PAC1 receptor antagonism in the bed nucleus of the stria terminalis (BNST) attenuates the endocrine and behavioral consequences of chronic stress

Psychoneuroendocrinology

Volumn 47, Issue , 2014, Pages 151-165

  Roman, Carolyn W ^a   Lezak, Kim R ^b   Hartsock, Matthew J ^b   Falls, William A ^b   Braas, Karen M ^a   Howard, Alan B ^c   Hammack, Sayamwong E ^b   May, Victor ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

^c Department of Mathematics and Statistics University of Vermont ^*  (United States)

Author keywords

Anxiety related behavior; Bed nucleus of the stria terminalis (BNST); Chronic variate stress; Hypothalamic pituitary adrenal (HPA) axis; PAC1 receptor; Pituitary adenylate cyclase activating polypeptide (PACAP)

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR; PACAP(6-38); RECEPTOR BLOCKING AGENT; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1 ANTAGONIST; HORMONE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOREXIA; ANXIETY; ARTICLE; BED NUCLEUS OF THE STRIA TERMINALIS; BEHAVIOR; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE RELEASE; DRUG TARGETING; ENDOCRINE FUNCTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; STRIA TERMINALIS; WEIGHT GAIN; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; BLOOD; CHRONIC DISEASE; DRUG EFFECTS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PSYCHOLOGY; SEPTUM NUCLEUS; SPRAGUE DAWLEY RAT;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; CHRONIC DISEASE; CORTICOSTERONE; HORMONES; INFUSIONS, INTRAVENTRICULAR; MALE; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; SEPTAL NUCLEI; STRESS, PSYCHOLOGICAL;

EID: 84903748405     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.05.014     Document Type: Article

References (79)

1. Agarwal A., Halvorson L.M., Legradi G. Pituitary adenylate cyclase-activating polypeptide (PACAP) mimics neuroendocrine and behavioral manifestations of stress: evidence for PKA-mediated expression of the corticotropin-releasing hormone (CRH) gene. Brain Res. Mol. Brain Res. 2005, 138:45-57.
2. Braas K.M., May V. Pituitary adenylate cyclase-activating polypeptides directly stimulate sympathetic neuron neuropeptide Y release through PAC(1) receptor isoform activation of specific intracellular signaling pathways. J. Biol. Chem. 1999, 274:27702-27710.
3. Brandenburg C.A., May V., Braas K.M. Identification of endogenous sympathetic neuron pituitary adenylate cyclase-activating polypeptide (PACAP): depolarization regulates production and secretion through induction of multiple propeptide transcripts. J. Neurosci. 1997, 17:4045-4055.
4. Chance W.T., Thompson H., Thomas I., Fischer J.E. Anorectic and neurochemical effects of pituitary adenylate cyclase activating polypeptide in rats. Peptides 1995, 16:1511-1516.
5. Choi D.C., Nguyen M.M., Tamashiro K.L., Ma L.Y., Sakai R.R., Herman J.P. Chronic social stress in the visible burrow system modulates stress-related gene expression in the bed nucleus of the stria terminalis. Physiol. Behav. 2006, 89:301-310.
6. Choi D.C., Furay A.R., Evanson N.K., Ostrander M.M., Ulrich-Lai Y.M., Herman J.P. Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J. Neurosci. 2007, 27:2025-2034.
7. Choi D.C., Evanson N.K., Furay A.R., Ulrich-Lai Y.M., Ostrander M.M., Herman J.P. The anteroventral bed nucleus of the stria terminalis differentially regulates hypothalamic-pituitary-adrenocortical axis responses to acute and chronic stress. Endocrinology 2008, 149:818-826.
8. Choi D.C., Furay A.R., Evanson N.K., Ulrich-Lai Y.M., Nguyen M.M., Ostrander M.M., Herman J.P. The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology 2008, 33:659-669.
9. Ciccocioppo R., Fedeli A., Economidou D., Policani F., Weiss F., Massi M. The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its reversal by nociceptin/orphanin FQ. J. Neurosci. 2003, 23:9445-9451.
10. Day H.E., Curran E.J., Watson S.J.J., Akil H. Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: evidence for their selective activation by interleukin-1beta. J. Comp. Neurol. 1999, 413:113-128.
11. Dong H.W., Petrovich G.D., Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 2001, 38:192-246.
12. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J. Comp. Neurol. 2006, 494:142-178.
13. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J. Comp. Neurol. 2006, 494:75-107.
14. Dore R., Iemolo A., Smith K.L., Wang X., Cottone P., Sabino V. CRF mediates the anxiogenic and anti-rewarding, but not the anorectic effects of PACAP. Neuropsychopharmacology 2013, 38:2160-2169.
15. Dumont E.C., Mark G.P., Mader S., Williams J.T. Self-administration enhances excitatory synaptic transmission in the bed nucleus of the stria terminalis. Nat. Neurosci. 2005, 8:413-414.
16. Fox A.S., Shelton S.E., Oakes T.R., Davidson R.J., Kalin N.H. Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS ONE 2008, 3:e2570.
17. Gagliano H., Fuentes S., Nadal R., Armario A. Previous exposure to immobilisation and repeated exposure to a novel environment demonstrate a marked dissociati on between behavioral and pituitary-adrenal responses. Behav. Brain Res. 2008, 187:239-245.
18. Gaszner B., Kormos V., Kozicz T., Hashimoto H., Reglodi D., Helyes Z. The behavioral phenotype of pituitary adenylate-cyclase activating polypeptide-deficient mice in anxiety and depression tests is accompanied by blunted c-Fos expression in the bed nucleus of the stria terminalis, central projecting Edinger-Westphal nucleus, ventral lateral septum, and dorsal raphe nucleus. Neuroscience 2012, 202:283-299.
19. Girard B.M., Lelievre V., Braas K.M., Razinia T., Vizzard M.A., Ioffe Y., El Meskini R., Ronnett G.V., Waschek J.A., May V. Noncompensation in peptide/receptor gene expression and distinct behavioral phenotypes in VIP- and PACAP-deficient mice. J. Neurochem. 2006, 99:499-513.
20. Griebel G., Simiand J., Steinberg R., Jung M., Gully D., Roger P., Geslin M., Scatton B., Maffrand J.P., Soubrié P. 4-(2-Chloro-4-methoxy-5-methylphenyl)-N-[(1S)-2-cyclopropyl-1-(3-fluoro-4-methylphenyl)ethyl]5-methyl-N-(2-propynyl)-1, 3-thiazol-2-amine hydrochloride (SSR 125543A), a potent and selective corticotrophin-releasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. J. Pharmacol. Exp. Ther. 2002, 301:333-345.
21. Hammack S.E., Cheung J., Rhodes K.M., Schutz K.C., Falls W.A., Braas K.M., May V. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 2009, 34:833-843.
22. Hammack S.E., Richey K.J., Schmid M.J., LoPresti M.L., Watkins L.R., Maier S.F. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J. Neurosci. 2002, 22:1020-1026.
23. Hammack S.E., Roman C.W., Lezak K.R., Kocho-Shellenberg M., Grimmig B., Falls W.A., Braas K., May V. Roles for pituitary adenylate cyclase-activating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J. Mol. Neurosci. 2010, 42:327-340.
24. Hannibal J. Pituitary adenylate cyclase activating peptide in the rat central nervous system: an immunocytochemical and in situ hybridization study. J. Comp. Neurol. 2002, 453:389-417.
25. Hashimoto H., Shintani N., Tanaka K., Mori W., Hirose M., Matsuda T., Sakaue M., Miyazaki J., Niwa H., Tashiro F., Yamamoto K., Koga K., Tomimoto S., Kunugi A., Suetake S., Baba A. Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc. Natl. Acad. Sci. U.S.A. 2001, 98:13355-13360.
26. Hatanaka M., Tanida M., Shintani N., Isojima Y., Kawaguchi C., Hashimoto H., Kakuda M., Haba R., Nagai K., Baba A. Lack of light-induced elevation of renal sympathetic nerve activity and plasma corticosterone levels in PACAP-deficient mice. Neurosci. Lett. 2008, 444:153-156.
27. Hattori S., Takao K., Tanda K., Toyama K., Shintani N., Baba A., Hashimoto H., Miyakawa T. Comprehensive behavioral analysis of pituitary adenylate cyclase-activating polypeptide (PACAP) knockout mice. Front. Behav. Neurosci. 2012, 6:58.
28. Hawke Z., Ivanov T.R., Bechtold D.A., Dhillon H., Lowell B.B., Luckman S.M. PACAP neurons in the hypothalamic ventromedial nucleus are targets of central leptin signaling. J. Neurosci. 2009, 29:14828-14835.
29. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:1201-1213.
30. Jennings J.H., Rizzi G., Stamatkis A.M., Ung R.L., Stuber G.D. The inhibitory circuit architecture of the lateral hypothalamus orchestrates feeding. Science 2013, 341:1517-1521.
31. Jovanovic T., Norrholm S.D., Davis J., Mercer K.B., Almli L., Nelson A., Cross D., Smith A., Ressler K.J., Bradley B. PAC1 receptor (ADCYAP1R1) genotype is associated with dark-enhanced startle in children. Mol. Psychiatry 2013, 18:742-743.
32. Ju G., Swanson L.W., Simerly R.B. Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: II. Chemoarchitecture. J. Comp. Neurol. 1989, 280:603-621.
33. Kalin N.H., Shelton S.E., Fox A.S., Oakes T.R., Davidson R.J. Brain regions associated with the expression and contextual regulation of anxiety in primates. Biol. Psychiatry 2005, 58:796-804.
34. Kalin N.H., Shelton S.E., Fox A.S., Rogers J., Oakes T.R., Davidson R.J. The serotonin transporter genotype is associated with intermediate brain phenotypes that depend on the context of eliciting stressor. Mol. Psychiatry 2008, 13:1021-1027.
35. Kocho-Schellenberg M., Lezak K.R., Harris O.M., Roelke E., Gick N., Choi I., Edwards S., Wasserman E., Toufexis D.J., Braas K.M., May V., Hammack S.E. PACAP in the BNST produces anorexia and weight loss in male and female rats. Neuropsychopharmacology 2014, 10.1038/npp.2014.8.
36. Koob G.F., Heinrichs S.C. A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Res. 1999, 848:141-152.
37. Kozicz T., Vigh S., Arimura A. Axon terminals containing PACAP- and VIP-immunoreactivity form synapses with CRF-immunoreactive neurons in the dorsolateral division of the bed nucleus of the stria terminalis in the rat. Brain Res. 1997, 767:109-119.
38. Kozicz T., Vigh S., Arimura A. The source of origin of PACAP- and VIP-immunoreactive fibers in the laterodorsal division of the bed nucleus of the stria terminalis in the rat. Brain Res. 1998, 810:211-219.
39. Krahn D.D., Gosnell B.A., Majchrzak M.J. The anorectic effects of CRH and restraint stress decrease with repeated exposures. Biol. Psychiatry 1990, 27:1094-1102.
40. Larriva-Sahd J. Histological and cytological study of the bed nuclei of the stria terminalis in adult rat. II. Oval nucleus: extrinsic inputs, cell types, neuropil, and neuronal modules. J. Comp. Neurol. 2006, 497:772-807.
41. Lezak K.R., Roelke E., Harris O., Choi I., Edwards S., Gick N., Cocchiaro G., Missig G., Roman C.W., Braas K.M., Toufexis D.J., May V., Hammack S.E. Pituitary adenylate cyclase activating polypeptide (PACAP) in the bed nucleus of the stria terminalis (BNST) increases corticosterone in male and female rats. Psychoneuroendocrinology 2014, 10.1016/j.psyneuen.2014.03.007.
42. Lee Y., Davis M. Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J. Neurosci. 1997, 17:6434-6446.
43. Lehmann M.L., Mustafa T., Eiden A.M., Herkenham M., Eiden L.E. PACAP-deficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress. Psychoneuroendocrinology 2013, 38:707-715.
44. Martí O., Armario A. Influence of regularity of exposure to chronic stress on the pattern of habituation of pituitary-adrenal hormones, prolactin and glucose. Stress 1997, 1:179-189.
45. Martí O., Martí J., Armario A. Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure. Physiol. Behav. 1994, 55:747-753.
46. Maruyama K., Miura T., Uchiyama M., Shioda S., Matsuda K. Relationship between anorexigenic action of pituitary adenylate cyclase-activating polypeptide (PACAP) and that of corticotropin-releasing hormone (CRH) in the goldfish, Carassius auratus. Peptides 2006, 27:1820-1826.
47. Mazzocchi G., Malendowicz L.K., Neri G., Andreis P.G., Ziolkowska A., Gottardo L., Nowak K.W., Nussdorfer G.G. Pituitary adenylate cyclase-activating polypeptide and PACAP receptor expression and function in the rat adrenal gland. Int. J. Mol. Med. 2002, 9:233-243.
48. Mazzocchi G., Malendowicz L.K., Rebuffat P., Gottardo L., Nussdorfer G.G. Expression and function of vasoactive intestinal peptide, pituitary adenylate cyclase-activating polypeptide, and their receptors in the human adrenal gland. J. Clin. Endocrinol. Metab. 2002, 87:2575-2580.
49. Mizuno Y., Kondo K., Terashima Y., Arima H., Murase T., Oiso Y. Anorectic effect of pituitary adenylate cyclase activating polypeptide (PACAP) in rats: lack of evidence for involvement of hypothalamic neuropeptide gene expression. J. Neuroendocrinol. 1998, 10:611-616.
50. Morita Y., Yanagida D., Shintani N., Ogita K., Nishiyama N., Tsuchida R., Hashimoto H., Baba A. Lack of trimethyltin (TMT)-induced elevation of plasma corticosterone in PACAP-deficient mice. Ann. N.Y. Acad. Sci. 2006, 1070:450-456.
51. Morley J.E., Horowitz M., Morley P.M., Flood J.F. Pituitary adenylate cyclase activating polypeptide (PACAP) reduces food intake in mice. Peptides 1992, 13:1133-1135.
52. Moro O., Lerner E.A. Maxadilan, the vasodilator from sand flies, is a specific pituitary adenylate cyclase activating peptide type I receptor agonist. J. Biol. Chem. 1997, 272:966-970.
53. Mounien L., Do Rego J.C., Bizet P., Boutelet I., Gourcerol G., Fournier A., Brabet P., Costentin J., Vaudry H., Jégou S. Pituitary adenylate cyclase-activating polypeptide inhibits food intake in mice through activation of the hypothalamic melanocortin system. Neuropsychopharmacology 2009, 34:424-435.
54. Oler J.A., Fox A.S., Shelton S.E., Christian B.T., Murali D., Oakes T.R., Davidson R.J., Kalin N.H. Serotonin transporter availability in the amygdala and bed nucleus of the stria terminalis predicts anxious temperament and brain glucose metabolic activity. J. Neurosci. 2009, 29:9961-9966.
55. Otto C., Martin M., Wolfer D.P., Lipp H.P., Maldonado R., Schutz G. Altered emotional behavior in PACAP-type-I-receptor-deficient mice. Brain Res. Mol. Brain Res. 2001, 92:78-84.
56. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2009, Academic Press, Burlington, MA. Compact 6th ed.
57. Pego J.M., Morgado P., Pinto L.G., Cerqueira J.J., Almeida O.F., Sousa N. Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur. J. Neurosci. 2008, 27:1503-1516.
58. Piggins H.D., Stamp J.A., Burns J., Rusak B., Semba K. Distribution of pituitary adenylate cyclase activating polypeptide (PACAP) immunoreactivity in the hypothalamus and extended amygdala of the rat. J. Comp. Neurol. 1996, 376:278-294.
59. Radley J.J., Sawchenko P.E. A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J. Neurosci. 2011, 31:9683-9695.
60. Ressler K.J., Mercer K.B., Bradley B., Jovanovic T., Mahan A., Kerley K., Norrholm S.D., Kilaru V., Smith A.K., Myers A.J., Ramirez M., Engel A., Hammack S.E., Toufexis D., Braas K.M., Binder E.B., May V. Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 2011, 470:492-497.
61. Roman C.W., Lezak K.R., Kocho-Schellenberg M., Garret M.A., Braas K., May V., Hammack S.E. Excitotoxic lesions of the bed nucleus of the stria terminalis (BNST) attenuate the effects of repeated stress on weight gain: evidence for the recruitment of BNST activity by repeated, but not acute, stress. Behav. Brain Res. 2012, 227:300-304.
62. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9:671-675.
63. Schulkin J., Gold P.W., McEwen B.S. Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 1998, 23:219-243.
64. Shioda S., Yada T., Nakajo S., Nakaya K., Nakai Y., Arimura A. Pituitary adenylate cyclase-activating polypeptide (PACAP): a novel regulator of vasopressin-containing neurons. Brain Res. 1997, 765:81-90.
65. Smagin G.N., Howell L.A., Redmann S.J., Ryan D.H., Harris R.B. Prevention of stress-induced weight loss by third ventricle CRF receptor antagonist. Am. J. Physiol. 1999, 276:R1461-R1468.
66. Somerville L.H., Whalen P.J., Kelley W.M. Human bed nucleus of the stria terminalis indexes hypervigilant threat monitoring. Biol. Psychiatry 2010, 68:416-424.
67. Stout S.C., Mortas P., Owens M.J., Nemeroff C.B., Moreau J. Increased corticotropin-releasing factor concentrations in the bed nucleus of the stria terminalis of anhedonic rats. Eur. J. Pharmacol. 2000, 401:39-46.
68. Straube T., Mentzel H.J., Miltner W.H. Waiting for spiders: brain activation during anticipatory anxiety in spider phobics. Neuroimage 2007, 37:1427-1436.
69. Stroth N., Eiden L.E. Stress hormone synthesis in mouse hypothalamus and adrenal gland triggered by restraint is dependent on pituitary adenylate cyclase-activating polypeptide signaling. Neuroscience 2010, 165:1025-1030.
70. Tachibana T., Saito S., Tomonaga S., Takagi T., Saito E.S., Boswell T., Furuse M. Intracerebroventricular injection of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibits feeding in chicks. Neurosci. Lett. 2003, 339:203-206.
71. Timpl P., Spanagel R., Sillaber I., Kresse A., Reul J.M., Stalla G.K., Blanquet V., Steckler T., Holsboer F., Wurst W. Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat. Genet. 1998, 19:162-166.
72. Tsukiyama N., Saida Y., Kakuda M., Shintani N., Hayata A., Morita Y., Tanida M., Tajiri M., Hazama K., Ogata K., Hashimoto H., Baba A. PACAP centrally mediates emotional stress-induced corticosterone responses in mice. Stress 2011, 14:368-375.
73. Vernikos J., Dallman M.F., Bonner C., Katzen A., Shinsako J. Pituitary-adrenal function in rats chronically exposed to cold. Endocrinology 1982, 110(2):413-420.
74. Vyas A., Bernal S., Chattarji S. Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res. 2003, 965:290-294.
75. Waddell J., Morris R.W., Bouton M.E. Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear. Behav. Neurosci. 2006, 120:324-336.
76. Walker D.L., Davis M. Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer. Brain Struct Funct. 2008, 213:29-42.
77. Walker D.L., Toufexis D.J., Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol. 2003, 463:199-216.
78. Walker D.L., Miles L.A., Davis M. Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:1291-1308.
79. Yamashita M., Takayanagi Y., Yoshida M., Nishimori K., Kusama M., Onaka T. Involvement of prolactin-releasing peptide in the activation of oxytocin neurones in response to food intake. J. Neuroendocrinol. 2013, 25:455-465.