Nesting behavior is associated with VIP expression and VIP-Fos colocalization in a network-wide manner

Hormones and Behavior

Volumn 69, Issue , 2015, Pages 68-81

  Kingsbury, Marcy A ^a   Jan, Namratha ^a   Klatt, James D ^a   Goodson, James L ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Hypothalamus; Medial amygdala; Nest building; Parental care; Periaqueductal gray; Preoptic area; Vasoactive intestinal polypeptide; Zebra finch

Indexed keywords

PROTEIN FOS; VASOACTIVE INTESTINAL POLYPEPTIDE; PROTEIN C FOS;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; CONTROLLED STUDY; FEMALE; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MEDIAL AMYGDALA; MOLECULAR CLONING; NESTING; NONHUMAN; PEPTIDE SYNTHESIS; PERIAQUEDUCTAL GRAY MATTER; PREOPTIC AREA; PREOPTIC NUCLEUS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SOCIAL BEHAVIOR; STRIA TERMINALIS; TAENIOPYGIA GUTTATA; TUBEROHYPOPHYSEAL TRACT; VENTRAL TEGMENTUM; ZONA INCERTA; ANIMAL; BRAIN; HUMAN; METABOLISM; NERVE CELL NETWORK; PHYSIOLOGY; SONGBIRD; TISSUE DISTRIBUTION;

AGGRESSION; ANIMALS; BRAIN; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NERVE NET; NESTING BEHAVIOR; PROTO-ONCOGENE PROTEINS C-FOS; SOCIAL BEHAVIOR; SONGBIRDS; TISSUE DISTRIBUTION; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84921038650     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.12.010     Document Type: Article

References (97)

1. Al Kahtane A., Chaiseha Y., El Halawani M. Dopaminergic regulation of avian prolactin gene transcription. J. Mol. Endocrinol. 2003, 31:185-196.
2. Alger S.J., Juang C., Riters L.V. Social affiliation relates to tyrosine hydroxylase immunolabeling in male and female zebra finches (Taeniopygia guttata). J. Chem. Neuroanat. 2011, 42:45-55.
3. Antonopoulos J., Papadopoulos G.C., Karamanlidis A.N., Parnavelas J.G., Dinopoulos A., Michaloudi H. VIP- and CCK-like-immunoreactive neurons in the hedgehog (Erinaceus europaeus) and sheep (Ovis aries) brain. J. Comp. Neurol. 1987, 263:290-307.
4. Aste N., Viglietti-Panzica C., Fasolo A., Panzica G.C. Mapping of neurochemical markers in quail central nervous system: VIP- and SP-like immunoreactivity. J. Chem. Neuroanat. 1995, 8:87-102.
5. Ball G.F., Balthazart J. How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior?. Horm. Behav. 2008, 53:307-311.
6. Balthazart J., Ball G.F. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front. Neuroendocrinol. 2007, 28:161-178.
7. Balthazart J., Dupiereux V., Aste N., Viglietti-Panzica C., Barrese M., Panzica G.C. Afferent and efferent connections of the sexually dimorphic medial preoptic nucleus of the male quail revealed by in vitro transport of DiI. Cell Tissue Res. 1994, 276:455-475.
8. Balthazart J., Absil P., Gerard M., Appeltants D., Ball G.F. Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J. Neurosci. 1998, 18:6512-6527.
9. Bandler R., Shipley M.T. Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?. Trends Neurosci. 1994, 17:379-389.
10. Bhatt R., Youngren O., Kang S., El Halawani M. Dopamine infusion into the third ventricle increases gene expression of hypothalamic vasoactive intestinal peptide and pituitary prolactin and luteinizing hormone beta subunit in the turkey. Gen. Comp. Endocrinol. 2003, 130:41-47.
11. Buntin J.D., Becker G.M., Ruzycki E. Facilitation of parental behavior in ring doves by systemic or intracranial injections of prolactin. Horm. Behav. 1991, 25:424-444.
12. Buntin J.D., Hnasko R.M., Zuzick P.H. Role of the ventromedial hypothalamus in prolactin-induced hyperphagia in ring doves. Physiol. Behav. 1999, 66:255-261.
13. Burke W.H., Dennison P.T. Prolactin and luteinizing hormone levels in female turkeys (Meleagris gallopavo) during a photoinduced reproductive cycle and broodiness. Gen. Comp. Endocrinol. 1980, 41:92-100.
14. Chaiseha Y., Tong Z., Youngren O.M., El Halawani M.E. Transcriptional changes in hypothalamic vasoactive intestinal peptide during a photo-induced reproductive cycle in the turkey. J. Mol. Endocrinol. 1998, 21:267-275.
15. Chaiyachet O.A., Chokchaloemwong D., Prakobsaeng N., Sartsoongnoen N., Kosonsiriluk S., Rozenboim I., El Halawani M.E., Porter T.E., Chaiseha Y. Neuroendocrine regulation of rearing behavior in the native Thai hen. Acta Histochem. 2013, 115:209-218.
16. Christensen D., Vleck C.M. Prolactin release and response to vasoactive intestinal peptide in an opportunistic breeder, the zebra finch (Taeniopygia guttata). Gen. Comp. Endocrinol. 2008, 157:91-98.
17. Christian H.C., Chapman L.P., Morris J.F. Thyrotrophin-releasing hormone, vasoactive intestinal peptide, prolactin-releasing peptide and dopamine regulation of prolactin secretion by different lactotroph morphological subtypes in the rat. J. Neuroendocrinol. 2007, 19:605-613.
18. Cloues R., Ramos C., Silver R. Vasoactive intestinal polypeptide-like immunoreactivity during reproduction in doves: influence of experience and number of offspring. Horm. Behav. 1990, 24:215-231.
19. Crawshaw L., Grahn D., Wollmuth L., Simpson L. Central nervous regulation of body temperature in vertebrates: comparative aspects. Pharmacol. Ther. 1985, 30:19-30.
20. de Ruiter A.J., Wendelaar Bonga S.E., Slijkhuis H., Baggerman B. The effect of prolactin on fanning behavior in the male three-spined stickleback, Gasterosteus aculeatus L. Gen. Comp. Endocrinol. 1986, 64:273-283.
21. De Vries G.J., Panzica G.C. Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 2006, 138:947-955.
22. De Vries G.J., Södersten P. Sex differences in the brain: the relation between structure and function. Horm. Behav. 2009, 55:589-596.
23. Deacon R.M. Assessing nest building in mice. Nat. Protoc. 2006, 1:1117-1119.
24. Domjan M., Hall S. Determinants of social proximity in Japanese quail (Coturnix coturnix japonica): male behavior. J. Comp. Psychol. 1986, 100:59-67.
25. El Halawani M. Vasoactive intestinal peptide as the avian prolactin-releasing factor. Perspectives in Avian Endocrinology 1997, 403-416. S. Harvey, R.J. Etches (Eds.).
26. El Halawani M.E., Pitts G.R., Sun S., Silsby J.L., Sivanandan V. Active immunization against vasoactive intestinal peptide prevents photo-induced prolactin secretion in turkeys. Gen. Comp. Endocrinol. 1996, 104:76-83.
27. Flannelly K.J., Kemble E.D., Blanchard D.C., Blanchard R.J. Effects of septal-forebrain lesions on maternal aggression and maternal care. Behav. Neural Biol. 1986, 45:17-30.
28. Gonzalez-Mariscal G. Neuroendocrinology of maternal behavior in the rabbit. Horm. Behav. 2001, 40:125-132.
29. Gonzalez-Mariscal G., Diaz-Sanchez V., Melo A.I., Beyer C., Rosenblatt J.S. Maternal behavior in New Zealand white rabbits: quantification of somatic events, motor patterns, and steroid plasma levels. Physiol. Behav. 1994, 55:1081-1089.
30. Gonzalez-Mariscal G., Melo A.I., Jimenez P., Beyer C., Rosenblatt J.S. Estradiol, progesterone, and prolactin regulate maternal nest-building in rabbits. J. Neuroendocrinol. 1996, 8:901-907.
31. Gonzalez-Mariscal G., Chirino R., Rosenblatt J.S., Beyer C. Forebrain implants of estradiol stimulate maternal nest-building in ovariectomized rabbits. Horm. Behav. 2005, 47:272-279.
32. Goodson J.L. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 1998, 34:67-77.
33. Goodson J.L. Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen. Comp. Endocrinol. 1998, 111:233-244.
34. Goodson J.L., Adkins-Regan E. Playback of crows of male Japanese quail elicits female phonotaxis. Condor 1997, 99:990-993.
35. Goodson J.L., Bass A.H. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Rev. 2001, 35:246-265.
36. Goodson J.L., Kingsbury M.A. What's in a name? Considerations of homologies and nomenclature for vertebrate social behavior networks. Horm. Behav. 2013, 64:103-112.
37. Goodson J.L., Wang Y. Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17013-17017.
38. Goodson J.L., Evans A.K., Wang Y. Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes. Horm. Behav. 2006, 50:223-236.
39. Goodson J.L., Kabelik D., Kelly A.M., Rinaldi J., Klatt J.D. Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:8737-8742.
40. Goodson J.L., Kelly A.M., Kingsbury M.A., Thompson R.R. An aggression-specific cell type in the anterior hypothalamus of finches. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13847-13852.
41. Goodson J.L., Wilson L.C., Schrock S.E. To flock or fight: neurochemical signatures of divergent life histories in sparrows. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(Suppl. 1):10685-10692.
42. Gorski R.A., Harlan R.E., Jacobson C.D., Shryne J.E., Southam A.M. Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J. Comp. Neurol. 1980, 193:529-539.
43. Grattan D.R., Bridges R.S. Prolactin actions in the brain. Hormones, Brain and Behavior 2009, 2471-2503. Elsevier, Oxford, UK. D.W. Pfaff (Ed.).
44. Gray P., Brooks P.J. Effect of lesion location within the medial preoptic-anterior hypothalamic continuum on maternal and male sexual behaviors in female rats. Behav. Neurosci. 1984, 98:703-711.
45. Hall Z.J., Bertin M., Bailey I.E., Meddle S.L., Healy S.D. Neural correlates of nesting behavior in zebra finches (Taeniopygia guttata). Behav. Brain Res. 2014, 264:26-33.
46. Hill J.M., Cuasay K., Abebe D.T. Vasoactive intestinal peptide antagonist treatment during mouse embryogenesis impairs social behavior and cognitive function of adult male offspring. Exp. Neurol. 2007, 206:101-113.
47. Hill J.M., Hauser J.M., Sheppard L.M., Abebe D., Spivak-Pohis I., Kushnir M., Deitch I., Gozes I. Blockage of VIP during mouse embryogenesis modifies adult behavior and results in permanent changes in brain chemistry. J. Mol. Neurosci. 2007, 31:183-200.
48. Jacobson C.D., Terkel J., Gorski R.A., Sawyer C.H. Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res. 1980, 194:471-478.
49. Joo K.M., Chung Y.H., Kim M.K., Nam R.H., Lee B.L., Lee K.H., Cha C.I. Distribution of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide receptors (VPAC1, VPAC2, and PAC1 receptor) in the rat brain. J. Comp. Neurol. 2004, 476:388-413.
50. Kalinichev M., Rosenblatt J.S., Morrell J.I. The medial preoptic area, necessary for adult maternal behavior in rats, is only partially established as a component of the neural circuit that supports maternal behavior in juvenile rats. Behav. Neurosci. 2000, 114:196-210.
51. Kelly A.M., Goodson J.L. Behavioral relevance of species-specific vasotocin anatomy in gregarious finches. Front. Neurosci. 2013, 7:242.
52. Kelly A.M., Goodson J.L. Functional significance of a phylogenetically widespread sexual dimorphism in vasotocin/vasopressin production. Horm. Behav. 2013, 64:840-846.
53. Kingsbury M.A., Goodson J.L. Pair bond formation is impaired by VPAC receptor antagonism in the socially monogamous zebra finch. Behav. Brain Res. 2014, 272:264-268.
54. Kingsbury M.A., Kelly A.K., Schrock S.E., Goodson J.L. Mammal-like organization of the avian midbrain central gray and a reappraisal of the intercollicular nucleus. PLoS ONE 2011, 6:e20720.
55. Kingsbury M.A., Miller K.M., Goodson J.L. VPAC receptor signaling modulates grouping behavior and social responses to contextual novelty in a gregarious finch: a role for a putative prefrontal cortex homologue. Horm. Behav. 2013, 64:511-518.
56. Klatt J.D., Goodson J.L. Sex-specific activity and function of hypothalamic nonapeptide neurons during nest-building in zebra finches. Horm. Behav. 2013, 64:818-824.
57. Kuenzel W.J., Blahser S. Vasoactive intestinal polypeptide (VIP)-containing neurons: distribution throughout the brain of the chick (Gallus domesticus) with focus upon the lateral septal organ. Cell Tissue Res. 1994, 275:91-107.
58. Kuenzel W.J., McCune S.K., Talbot R.T., Sharp P.J., Hill J.M. Sites of gene expression for vasoactive intestinal polypeptide throughout the brain of the chick (Gallus domesticus). J. Comp. Neurol. 1997, 381:101-118.
59. Kulick R.S., Chaiseha Y., Kang S.W., Rozenboim I., El Halawani M.E. The relative importance of vasoactive intestinal peptide and peptide histidine isoleucine as physiological regulators of prolactin in the domestic turkey. Gen. Comp. Endocrinol. 2005, 142:267-273.
60. Lam K.S. Vasoactive intestinal peptide in the hypothalamus and pituitary. Neuroendocrinology 1991, 53(Suppl. 1):45-51.
61. Lammel S., Hetzel A., Haeckel O., Jones I., Liss B., Roeper J. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008, 57:760-773.
62. Lea R.W., Vowles D.M. Vasoactive intestinal polypeptide stimulates prolactin release in vivo in the ring dove (Streptopelia risoria). Experientia 1986, 42:420-422.
63. Lea R.W., Talbot R.T., Sharp P.J. Passive immunization against chicken vasoactive intestinal polypeptide suppresses plasma prolactin and crop sac development in incubating ring doves. Horm. Behav. 1991, 25:283-294.
64. Lin D., Boyle M.P., Dollar P., Lee H., Lein E.S., Perona P., Anderson D.J. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011, 470:221-226.
65. Macnamee M.C., Sharp P.J., Lea R.W., Sterling R.J., Harvey S. Evidence that vasoactive intestinal polypeptide is a physiological prolactin-releasing factor in the bantam hen. Gen. Comp. Endocrinol. 1986, 62:470-478.
66. Maney D.L., Schoech S.J., Sharp P.J., Wingfield J.C. Effects of vasoactive intestinal peptide on plasma prolactin in passerines. Gen. Comp. Endocrinol. 1999, 113:323-330.
67. Maney D.L., Erwin K.L., Goode C.T. Neuroendocrine correlates of behavioral polymorphism in white-throated sparrows. Horm. Behav. 2005, 48:196-206.
68. Meddle S.L., King V.M., Follett B.K., Wingfield J.C., Ramenofsky M., Foidart A., Balthazart J. Copulation activates Fos-like immunoreactivity in the male quail forebrain. Behav. Brain Res. 1997, 85:143-159.
69. Meddle S.L., Foidart A., Wingfield J.C., Ramenofskyand M., Balthazart J. Effects of sexual interactions with a male on fos-like immunoreactivity in the female quail brain. J. Neuroendocrinol. 1999, 11:771-784.
70. Miceli M.O., Malsbury C.W. Sagittal knife cuts in the near and far lateral preoptic area-hypothalamus disrupt maternal behaviour in female hamsters. Physiol. Behav. 1982, 28:856-867.
71. Miceli M.O., Fleming A.S., Malsbury C.W. Disruption of maternal behaviour in virgin and postparturient rats following sagittal plane knife cuts in the preoptic area-hypothalamus. Behav. Brain Res. 1983, 9:337-860.
72. Morrison S.F., Nakamura K. Central neural pathways for thermoregulation. Front. Biosci. 2011, 16:74-104.
73. Moura L.M., Canteras N.S., Sukikara M.H., Felicio L.F. Morphine infusions into the rostrolateral periaqueductal gray affect maternal behaviors. Braz. J. Med. Biol. Res. 2010, 43:899-905.
74. Newman S.W. The medial extended amygdala in male reproductive behavior: a node in the mammalian social behavior network. Ann. N. Y. Acad. Sci. 1999, 877:242-257.
75. Numan M. Motivational systems and the neural circuitry of maternal behavior in the rat. Dev. Psychobiol. 2007, 49:12-21.
76. Numan M., Smith H.G. Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 1984, 98:712-727.
77. O'Connell L.A., Hofmann H.A. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 2011, 519:3599-3639.
78. Olazabal D.E., Kalinichev M., Morrell J.I., Rosenblatt J.S. MPOA cytotoxic lesions and maternal behavior in the rat: effects of midpubertal lesions on maternal behavior and the role of ovarian hormones in maturation of MPOA control of maternal behavior. Horm. Behav. 2002, 41:126-138.
79. Oxley G., Fleming A.S. The effects of medial preoptic area and amygdala lesions on maternal behavior in the juvenile rat. Dev. Psychobiol. 2000, 37:253-265.
80. Panzica G.C., Viglietta-Panzica C., Balthazart J. The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 1996, 17:51-125.
81. Paton J.J., Belova M.A., Morrison S.E., Salzman C.D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 2006, 439:865-870.
82. Pfaus J.G., Frank A. Beach award-homologies of animal and human sexual behaviors. Horm. Behav. 1996, 30:187-200.
83. Potash L.M. An experimental analysis of the use of location calls by Japanese quail, Coturnix coturnix japonica. Behaviour 1974, 54:153-180.
84. Prakobsaeng N., Sartsoongnoen N., Kosonsiriluk S., Chaiyachet O.A., Chokchaloemwong D., Rozenboim I., El Halawani M., Porter T.E., Chaiseha Y. Changes in vasoactive intestinal peptide and tyrosine hydroxylase immunoreactivity in the brain of nest-deprived native Thai hen. Gen. Comp. Endocrinol. 2011, 171:189-196.
85. Roberts G.W., Woodhams P.L., Polak J.M., Crow T.J. Distribution of neuropeptides in the limbic system of the rat: the amygdaloid complex. Neuroscience 1982, 7:99-131.
86. Sharp P.J., Sterling R.J., Talbot R.T., Huskisson N.S. The role of hypothalamic vasoactive intestinal polypeptide in the maintenance of prolactin secretion in incubating bantam hens: observations using passive immunization, radioimmunoassay and immunohistochemistry. J. Endocrinol. 1989, 122:5-13.
87. Sheehan T.P., Paul M., Amaral E., Numan M.J., Numan M. Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats. Neuroscience 2001, 106:341-356.
88. Sims K.B., Hoffman D.L., Said S.I., Zimmerman E.A. Vasoactive intestinal polypeptide (VIP) in mouse and rat brain: an immunocytochemical study. Brain Res. 1980, 186:165-183.
89. Slotnick B.M., Nigrosh B.J. Maternal behavior of mice with cingulate cortical, amygdala, or septal lesions. J. Comp. Physiol. Psychol. 1975, 88:118-127.
90. Taziaux M., Cornil C.A., Dejace C., Arckens L., Ball G.F., Balthazart J. Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur. J. Neurosci. 2006, 23:1869-1887.
91. Terkel J., Bridges R.S., Sawyer C.H. Effects of transecting lateral neural connections of the medial preoptic area on maternal behavior in the rat: nest building, pup retrieval and prolactin secretion. Brain Res. 1979, 169:369-380.
92. Vleck C.M., Patrick D.J. Effects of vasoactive intestinal peptide on prolactin secretion in three species of passerine birds. Gen. Comp. Endocrinol. 1999, 113:146-154.
93. Watanobe H., Sasaki S. Effect of thyroid status on the prolactin-releasing action of vasoactive-intestinal-peptide in humans - comparison with the action of thyrotropin-releasing-hormone. Neuroendocrinology 1995, 61:207-212.
94. Wu Z., Autry A.E., Bergan J.F., Watabe-Uchida M., Dulac C.G. Galanin neurons in the medial preoptic area govern parental behaviour. Nature 2014, 509:325-330.
95. Youngren O.M., Pitts G.R., Phillips R.E., El Halawani M.E. Dopaminergic control of prolactin secretion in the turkey. Gen. Comp. Endocrinol. 1996, 104:225-230.
96. Youngren O.M., Chaiseha Y., El Halawani M.E. Regulation of prolactin secretion by dopamine and vasoactive intestinal peptide at the level of the pituitary in the turkey. Neuroendocrinology 1998, 68:319-325.
97. Zann R.A. The Zebra Finch: A Synthesis of Field and Laboratory Studies 1996, Oxford University Press, Oxford.