Mechanisms of neuromodulation by a nonhypophysiotropic GnRH system controlling motivation of reproductive behavior in the teleost brain

Journal of Reproduction and Development

Volumn 57, Issue 6, 2011, Pages 665-674

  Hideki, A B E ^a   Yoshitaka, O K A ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Excitation secretion coupling; GnRH; Neuromodulation; Reproductive behavior; Sensory modulation

Indexed keywords

GONADORELIN; NEUROPEPTIDE;

ANIMAL; BRAIN; FEMALE; FISH; MALE; NERVE CELL; PHYSIOLOGY; REVIEW; SECRETION; SEXUAL BEHAVIOR;

ANIMALS; BRAIN; FEMALE; FISHES; GONADOTROPIN-RELEASING HORMONE; MALE; NEURONS; NEUROPEPTIDES; SEXUAL BEHAVIOR, ANIMAL;

TELEOSTEI;

EID: 84856332777     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.11-055E     Document Type: Review

References (67)

1. Maeda K-i, Ohkura S, Uenoyama Y, Wakabayashi Y, Oka Y, Tsukamura H, Okamura H. Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus. Brain Res, 2010; 1364: 103-115.
2. Oka Y. The gonadotropin-releasing hormone (GnRH) neuronal system of fish brain as a model system for the study of peptidergic neuromodulation. In: Parhar IS, Sakuma Y (eds.), GnRH Neurons: Genes to Behavior. Tokyo: Brain shuppan; 1997: 245-276 (In Japanese).
3. Okubo K, Nagahama Y. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiologica, 2008; 193: 3-15.
4. Yamamoto N, Oka Y, Amano M, Aida K, Hasegawa Y, Kawashima S. Multiple gonadotropin-releasing hormone (GnRH)-immunoreactive systems in the brain of the dwarf gourami, Colisa lalia: immunohistochemistry and radioimmunoassay. J Comp Neurol, 1995; 355: 354-368.
5. Yamamoto N, Parhar IS, Sawai N, Oka Y, Ito H. Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neurosci Res, 1998; 31: 31-38.
6. Yamamoto N, Oka Y, Yoshimoto M, Sawai N, Albert JS, Ito H. Gonadotropin-releasing hormone neurons in the gourami midbrain: a double labeling study by immunocytochemistry and tracer injection. Neurosci Lett, 1998; 240: 50-52.
7. Kanda S, Nishikawa K, Karigo T, Okubo K, Isomae S, Abe H, Kobayashi D, Oka Y. Regular pacemaker activity characterizes gonadotropin-releasing hormone 2 neurons recorded from green fluorescent protein-transgenic medaka. Endocrinology, 2010; 151: 695-701.
8. Oka Y. Electrophysiological characteristics of gonadotrophin-releasing hormone 1-3 neurones: insights from a study of fish brains. J Neuroendocrinol, 2010; 22: 659-663.
9. Abe H, Oka Y. Neuromodulatory functions of terminal nerve-GnRH neurons. Fish Physiology, 2006; 25: 455-503.
10. Del Castillo J, Katz B. Quantal components of the end-plate potential. J Physiol (Lond), 1954; 124: 560-573.
11. Redman S. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev, 1990; 70: 165-198.
12. Ghijsen WEJM, Miriam Leenders AG. Differential signaling in presynaptic neurotransmitter release. CMLS Cell Mol Life Sci, 2005; 62: 937-954.
13. Leng G, Ludwig M. Neurotransmitters and peptides: whispered secrets and public announcements. J Physiol (Lond), 2008; 586: 5625-5632.
14. Fuxe K, Dahlstrom A, Hoistad M, Marcellino D, Jansson A, Rivera A, Diaz-Cabiale Z, Jacobsen K, Tinner-Staines B, Hagman B, Leo G, Staines W, Guidolin D, Kehr J, Genedani S, Belluardo N, Agnati LF. From the Golgi-Cajal mapping to the transmitter-based characterization of the neuronal networks leading to two modes of brain communication: wiring and volume transmission. Brain Res Rev, 2007; 55: 17-54.
15. Nässel DR. Neuropeptide signaling near and far: how localized and timed is the action of neuropeptides in brain circuits? Invert Neurosci, 2009; 9: 57-75.
16. Chen CC, Fernald RD. Distributions of two gonadotropin-releasing hormone receptor types in a cichlid fish suggest functional specialization. J Comp Neurol, 2006; 495: 314-323.
17. Peter RE, Prasada Rao PD, Baby SM, Illing N, Millar RP. Differential brain distribution of gonadotropin-releasing hormone receptors in the goldfish. Gen Comp Endocrinol, 2003; 132: 399-408.
18. Soga T, Ogawa S, Millar RP, Sakuma Y, Parhar IS. Localization of the three GnRH types and GnRH receptors in the brain of a cichlid fish: Insights into their neuroendocrine and neuromodulator functions. J Comp Neurol, 2005; 487: 28-41.
19. Millar RP, Pawson AJ, Morgan K, Rissman EF, Lu ZL. Diversity of actions of GnRHs mediated by ligand-induced selective signaling. Front Neuroendocrinol, 2008; 29: 17-35.
20. Yamamoto N, Ito H. Afferent sources to the ganglion of the terminal nerve in teleosts. J Comp Neurol, 2000; 428: 355-375.
21. Yamamoto N, Oka Y, Kawashima S. Lesions of gonadotropin-releasing hormoneimmunoreactive terminal nerve cells: effects on the reproductive behavior of male dwarf gouramis. Neuroendocrinology, 1997; 65: 403-412.
22. Ishizaki M, Iigo M, Yamamoto N, Oka Y. Different modes of gonadotropin-releasing hormone (GnRH) release from multiple GnRH systems as revealed by radioimmunoassay using brain slices of a teleost, the dwarf gourami (Colisa lalia). Endocrinology, 2004; 145: 2092-2103.
23. Abe H, Oka Y. Primary culture of the isolated terminal nerve-gonadotrophin-releasing hormone neurones derived from adult teleost (dwarf gourami, Colisa lalia) brain for the study of peptide release mechanisms. J Neuroendocrinol, 2009; 21: 489-505.
24. Oka Y, Ichikawa M. Ultrastructure of the ganglion cells of the terminal nerve in the dwarf gourami (Colisa lalia). J Comp Neurol, 1991; 304: 161-171.
25. De-Miguel FF, Trueta C. Synaptic and extrasynaptic secretion of serotonin. Cell Mol Neurobiol, 2005; 25: 297-312.
26. Ludwig M, Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci, 2006; 7: 126-136.
27. Akazome Y, Kanda S, Oka Y. Expression of vesicular glutamate transporter-2.1 in medaka terminal nerve gonadotrophin-releasing hormone neurones. J Neuroendocrinol., 2011; 23: 570-576.
28. Bean AJ, Roth RH. Dopamine-neurotensin interactions in mesocortical neurons. Evidence from microdialysis studies. Ann NY Acad Sci, 1992; 668: 43-53.
29. Schroeder TJ, Jankowski JA, Senyshyn J, Holz RW, Wightman RM. Zones of exocytotic release on bovine adrenal medullary cells in culture. J Biol Chem, 1994; 269: 17215-17220.
30. Vardjan N, Jorgacevski J, Stenovec M, Kreft M, Zorec R. Compound exocytosis in pituitary cells. Ann NY Acad Sci, 2009; 1152: 63-75.
31. Pickett JA, Edwardson JM. Compound exocytosis: mechanisms and functional significance. Traffic, 2006; 7: 109-116.
32. Oka Y, Ichikawa M. Ultrastructural characterization of gonadotropin-releasing hormone (GnRH)-immunoreactive terminal nerve cells in the dwarf gourami. Neurosci Lett, 1992; 140: 200-202.
33. Abe H, Oka Y. Modulation of pacemaker activity by salmon gonadotropin-releasing hormone (sGnRH) in terminal nerve (TN)-GnRH neurons. J Neurophysiol, 2000; 83: 3196-3200.
34. Hajdü P, Ikemoto T, Akazome Y, Park MK, Oka Y. Terminal nerve gonadotrophinreleasing hormone (GnRH) neurones express multiple GnRH receptors in a teleost, the dwarf gourami (Colisa lalia). J Neuroendocrinol, 2007; 19: 475-479.
35. Bechtold DA, Luckman SM. The role of RFamide peptides in feeding. J Endocrinol, 2007; 192: 3-15.
36. Saito TH, Nakane R, Akazome Y, Abe H, Oka Y. Electrophysiological analysis of the inhibitory effects of FMRFamide-like peptides on the pacemaker activity of gonadotropin-releasing hormone neurons. J Neurophysiol, 2010; 104: 3518-3529.
37. Wirsig-Wiechmann CR, Oka Y. The terminal nerve ganglion cells project to the olfactory mucosa in the dwarf gourami. Neurosci Res, 2002; 44: 337-341.
38. Osugi T, Ukena K, Sower SA, Kawauchi H, Tsutsui K. Evolutionary origin and divergence of PQRFamide peptides and LPXRFamide peptides in the RFamide peptide family. Insights from novel lamprey RFamide peptides. FEBS J 2006; 273: 1731-1743.
39. Oehlmann VD, Korte H, Sterner C, Korsching SI. A neuropeptide FF-related gene is expressed selectively in neurons of the terminal nerve in Danio rerio. Mech Dev, 2002; 117: 357-361.
40. Rossoni E, Feng J, Tirozzi B, Brown D, Leng G, Moos F, Friston KJ. Emergent synchronous bursting of oxytocin neuronal network. PLoS Comput Biol, 2008; 4: e1000123.
41. Haneda K, Oka Y. Coordinated synchronization in the electrically coupled network of terminal nerve gonadotropin-releasing hormone neurons as demonstrated by double patch-clamp study. Endocrinology, 2008; 149: 3540-3548.
42. Grens KE, Greenwood AK, Fernald RD. Two visual processing pathways are targeted by gonadotropin-releasing hormone in the retina. Brain Behav Evol, 2005; 66: 1-9.
43. Eisthen HL, Delay RJ, Wirsig-Wiechmann CR, Dionne VE. Neuromodulatory effects of gonadotropin releasing hormone on olfactory receptor neurons. J Neurosci, 2000; 20: 3947-3955.
44. Maruska KP, Tricas TC. Gonadotropin-releasing hormone and receptor distributions in the visual processing regions of four coral reef fishes. Brain Behav Evol, 2007; 70: 40-56.
45. Park D, Eisthen HL. Gonadotropin releasing hormone (GnRH) modulates odorant responses in the peripheral olfactory system of axolotls. J Neurophysiol, 2003; 90: 731-738.
46. Kawai T, Abe H, Akazome Y, Oka Y. Neuromodulatory effect of GnRH on the synaptic transmission of the olfactory bulbar neural circuit in goldfish, Carassius auratus. J Neurophysiol, 2010; 104: 3540-3550.
47. Satou M. Synaptic organization, local neuronal circuitry, and functional segregation of the teleost olfactory bulb. Prog Neurobiol, 1990; 34: 115-142.
48. Jodo A, Kitahashi T, Taniyama S, Bhandari RK, Ueda H, Urano A, Ando H. Seasonal variation in the expression of five subtypes of gonadotropin-releasing hormone receptor genes in the brain of masu salmon from immaturity to spawning. Zool Sci, 2005; 22: 1331-1338.
49. Maruska KP, Fernald RD. Reproductive status regulates expression of sex steroid and GnRH receptors in the olfactory bulb. Behav Brain Res, 2010; 213: 208-217.
50. Onuma T, Higa M, Ando H, Ban M, Urano A. Elevation of gene expression for salmon gonadotropin-releasing hormone in discrete brain loci of prespawning chum salmon during upstream migration. J Neurobiol, 2005; 63: 126-145.
51. Behrens U, Wagner HJ. Terminal nerve and vision. Microsc Res Tech, 2004; 65: 25-32.
52. Kinoshita M, Kobayashi S, Urano A, Ito E. Neuromodulatory effects of gonadotropin-releasing hormone on retinotectal synaptic transmission in the optic tectum of rainbow trout. Eur J Neurosci, 2007; 25: 480-484.
53. Maaswinkel H, Li L. Olfactory input increases visual sensitivity in zebrafish: a possible function for the terminal nerve and dopaminergic interplexiform cells. J Exp Biol, 2003; 206: 2201-2209.
54. 2+signalling pathways. J Physiol (Lond), 2005; 569: 939-948.
55. Miklósi A, Andrew RJ. The zebrafish as a model for behavioral studies. Zebrafish, 2006; 3: 227-234.
56. Maruska KP, Tricas TC. Gonadotropin-releasing hormone (GnRH) modulates auditory processing in the fish brain. Horm Behav, 2011; 59: 451-464.
57. Munakata A, Kobayashi M. Endocrine control of sexual behavior in teleost fish. Gen Comp Endocrinol, 2010; 165: 456-468.
58. Ogawa S, Akiyama G, Kato S, Soga T, Sakuma Y, Parhar IS. Immunoneutralization of gonadotropin-releasing hormone type-III suppresses male reproductive behavior of cichlids. Neurosci Lett, 2006; 403: 201-205.
59. Fiszbein A, Canepa M, Vazquez GR, Maggese C, Pandolfi M. Photoperiodic modulation of reproductive physiology and behaviour in the cichlid fish Cichlasoma dimerus. Physiol Behav, 2010; 99: 425-432.
60. Volkoff H, Peter RE. Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen Comp Endocrinol, 1999; 116: 347-355.
61. Ramakrishnan S, Wayne NL. Social cues from conspecifics alter electrical activity of gonadotropin-releasing hormone neurons in the terminal nerve via visual signals. Am J Physiol Regul Integr Comp Physiol, 2009; 297: R135-R141.
62. Kauffman AS. Emerging functions of gonadotropin-releasing hormone II in mammalian physiology and behaviour. J Neuroendocrinol, 2004; 16: 794-806.
63. Matsuda K, Nakamura K, Shimakura S, Miura T, Kageyama H, Uchiyama M, Shioda S, Ando H. Inhibitory effect of chicken gonadotropin-releasing hormone II on food intake in the goldfish, Carassius auratus. Horm Behav, 2008; 54: 83-89.
64. Biju KC, Singru PS, Schreibman MP, Subhedar N. Reproduction phase-related expression of GnRH-like immunoreactivity in the olfactory receptor neurons, their projections to the olfactory bulb and in the nervus terminalis in the female Indian major carp Cirrhinus mrigala, (Ham.). Gen Comp Endocrinol, 2003; 133: 358-367.
65. White SA, Fernald RD. Gonadotropin-releasing hormone-containing neurons change size with reproductive state in female Haplochromis burtoni. J Neurosci, 1993; 13: 434-441.
66. White SA, Nguyen T, Fernald RD. Social regulation of gonadotropin-releasing hormone. J Exp Biol, 2002; 205: 2567-2581.
67. Burmeister SS, Jarvis ED, Fernald RD. Rapid behavioral and genomic responses to social opportunity. PLoS Biol, 2005; 3: e363.