hypothalamic neural activation and neurochemical associations with aggression in pair-bonded male prairie voles. J. Comp. Neurol. 2007, 502:1109-1122.
20. Griebel G., Belzung C., Perrault G., Sanger D.J. Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice. Psychopharmacology (Berl) 2000, 148:164-170.
21. Heinrichs M., Baumgartner T., Kirschbaum C., Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol. Psychiatry 2003, 54:1389-1398.
22. Hendrie C.A., Eilam D., Weiss S.M. Effects of diazepam and buspirone on the behaviour of wild voles (Microtus socialis) in two models of anxiety. Pharmacol. Biochem. Behav. 1997, 58:573-576.
23. Herman J.P., Tasker J.G., Ziegler D.R., Cullinan W.E. Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol. Biochem. Behav. 2002, 71:457-468.
24. Hillhouse E.W., Milton N.G. Effect of noradrenaline and gamma-aminobutyric acid on the secretion of corticotrophin-releasing factor-41 and arginine vasopressin from the rat hypothalamus in vitro. J. Endocrinol. 1989, 122:719-723.
25. Israel J.M., Poulain D.A., Oliet S.H. Oxytocin-induced postinhibitory rebound firing facilitates bursting activity in oxytocin neurons. J. Neurosci. 2008, 28:385-394.
26. Jurek B., Slattery D.A., Hiraoka Y., Liu Y., Nishimori K., Aguilera G., Neumann I.D., Burg v.d E.H. Oxytocin regulates stress-induced Crf gene transcription through CREB-regulated transcription coactivator 3. J. Neurosci. 2015, 35:12248-12260.
27. Jurek B., Slattery D.A., Maloumby R., Hillerer K., Koszinowski S., Neumann I.D., van den Burg E.H. Differential contribution of hypothalamic MAPK activity to anxiety-like behaviour in virgin and lactating rats. PLoS One 2012, 7:e37060.
28. Kajantie E., Phillips D.I.W. The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 2006, 31:151-178.
29. Lin E.J. Neuropeptides as therapeutic targets in anxiety disorders. Curr. Pharm. Des. 2012, 8:5709-5727.
30. Ludwig M., Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 2006, 7:126-136.
31. Marques de Souza L., Franci C.R. GABAergic mediation of stress-induced secretion of corticosterone and oxytocin, but not prolactin, by the hypothalamic paraventricular nucleus. Life Sci. 2008, 83:686-692.
32. Miklos I.H., Kovacs K.J. GABAergic innervation of corticotropin-releasing hormone (CRH)-secreting parvocellular neurons and its plasticity as demonstrated by quantitative immunoelectron microscopy. Neuroscience 2002, 113:581-592.
33. Moos F., Freund-Mercier M.J., Guerne Y., Guerne J.M., Stoeckel M.E., Richard P. Release of oxytocin and vasopressin by magnocellular nuclei in vitro: Specific facilitatory effect of oxytocin on its own release. J. Endocrinol. 1984, 102:63-72.
34. Neumann I.D., Ludwig M., Engelmann M., Pittman Q.J., RL Simultaneous microdialysis in blood and brain: Oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology 1993, 58:637-645.
35. Neumann I.D., Wigger A., Torner L., Holsboer F., Landgraf R. Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: Partial action within the paraventricular nucleus. J. Neuroendocrinol. 2000, 12:235-243.
36. Nishioka T., Anselmo-Franci J.A., Li P., Callahan M.F., Morris M. Stress increases oxytocin release within the hypothalamic paraventricular nucleus. Brain Res. 1998, 781:57-61.
37. Ontjes D.A., Ways D.K., Mahaffee D.D., Zimmerman C.F., Gwynne J.T. Part IV. ACTH action II. ACTH action on the adrenal cortex ACTH receptors and the effect of ACTH on adrenal organelles. Ann. N. Y. Acad. Sci. 1977, 297:295-312.
38. Petersson M., Hulting A.-L., Uvnäs-Moberg K. Oxytocin causes a sustained decrease in plasma levels of corticosterone in rats. Neurosci. Lett. 1999, 264:41-44.
39. Plotsky P.M., Otto S., Sutton S. Neurotransmitter modulation of corticotropin releasing factor secretion into the hypophysial-portal circulation. Life Sci. 1987, 41:1311-1317.
40. Pritchett D.B., Seeburg P.H. Gamma-aminobutyric acidA receptor alpha 5-subunit creates novel type II benzodiazepine receptor pharmacology. J. Neurochem. 1990, 54:1802-1804.
41. Roberts R.L., Wolf K.N., Sprangel M.E., Rall W.F., Wildt D.E. Prolonged mating in prairie voles (Microtus ochrogaster) increases likelihood of ovulation and embryo number. Biol. Reprod. 1999, 60:756-762.
42. Russell J.A., Neumann I., Landgraf R. Oxytocin and vasopressin release in discrete brain areas after naloxone in morphine-tolerant and -dependent anesthetized rats: push-pull perfusion study. J. Neurosci. 1992, 12:1024-1032.
43. Smith A.S., Wang Z. Salubrious effects of oxytocin on social stress-induced deficits. Horm. Behav. 2012, 61:320-330.
44. Smith A.S., Wang Z. Hypothalamic oxytocin mediates social buffering of the stress response. Biol. Psychiatry 2014, 76:281-288.
45. Tasker J.G., Dudek F.E. Local inhibitory synaptic inputs to neurones of the paraventricular nucleus in slices of rat hypothalamus. J. Physiol. 1993, 469:179-192.
46. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
47. Veenema A.H., Bredewold R., Neumann I.D. Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: Link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 2007, 32:437-450.
48. Waldherr M., Neumann I.D. Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16681-16684.
49. Windle R.J., Kershaw Y.M., Shanks N., Wood S.A., Lightman S.L., Ingram C.D. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J. Neurosci. 2004, 24:2974-2982.
50. Windle R.J., Shanks N., Lightman S.L., Ingram C.D. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 1997, 138:2829-2834.
51. Wotjak C.T., Ganster J., Kohl G., Holsboer F., Landgraf R., Engelmann M. Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: New insights into the secretory capacities of peptidergic neurons. Neuroscience 1998, 85:1209-1222.
52. Zahner M.R., Li D.P., Pan H.L. Benzodiazepine inhibits hypothalamic presympathetic neurons by potentiation of GABAergic synaptic input. Neuropharmacology 2007, 52:467-475.