Neural Correlates of Migration: Activation of Hypothalamic Clock(s) in and out of Migratory State in the Blackheaded Bunting (Emberiza melanocephala)

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Rastogi, Ashutosh ^a   Kumari, Yatinesh ^a   Rani, Sangeeta ^a   Kumar, Vinod ^b  

^a UNIVERSITY OF LUCKNOW   (India)

^b UNIVERSITY OF DELHI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPEPTIDE Y; PROTEIN C FOS; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLACKHEADED BUNTING; CIRCADIAN RHYTHM; CONTROLLED STUDY; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; EMBERIZIDAE; HYPERPHAGIA; INFERIOR HYPOTHALAMIC NUCLEUS; MALE; MEDIOBASAL HYPOTHALAMUS; NONHUMAN; PHOTOPERIODICITY; PITUITARY STALK; POPULATION MIGRATION; PROTEIN EXPRESSION; SUPRACHIASMATIC NUCLEUS;

ANALYSIS OF VARIANCE; ANIMAL MIGRATION; ANIMALS; BIOLOGICAL CLOCKS; CIRCADIAN RHYTHM; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; NEUROPEPTIDE Y; PASSERIFORMES; PROTO-ONCOGENE PROTEINS C-FOS; SUPRACHIASMATIC NUCLEUS;

EID: 84886911465     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070065     Document Type: Article

References (65)

1. Gwinner E, (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199: 39-48.
2. Kumar V, Singh BP, Rani S, (2004) The Bird Clock: A complex multi oscillatory and highly diversified system. Biol Rhythm Res 35: 121-144.
3. Dawson A, King VM, Bentley GE, Ball GF, (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16: 365-380.
4. Kumar V, Wingfield JC, Dawson A, Ramenofsky M, Rani S, et al. (2010) Biological clocks and regulation of seasonal reproduction and migration in birds. Physiol Biochem Zool 83: 827-835.
5. Budki P, Rani S, Kumar V, (2012) Persistence of circannual rhythms under constant periodic and aperiodic light conditions: sex differences and relationship with the external environment. J Exp Biol 215: 3774-3785.
6. Bartell P, Gwinner E, (2005) A separate circadian oscillator controls nocturnal migratory restlessness in a songbird Sylvia borin. J Biol Rhythms 20: 538-549.
7. Rani S, Malik S, Trivedi AK, Singh S, Kumar V, (2006) A circadian clock regulates migratory restlessness in the blackheaded bunting, Emberiza melanocephala. Curr Sci 91: 1093-1096.
8. Rastogi A, Kumari Y, Rani R, Kumar V, (2011) Phase inversion of neural activity in the olfactory and visual systems of a night-migratory bird during migration. Eur J Neurosci 34: 99-109.
9. Sumova A, Jac M, Sladek M, Illnerova H, (2002) Entrainment of the circadian pacemaker in the rat suprachiasmatic nucleus. Physiol Res 51: 44P.
10. Cantwell EL, Cassone VM, (2006) Chicken suprachiasmatic nuclei: I. efferent and afferent connections. J Comp Neurol 496: 97-120.
11. Wilson FE, (1991) Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). J Exp Zool 259: 117-127.
12. Thayananuphat A, Kang SW, Bakken T, Millam JR, El Halawani ME, (2007) Rhythm-dependent light induction of the c-fos gene in the turkey hypothalamus. J Neuroendocrinol 19: 407-417.
13. Kumar V, (1988) Investigations of photoperiodically induced fattening in migratory blackheaded bunting (Emberiza melanocephala) (Aves). J Zool Lond 216: 253-263.
14. Sharp PJ, Follett BK, (1969) The effect of hypothalamic lesions on gonadotrophin release in Japanese quail (Coturnix coturnix japonica). Neuroendocrinology 5: 205-218.
15. Ohta M, Wada M, Homma K, (1984) Induction of rapid testicular growth in Japanese quail by phasic electrical stimulation of the hypothalamic photosensitive area. J Comp Physiol A 154: 583-589.
16. Meddle SL, Follett BK, (1997) Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J Neurosci 17: 8909-8918.
17. Yasuo S, Watanabe M, Okabayashi N, Ebihara S, Yoshimura T, (2003) Circadian clock genes and photoperiodism: comprehensive analysis of clock gene expression in the mediobasal hypothalamus, the suprachiasmatic nucleus, and the pineal gland of Japanese quail under various light schedules. Endocrinology 144: 3742-3748.
18. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, et al. (2008) Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452: 317-U311.
19. Stevenson TJ, Ball GF, (2012) Disruption of neuropsin mRNA expression via RNA interference facilitates the photoinduced increase in thyrotropin-stimulating subunit b in birds. Eur J Neurosci 36: 2859-2865 doi:10.1111/j.1460-9568.2012.08209.x.
20. Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, et al. (2003) Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426: 178-181.
21. Li H, Kuenzel WJ, (2008) A possible neural cascade involving the photoneuroendocrine system (PNES) responsible for regulating gonadal development in an avian species, Gallus gallus. Brain Res Bul 76: 586-596.
22. Perfito N, Jeong SY, Silverin B, Calisi RM, Bentley GE, et al. (2012) Anticipating Spring: Wild Populations of Great Tits (Parus major) Differ in Expression of Key Genes for Photoperiodic Time Measurement. PLoS ONE 7: e34997 doi:10.1371/journal.pone.0034997.
23. Saab SS, Lange HS, Maney DL, (2010) Gonadotrophin-releasing hormone neurons in a photoperiodic songbird express Fos and Egr-1 protein after a single long day. J Neuroendocrinol 22: 196-207.
24. Silver R, Witkovsky P, Horvath P, Alones V, Barnstable CJ, et al. (1988) Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tis Res 253: 189-198.
25. Rathinam T, Kuenzel WJ, (2005) Attenuation of gonadal response to photostimulation following ablation of neurons in the lateral septal organ of chicks. Brain Res Bull 64: 455-461.
26. Teruyama R, Beck MM, (2001) Double immunocytochemistry of vasoactive intestinal peptide and cGnRH-I in male quail: photoperiodic effects. Cell Tis Res 303: 403-414.
27. Proudman JA, Opel H, (1983) Stimulation of prolactin and growth hormone secretion from turkey pituitary cells. Poult Sci 62: 1484-1485.
28. Macnamee MC, Sharp PJ, Lea RW, Sterling RJ, Harvey S, (1986) Evidence that vasoactive intestinal polypeptide is a physiological prolactin-releasing factor in the bantam hen. Gen Comp Endocrinol 62: 470-478.
29. Sharp PJ, Sterling RJ, Talbot RT, Huskisson NS, (1989) 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 122: 5-13.
30. Kuenzel WJ, (2000) Central nervous system regulation of gonadal development in the avian male. Poult Sci 79: 1679-1688.
31. Contijoch AM, Malamed S, McDonald JK, Advis JP, (1993) Neuropeptide Y regulation of LHRH release in the median eminence: immunocytochemical and physiological evidence in hens. Neuroendocrinology 57: 135-145.
32. Fraley GS, Kuenzel WJ, (1993) Precocious puberty in chicks (Gallus domesticus) induced by central injections of neuropeptide Y. Life Sci 52: 1649-1656.
33. Richardson RD, Boswell T, Raffety BD, Seeley RJ, Wingfield JC, et al. (1995) NPY increases food intake in white-crowned sparrows: effect in short and long photoperiods. Am J Physiol 268: R1418-R1422.
34. Boswell T, (2005) Regulation of energy balance in birds by the neuroendocrine hypothalamus. J Poult Sci 42: 161-181.
35. Ramakrishnan S, Strader AD, Wimpee B, Chen P, Smith MS, et al. (2007) Evidence for increased neuropeptide Y synthesis in mediobasal hypothalamus in relation to parental hyperphagia and gonadal activation in breeding ringdoves. J Neuroendocrinol 19: 163-171.
36. Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED, (2005) Night-vision brain area in migratory songbirds. Proc Natl Acad Sci USA 102: 8339-8344 doi 10.1073pnas.0409575102/pnas.0409575102.
37. Zapka M, Heyers D, Hein CM, Engels S, Schneider NL, et al. (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461: 1274-1277.
38. Heyers D, Zapka M, Hoffmeister M, Wild JM, Mouritsen H, (2010) Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc Natl Acad Sci USA 107: 9394-9399 doi/10.1073/pnas.0907068107.
39. Kumar V, Jain N, Singh BP, Kumar BS, (1993) Plasma levels of luteinizing hormone in intact and castrated blackheaded bunting (Emberiza melanocephala) exposed to stimulatory and nonstimulatory photoperiods. Reprod Nutr Dev 33: 143-150.
40. Ali S, Ripley SD (1974) Handbook of birds of India and Pakistan. Bombay: Oxford University Press.
41. Malik S, Rani S, Kumar V, (2004) Wavelength dependency of light-induced effects on photoperiodic clock in the migratory blackheaded bunting (Emberiza melanocephala). Chronobiol Int 21: 367-384.
42. Klüver H, Barrera E, (1953) A method for the combined staining of cells and fibers in the nervous system. J Neuropathol Exp Neurol 12: 400-403.
43. Sharp PJ, (2005) Photoperiodic regulation of seasonal breeding in birds. Annals of the New York Academy of Sciences 1040: 189-199.
44. Sakharkar AJ, Singru PS, Sarkar K, Subhedar N, (2005) Neuropeptide Y in the forebrain of the adult male cichlid fish Oreochromis mossambicus: distribution, effects of castration and testosterone replacement. J Comp Neurol 489: 148-165.
45. D'hondt E, Vermeiren J, Peeters K, Balthazart J, Tlemcani O, et al. (1999) Validation of a new antiserum directed towards the synthetic c-terminus of the FOS protein in avian species: immunological, physiological and behavioral evidence. J Neurosci Methods 91: 31-45.
46. Kumar V, Goguen DM, Guido ME, Rusak B, (1997) Melatonin does not influence the expression of c-fos in the suprachiasmatic nucleus of rats and hamsters. Mol Brain Res 52: 242-248.
47. Gentner TQ, Hulse SH, Duffy D, Ball GF, (2001) Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46: 48-58.
48. Small TW, Sharp PJ, Bentley GE, Millar RP, Tsutsui K, et al. (2008) Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living Sonaran desert bird, the Rufous-winged sparrow (Aimophila carpalis). Brain Behav Evol 71: 127-142.
49. King VM, Follett BK, (1997) c-fos expression in the putative avian suprachiasmatic nucleus. J Comp Physiol A 180: 541-551.
50. Wallman J, Saldanha CJ, Silver R, (1994) A putative suprachiasmatic nucleus of birds responds to visual motion. J Comp Physiol A 174: 297-304.
51. Brandstätter R, Abraham U, (2003) Hypothalamic circadian organization in birds. I. Anatomy, functional morphology, and terminology of the suprachiasmatic region. Chronobiol Int 20: 637-655.
52. Bernardis LL, Bellinger LL, (1998) The dorsomedial hypothalamic nucleus revisited: update. Proc Soc Exp Biol Med 218: 284-306.
53. Chou TC, Scammell TE, Gooley JJ, Gaus SE, Saper CB, et al. (2003) Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci 23: 10691-10702.
54. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML, (2001) A neural circuit for circadian regulation of arousal. Nat Neurosci 4: 732-738.
55. Saper CB, Lu J, Chou TC, Gooley J, (2005) The hypothalamic integrator for circadian rhythms. Trends Neurosci 28: 152-157.
56. Saldanha CJ, Silverman AJ, Silver R, (2001) Direct innervation of GnRH neurons by encephalic photoreceptors in birds. J Biol Rhythms 16: 39-49.
57. Wang G, Wingfield JC, (2011) Immunocytochemical study of rhodopsin-containing putative encephalic photoreceptors in house sparrow, Passer domesticus. Gen Comp Endocrinol 170: 589-596.
58. Molinero P, Guerrero JM, (1993) Vasoactive intestinal peptide stimulates type II thyroxine 5-deiodinase and N-acetyltransferase activities in dispersed pineal cells of euthyroid and hypothyroid rats. Neurosci Lett 151: 130-133.
59. El Halawani ME, Youngren OM, Pitts GR (1997) Vasoactive intestinal peptide as the avian prolactin releasing factor. In: Harvey S, Etches RJ, editors. Perspectives in Avian Endocrinology. Bristol: Journal of Endocrinology Ltd. pp. 403-416.
60. Opel H, Proudman JA, (1988) Stimulation of prolactin release in turkeys by vasoactive intestinal peptide. Proc Soc Exp Biol Med 187: 455-460.
61. Tewary PD, Kumar V, Tripathi BK, (1984) Response to exogenous prolactin during gonadal photostimulation in blackheaded bunting. Current Sci 53: 1307-1308.
62. Kuenzel WJ, Douglass LW, Davison BA, (1987) Robust feeding following central administration of neuropeptide Y or peptide YY in chicks, Gallus domesticus. Peptides 8: 823-828.
63. Kawaguchi M, Scott KA, Moran TH, Bi S, (2005) Dorsomedial hypothalamic corticotropin-releasing factor mediation of exercise-induced anorexia. Am J Physiol Regul Integr Comp Physiol 288: R1800-R1805.
64. Tewary PD, Kumar V, (1981) Effect of castration on photoperiodically induced weight gain in a migratory finch: Blackheaded bunting Emberiza melanocephala. Indian J Exp Biol 19: 469-471.
65. Gupta NJ, Kumar V, (2013) Testes play a role in termination but not in initiation of the spring migration in the night-migratory blackheaded bunting. Anim Biol (in press).