title: VPAC receptor signaling modulates grouping behavior and social responses to contextual novelty in a gregarious finch: a role for a putative prefrontal cortex homologue.
abstract: In both mammals and birds, vasoactive intestinal polypeptide (VIP) neurons and fibers are present in virtually every brain area that is important for social behavior. VIP influences aggression in birds, social recognition in rodents, and prolactin secretion in both taxa, but other possible functions in social modulation remain little explored. VIP effects are mediated by VPAC receptors, which bind both VIP and pituitary adenylate cyclase activating peptide. Within the lateral septum and medial bed nucleus of the stria terminalis, VPAC receptors are found at higher densities in gregarious finch species relative to territorial species, suggesting that VPAC receptor activation promotes social contact and/or preference for larger groups. Here we here test this hypothesis in zebra finches (Taeniopygia guttata), and also examine the relevance of VPAC receptors to anxiety-like processes. Intraventricular infusions of the VPAC receptor antagonist, neurotensin6-11 mouseVIP7-28, strongly reduce social contact when animals are tested in a novel environment, and exert sex-specific effects on grouping behavior. Specifically, VPAC receptor antagonism reduces gregariousness in females but increases gregariousness in males. Interestingly, VPAC antagonism in the medial pallium (putative prefrontal cortex homologue) significantly reduces gregariousness in both sexes, suggesting site-specific effects of VIP signaling. However, VPAC antagonism does not modulate novel-familiar social preferences in a familiar environment or general anxiety-like behaviors. The current results suggest that endogenous activation of VPAC receptors promotes social contact under novel environmental conditions, a function that may be accentuated in gregarious species. Moreover, endogenous VIP modulates gregariousness in both males and females.
authors.affiliation: Department of Biology, Indiana University, 1001 East Third Street, Bloomington, IN 47405, USA. Electronic address: mk24@indiana.edu.
authors.forename: Marcy A
authors.initials: MA
authors.lastname: Kingsbury
authors.forename: Katherine M
authors.initials: KM
authors.lastname: Miller
authors.forename: James L
authors.initials: JL
authors.lastname: Goodson
mesh_terms: D000818:Animals; D001007:Anxiety / Q000503:physiopathology; D001522:Behavior, Animal / Q000187:drug effects / Q000502:physiology*; D004777:Environment; D005106:Exploratory Behavior / Q000187:drug effects / Q000502:physiology*; D005260:Female; D046369:Finches / Q000502:physiology*; D008297:Male; D009496:Neurotensin / Q000494:pharmacology*; D017397:Prefrontal Cortex / Q000187:drug effects* / Q000502:physiology; D018005:Receptors, Vasoactive Intestinal Peptide / Q000037:antagonists & inhibitors / Q000502:physiology*; D011993:Recombinant Fusion Proteins / Q000494:pharmacology; D015398:Signal Transduction / Q000187:drug effects / Q000502:physiology; D012919:Social Behavior; D014660:Vasoactive Intestinal Peptide / Q000031:analogs & derivatives / Q000037:antagonists & inhibitors / Q000494:pharmacology*
chemical_list: D018005:Receptors, Vasoactive Intestinal Peptide; D011993:Recombinant Fusion Proteins; C069189:(VIP-neurotensin) hybrid antagonist; D014660:Vasoactive Intestinal Peptide; D009496:Neurotensin
keywords: Affiliation; Anxiety-like behavior; Gregariousness; Social approach; Vasoactive intestinal polypeptide; Zebra finches
references.citation: Ann N Y Acad Sci. 1999 Jun 29;877:242-57
references.pmid: 10415653
references.citation: Brain Behav Evol. 1997;49(2):78-98
references.pmid: 9031732
references.citation: Brain Behav Evol. 1995;45(3):153-77
references.pmid: 7796094
references.citation: Endocrinology. 2008 Jun;149(6):3130-6
references.pmid: 18326000
references.citation: J Comp Neurol. 2004 Aug 30;476(4):388-413
references.pmid: 15282712
references.citation: Brain Res. 2011 Nov 8;1422:20-31
references.pmid: 21974861
references.citation: Brain Res. 1980 Mar 17;186(1):165-83
references.pmid: 6986955
references.citation: Br J Pharmacol. 2012 May;166(1):4-17
references.pmid: 22289055
references.citation: Gen Comp Endocrinol. 1996 Oct;104(1):76-83
references.pmid: 8921358
references.citation: Neuroscience. 1982 Jan;7(1):99-131
references.pmid: 6176906
references.citation: Gen Comp Endocrinol. 1999 Jan;113(1):146-54
references.pmid: 9882553
references.citation: Horm Behav. 2005 Aug;48(2):196-206
references.pmid: 15878570
references.citation: Proc Natl Acad Sci U S A. 2006 Nov 7;103(45):17013-7
references.pmid: 17071744
references.citation: Horm Behav. 2012 Mar;61(3):239-50
references.pmid: 22269661
references.citation: J Comp Neurol. 2004 Jul 26;475(3):426-61
references.pmid: 15221956
references.citation: Brain Res Mol Brain Res. 2001 Aug 15;92(1-2):78-84
references.pmid: 11483244
references.citation: Pharmacol Rev. 2000 Jun;52(2):269-324
references.pmid: 10835102
references.citation: Horm Behav. 1990 Jun;24(2):215-31
references.pmid: 2194925
references.citation: Psychoneuroendocrinology. 2009 Jul;34(6):833-43
references.pmid: 19181454
references.citation: J Comp Neurol. 1991 Mar 15;305(3):393-411
references.pmid: 1645376
references.citation: Gen Comp Endocrinol. 1998 Aug;111(2):233-44
references.pmid: 9679095
references.citation: J Mol Neurosci. 1989;1(1):55-61
references.pmid: 2642065
references.citation: J Neurosci. 2002 Nov 15;22(22):10046-52
references.pmid: 12427862
references.citation: Horm Behav. 1998 Aug;34(1):67-77
references.pmid: 9735230
references.citation: Gen Comp Endocrinol. 1999 Mar;113(3):323-30
references.pmid: 10068494
references.citation: J Mol Neurosci. 2007;31(3):183-200
references.pmid: 17726225
references.citation: J Comp Neurol. 1996 Dec 02;376(1):1-27
references.pmid: 8946281
references.citation: J Neurosci. 2004 Oct 6;24(40):8786-95
references.pmid: 15470144
references.citation: Physiol Behav. 2010 Aug 4;101(1):141-52
references.pmid: 20451539
references.citation: Horm Behav. 2007 Nov;52(4):445-53
references.pmid: 17678929
references.citation: Horm Behav. 2008 Jan;53(1):287-94
references.pmid: 18036596
references.citation: Neurosci Biobehav Rev. 2005 Feb;29(1):137-50
references.pmid: 15652261
references.citation: Am Nat. 2007 Dec;170(6):864-75
references.pmid: 18171169
references.citation: Cell Tissue Res. 1994 Jan;275(1):91-107
references.pmid: 8118850
references.citation: J Comp Neurol. 1991 Dec 15;314(3):478-92
references.pmid: 1726107
references.citation: Neuropsychopharmacology. 2009 Oct;34(11):2459-68
references.pmid: 19553916
references.citation: Acta Histochem. 2013 Apr;115(3):209-18
references.pmid: 22795268
references.citation: Eur J Neurosci. 2008 Sep;28(5):883-92
references.pmid: 18717734
references.citation: Science. 2009 Aug 14;325(5942):862-6
references.pmid: 19679811
references.citation: PLoS One. 2010 Jul 14;5(7):e11597
references.pmid: 20644737
references.citation: J Endocrinol. 1981 Sep;90(3):437-43
references.pmid: 7276801
references.citation: Neurosci Lett. 2003 Feb 27;338(2):155-8
references.pmid: 12566176
references.citation: Gen Comp Endocrinol. 1988 Nov;72(2):226-36
references.pmid: 3197943
references.citation: Proc Natl Acad Sci U S A. 2012 Aug 21;109(34):13847-52
references.pmid: 22872869
references.citation: Behav Neurosci. 2001 Aug;115(4):910-9
references.pmid: 11508730
references.citation: Horm Behav. 2012 Mar;61(3):454-61
references.pmid: 22300676
references.citation: Horm Behav. 2009 Jan;55(1):197-202
references.pmid: 19013174
references.citation: Int J Dev Neurosci. 2008 Aug;26(5):423-34
references.pmid: 18423945
references.citation: Pharmacol Rev. 2009 Sep;61(3):283-357
references.pmid: 19805477
references.citation: J Neuroendocrinol. 1999 Jan;11(1):19-25
references.pmid: 9918225
references.citation: Behav Brain Res. 1992 Nov 15;51(2):149-55
references.pmid: 1466781
references.citation: Exp Neurol. 2007 Jul;206(1):101-13
references.pmid: 17521630
references.citation: Science. 2011 Jul 15;333(6040):353-7
references.pmid: 21764750
references.citation: Behav Neurosci. 2009 Oct;123(5):979-91
references.pmid: 19824764
references.citation: Anim Cogn. 2010 Sep;13(5):701-10
references.pmid: 20300791
references.citation: Gen Comp Endocrinol. 2008 Jun;157(2):91-8
references.pmid: 18555065
references.citation: Proc Natl Acad Sci U S A. 2012 Jun 26;109 Suppl 1:10685-92
references.pmid: 22723363
references.citation: J Mol Neurosci. 2003 Apr;20(2):163-72
references.pmid: 12794310
references.citation: J Comp Neurol. 2003 May 5;459(3):301-26
references.pmid: 12655512
references.citation: J Comp Neurol. 1987 Sep 8;263(2):290-307
references.pmid: 3312309
references.citation: Exp Neurol. 2008 May;211(1):67-84
references.pmid: 18316078
references.citation: Gen Comp Endocrinol. 1986 Jun;62(3):470-8
references.pmid: 3770438
references.citation: J Neuroendocrinol. 2007 Aug;19(8):605-13
references.pmid: 17620102
references.citation: J Exp Zool. 1984 Dec;232(3):521-9
references.pmid: 6240524
references.citation: J Comp Neurol. 1997 Apr 28;381(1):101-18
references.pmid: 9087422
references.citation: Horm Behav. 2001 Sep;40(2):133-8
references.pmid: 11534973
references.citation: J Comp Neurol. 2011 May 1;519(7):1371-94
references.pmid: 21452202
references.citation: Horm Behav. 2006 Aug;50(2):223-36
references.pmid: 16643915
references.citation: Horm Behav. 1983 Mar;17(1):54-65
references.pmid: 6862393
references.citation: Endocrinology. 1992 Apr;130(4):1796-801
references.pmid: 1547709
references.citation: Regul Pept. 1995 Nov 10;59(3):321-33
references.pmid: 8577937
references.citation: Prog Neurobiol. 1998 Mar;54(4):417-58
references.pmid: 9522395
references.citation: Horm Behav. 2011 Jun;60(1):12-21
references.pmid: 21295577
references.citation: Horm Behav. 2005 Jun;48(1):11-22
references.pmid: 15885690
references.citation: Brain Behav Evol. 2001 May;57(5):252-70
references.pmid: 11641562
references.citation: J Comp Neurol. 1978 Jul 1;180(1):59-71
references.pmid: 649789
references.citation: Regul Pept. 1994 May 26;51(3):221-7
references.pmid: 7938706
references.citation: Behav Brain Res. 1999 Jun;101(2):129-52
references.pmid: 10372570
references.citation: Front Behav Neurosci. 2009 Sep 15;3:25
references.pmid: 19826497
references.citation: Neuroendocrinology. 1991;53 Suppl 1:45-51
references.pmid: 1901391
references.citation: Behav Neurosci. 1989 Oct;103(5):1009-16
references.pmid: 2803548