Neurobiological study of fish brains gives insights into the nature of gonadotropin-releasing hormone 1-3 neurons

Frontiers in Endocrinology

Volumn 4, Issue NOV, 2013, Pages

  Karigo, Tomomi ^a   Oka, Yoshitaka ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Behavior; Electrophysiology; Evolution; GnRH; gnrh1; gnrh2; gnrh3; Morphology

Indexed keywords

EID: 84890306412     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00177     Document Type: Review

References (129)

1. Oka Y. The Gonadotropin-Releasing Hormone (GnRH) Neuronal System of Fish Brain as a Model System for the Study of Peptidergic Neuromodulation. Tokyo: Brain Shuppan (1997).
2. Oka Y. Physiology and release activity of GnRH neurons. Progr Brain Res (2002) 141:259-81. doi: 10.1016/S0079-6123(02)41098-9
3. Abe H, Oka Y. Neuromodulatory functions of terminal nerve-GnRH neurons. In: Hara T, Zielenski B editors. Sensory Systems Neuroscience. San Diego: Elsevier (2007). p. 455-503.
4. Okubo K, Nagahama Y. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol (2008) 193:3-15. doi:10.1111/j.1748-1716.2008.01832.x
5. Ohno S. Evolution by Gene Duplication. Berlin: Springer Verlag (1970).
6. Oka Y. Electrophysiological characteristics of gonadotrophin-releasing hormone 1-3 neurones: insights from a study of fish brains. J Neuroendocrinol (2010) 22:659-63. doi:10.1111/j.1365-2826.2010.02035.x
7. Wayne NL, Kuwahara K, Aida K, Nagahama Y, Okubo K. Whole-cell electrophysiology of gonadotropin-releasing hormone neurons that express green fluorescent protein in the terminal nerve of transgenic medaka (Oryzias latipes). Biol Reprod (2005) 73:1228-34. doi:10.1095/biolreprod.105.042721
8. 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) 297:135-41. doi:10.1152/ajpregu.00143.2009
9. Bushnik TL, Fernald RD. The population of GnRH-containing neurons showing socially mediated size changes project to the pituitary in a teleost, Haplochromis burtoni. Brain Behav Evol (1995) 46:371-7. doi:10.1159/000113287
10. Yamamoto N, Parhar IS, Sawai N, Oka Y, Ito H. Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neurosci Res (1998) 31:31-8. doi:10.1016/S0168-0102(98)00022-4
11. Karigo T, Kanda S, Takahashi A, Abe H, Okubo K, Oka Y. Time-of-day-dependent changes in GnRH1 neuronal activities and gonadotropin mRNA expression in a daily spawning fish, medaka. Endocrinology (2012) 153:3394-404. doi:10.1210/en.2011-2022
12. Kelly MJ, Ronnekleiv OK, Eskay RL. Identification of estrogen-responsive LHRH neurons in the guinea pig hypothalamus. Brain Res Bull (1984) 12:399-407. doi:10.1016/0361-9230(84)90112-6
13. Kelly MJ, Condon TP, Levine JE, Ronnekleiv OK. Combined electrophysiological, immunocytochemical and peptide release measurements in the hypothalamic slice. Brain Res (1985) 345:264-70. doi:10.1016/0006-8993(85)91002-9
14. Lagrange AH, Ronnekleiv OK, Kelly MJ. Estradiol-17 beta and mu-opioid peptides rapidly hyperpolarize GnRH neurons: A cellular mechanism of negative feedback? Endocrinology (1995) 136:2341-4. doi:10.1210/en.136.5.2341
15. + conductance. Neuroendocrinology (1998) 67:73-82. doi:10.1159/000054301
16. Spergel DJ, Kruth U, Hanley DF, Sprengel R, Seeburg PH. GABA-and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci (1999) 19:2037-50.
17. Suter KJ, Song WJ, Sampson TL, Wuarin JP, Saunders JT, Dudek FE, et al. Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: Characterization of whole-cell electrophysiological properties and morphology. Endocrinology (2000) 141:412-9. doi:10.1210/en.141.1.412
18. Kato M, Ui-Tei K, Watanabe M, Sakuma Y. Characterization of voltage-gated calcium currents in gonadotropin-releasing hormone neurons tagged with green fluorescent protein in rats. Endocrinology (2003) 144:5118-25. doi:10.1210/en.2003-0213.
19. Han SK, Todman MG, Herbison AE. Endogenous GABA release inhibits the firing of adult gonadotropin-releasing hormone neurons. Endocrinology (2004) 145:495-9. doi:10.1210/en.2003-1333
20. Okubo K, Sakai F, Lau EL, Yoshizaki G, Takeuchi Y, Naruse K, et al. Forebrain gonadotropin-releasing hormone neuronal development: Insights from transgenic medaka and the relevance to X-linked Kallmann syndrome. Endocrinology (2006) 147:1076-84. doi:10.1210/en.2005-0468
21. Jasoni CL, Todman MG, Strumia MM, Herbison AE. Cell type-specific expression of a genetically encoded calcium indicator reveals intrinsic calcium oscillations in adult gonadotropin-releasing hormone neurons. J Neurosci (2007) 27:860-7. doi:10.1523/JNEUROSCI.3579-06.2007
22. Greenwood AK, Fernald RD. Social regulation of the electrical properties of gonadotropin-releasing hormone neurons in a cichlid fish (Astatotilapia burtoni). Biol Reprod (2004) 71:909-18. doi:10.1095/biolreprod.104.030072
23. Kawabata Y, Hiraki T, Takeuchi A, Okubo K. Sex differences in the expression of vasotocin/isotocin, gonadotropin-releasing hormone, and tyrosine and tryptophan hydroxylase family genes in the medaka brain. Neuroscience (2012) 218:65-77. doi:10.1016/j.neuroscience.2012.05.021
24. Kanda S, Nishikawa K, Karigo T, Okubo K, Isomae S, Abe H, et al. Regular pacemaker activity characterizes gonadotropin-releasing hormone 2 neurons recorded from green fluorescent protein-transgenic medaka. Endocrinology (2010) 151:695-701. doi:10.1210/en.2009-0842
25. Suter KJ, Wuarin JP, Smith BN, Dudek FE, Moenter SM. Whole-cell recordings from preoptic/hypothalamic slices reveal burst firing in gonadotropin-releasing hormone neurons identified with green fluorescent protein in transgenic mice. Endocrinology (2000) 141:3731-6. doi:10.1210/en.141.10.3731
26. Nunemaker CS, Defazio RA, Moenter SM. Estradiol-sensitive afferents modulate long-term episodic firing patterns of GnRH neurons. Endocrinology (2002) 143:2284-92. doi:10.1210/en.143.6.2284
27. Abe H, Terasawa E. Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons. Endocrinology (2005) 146:4312-20. doi:10.1210/en.2005-0435
28. Ishizaki M, Oka Y. Amperometric recording of gonadotropin-releasing hormone release activity in the pituitary of the dwarf gourami (teleost) [correction of (teleosat)] brain-pituitary slices. Neurosci Lett (2001) 299:121-4. doi:10.1016/S0304-3940(01)01492-6
29. 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) 145:2092-103. doi:10.1210/en.2003-0960
30. Glanowska KM, Venton BJ, Moenter SM. Fast scan cyclic voltammetry as a novel method for detection of real-time gonadotropin-releasing hormone release in mouse brain slices. J Neurosci (2012) 32:14664-9. doi:10.1523/JNEUROSCI.1303-12.2012
31. Karigo T, Aikawa M, Kondo C, Abe H, Kanda S, Oka Y. Whole brain-pituitary in vitro preparation of the transgenic medaka (Oryzias latipes) as a tool for analyzing the differential regulatory mechanisms of LH and FSH release. Endocrinology (2013) (in press).
32. Christian CA, Moenter SM. The neurobiology of preovulatory and estradiol-induced gonadotropin-releasing hormone surges. Endocr Rev (2010) 31:544-77. doi:10.1210/er.2009-0023
33. Christian CA, Mobley JL, Moenter SM. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity. Proc Natl Acad Sci U S A (2005) 102:15682-7. doi:10.1073/pnas.0504270102
34. Moenter SM. Identified GnRH neuron electrophysiology: A decade of study. Brain Res (2010) 1364:10-24. doi:10.1016/j.brainres.2010.09.066
35. Defazio RA, Heger S, Ojeda SR, Moenter SM. Activation of A-type gamma-aminobutyric acid receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol (2002) 16:2872-91. doi:10.1210/me.2002-0163
36. Moenter SM, DeFazio RA. Endogenous gamma-aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology (2005) 146:5374-9. doi:10.1210/en.2005-0788
37. Yin C, Ishii H, Tanaka N, Sakuma Y, Kato M. Activation of A-type gamma-amino butyric acid receptors excites gonadotrophin-releasing hormone neurones isolated from adult rats. J Neuroendocrinol (2008) 20:566-75. doi:10.1111/j.1365-2826.2008.01697.x
38. Herbison AE, Moenter SM. Depolarising and hyperpolarising actions of GABAA receptor activation on gonadotrophin-releasing hormone neurones: Towards an emerging consensus. J Neuroendocrinol (2011) 23:557-69. doi:10.1111/j.1365-2826.2011.02145.x
39. Christian CA, Pielecka-Fortuna J, Moenter SM. Estradiol suppresses glutamatergic transmission to gonadotropin-releasing hormone neurons in a model of negative feedback in mice. Biol Reprod (2009) 80:1128-35. doi:10.1095/biolreprod.108.075077
40. Christian CA, Moenter SM. Estradiol induces diurnal shifts in GABA transmission to gonadotropin-releasing hormone neurons to provide a neural signal for ovulation. J Neurosci (2007) 27:1913-21. doi:10.1523/JNEUROSCI.4738-06.2007
41. Chappell PE, Goodall CP, Tonsfeldt KJ, White RS, Bredeweg E, Latham KL. Modulation of gonadotrophin-releasing hormone secretion by an endogenous circadian clock. J Neuroendocrinol (2009) 21:339-45. doi:10.1111/j.1365-2826.2009.01845.x
42. Williams WP III, Kriegsfeld LJ. Circadian control of neuroendocrine circuits regulating female reproductive function. Front Endocrinol (2012) 3:60. doi:10.3389/fendo.2012.00060
43. Van der Beek EM, Horvath TL, Wiegant VM, Van Den Hurk R, Buijs RM. Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: Combined tracing and light and electron microscopic immunocytochemical studies. J Comp Neurol (1997) 384:569-79. doi:10.1002/(SICI)1096-9861(19970811)384:4<569::AID-CNE6>3.0.CO;2-0
44. Van der Beek EM, Wiegant VM, Van Oudheusden HJ, Van Der Donk HA, Van Den Hurk R, Buijs RM. Synaptic contacts between gonadotropin-releasing hormone-containing fibers and neurons in the suprachiasmatic nucleus and perichiasmatic area: An anatomical substrate for feedback regulation? Brain Res (1997) 755:101-11. doi:10.1016/S0006-8993(97)00086-3
45. de la Iglesia HO, Meyer J, Schwartz WJ. Lateralization of circadian pacemaker output: Activation of left-and right-sided luteinizing hormone-releasing hormone neurons involves a neural rather than a humoral pathway. J Neurosci (2003) 23:7412-4.
46. Brown-Grant K, Raisman G. Abnormalities in reproductive function associated with the destruction of the suprachiasmatic nuclei in female rats. Proc R Soc Lond B Biol Sci (1977) 198:279-96. doi:10.1098/rspb.1977.0098
47. Miller BH, Olson SL, Turek FW, Levine JE, Horton TH, Takahashi JS. Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr Biol (2004) 14:1367-73. doi:10.1016/j.cub.2004.07.055
48. Watson RE Jr, Langub MC Jr, Engle MG, Maley BE. Estrogen-receptive neurons in the anteroventral periventricular nucleus are synaptic targets of the suprachiasmatic nucleus and peri-suprachiasmatic region. Brain Res (1995) 689:254-64. doi:10.1016/0006-8993(95)00548-5
49. Vida B, Deli L, Hrabovszky E, Kalamatianos T, Caraty A, Coen CW, et al. Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: regulation by oestrogen. J Neuroendocrinol (2010) 22:1032-9. doi:10.1111/j.1365-2826.2010.02045.x
50. Hickok JR, Tischkau SA. In vivo circadian rhythms in gonadotropin-releasing hormone neurons. Neuroendocrinology (2010) 91:110-20. doi:10.1159/000243163
51. Mansuy V, Risold PY, Glauser M, Fraichard A, Pralong FP. Expression of the GABAA receptor associated protein Gec1 is circadian and dependent upon the cellular clock machinery in GnRH secreting GnV-3 cells. Mol Cell Endocrinol (2009) 307:68-76. doi:10.1016/j.mce.2009.02.029
52. Sun J, Chu Z, Moenter SM. Diurnal in vivo and rapid in vitro effects of estradiol on voltage-gated calcium channels in gonadotropin-releasing hormone neurons. J Neurosci (2010) 30:3912-23. doi:10.1523/JNEUROSCI.6256-09.2010
53. Trudeau VL. Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus. Rev Reprod (1997) 2:55-68. doi:10.1530/ror.0.0020055
54. Zohar Y, Munoz-Cueto JA, Elizur A, Kah O. Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol (2010) 165:438-55. doi:10.1016/j.ygcen.2009.04.017
55. Yu KL, Peter RE. Dopaminergic regulation of brain gonadotropin-releasing hormone in male goldfish during spawning behavior. Neuroendocrinology (1990) 52:276-83. doi:10.1159/000125598
56. Yu KL, Peter RE. Adrenergic and dopaminergic regulation of gonadotropin-releasing hormone release from goldfish preoptic-anterior hypothalamus and pituitary in vitro. Gen Comp Endocrinol (1992) 85:138-46. doi:10.1016/0016-6480(92)90181-I
57. Yu KL, Rosenblum PM, Peter RE. In vitro release of gonadotropin-releasing hormone from the brain preoptic-anterior hypothalamic region and pituitary of female goldfish. Gen Comp Endocrinol (1991) 81:256-67. doi:10.1016/0016-6480(91)90010-4
58. Tsutsui K, Bentley GE, Ubuka T, Saigoh E, Yin H, Osugi T, et al. The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). Gen Comp Endocrinol (2007) 153:365-70. doi:10.1016/j.ygcen.2006.10.005
59. Qi X, Zhou W, Li S, Lu D, Yi S, Xie R, et al. Evidences for the regulation of GnRH and GTH expression by GnIH in the goldfish, Carassius auratus. Mol Cell Endocrinol (2013) 366:9-20. doi:10.1016/j.mce.2012.11.001
60. Mercer RE, Chee MJ, Colmers WF. The role of NPY in hypothalamic mediated food intake. Front Neuroendocrinol (2011) 32:398-415. doi:10.1016/j.yfrne.2011.06.001
61. Matsuda K, Sakashita A, Yokobori E, Azuma M. Neuroendocrine control of feeding behavior and psychomotor activity by neuropeptideY in fish. Neuropeptides (2012) 46:275-83. doi:10.1016/j.npep.2012.09.006
62. Peng C, Chang JP, Yu KL, Wong AO, Van Goor F, Peter RE, et al. Neuropeptide-Y stimulates growth hormone and gonadotropin-II secretion in the goldfish pituitary: involvement of both presynaptic and pituitary cell actions. Endocrinology (1993) 132:1820-9. doi:10.1210/en.132.4.1820
63. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev (2009) 30:713-43. doi:10.1210/er.2009-0005
64. Kanda S, Oka Y. Evolutionary insights into the steroid sensitive kiss1 and kiss2 neurons in the vertebrate brain. Front Endocrinol (2012) 3:28. doi:10.3389/fendo.2012.00028
65. Akazome Y, Kanda S, Okubo K, Oka Y. Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain. J Fish Biol (2010) 76:161-82. doi:10.1111/j.1095-8649.2009.02496.x
66. Kanda S, Oka Y. Structure, synthesis, and phylogeny of kisspeptin and its receptor. In: Kauffman AS, Smith JT editors. Kisspeptin Signaling in Reproductive Biology, Advances in Experimental Medicine and Biology. Berlin: Springer (2013). p. 9-26.
67. Felip A, Zanuy S, Pineda R, Pinilla L, Carrillo M, Tena-Sempere M, et al. Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol Cell Endocrinol (2009) 312:67-71. doi:10.1016/j.mce.2008.11.017
68. Kitahashi T, Ogawa S, Parhar IS. Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology (2009) 150:821-31. doi:10.1210/en.2008-0940
69. Li S, Zhang Y, Liu Y, Huang X, Huang W, Lu D, et al. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J Endocrinol (2009) 201:407-18. doi:10.1677/JOE-09-0016
70. Selvaraj S, Ohga H, Kitano H, Nyuji M, Yamaguchi A, Matsuyama M. Peripheral administration of Kiss1 pentadecapeptide induces gonadal development in sexually immature adult scombroid fish. Zoolog Sci (2013) 30:446-54. doi:10.2108/zsj.30.446
71. Grone BP, Maruska KP, Korzan WJ, Fernald RD. Social status regulates kisspeptin receptor mRNA in the brain of Astatotilapia burtoni. Gen Comp Endocrinol (2010) 169:98-107. doi:10.1016/j.ygcen.2010.07.018
72. Escobar S, Servili A, Espigares F, Gueguen MM, Brocal I, Felip A, et al. Expression of kisspeptins and kiss receptors suggests a large range of functions for kisspeptin systems in the brain of the European sea bass. PLoS One (2013) 8:e70177. doi:10.1371/journal.pone.0070177
73. Kanda S, Akazome Y, Mitani Y, Okubo K, Oka Y. Neuroanatomical evidence that kisspeptin directly regulates isotocin and vasotocin neurons. PLoS One (2013) 8:e62776. doi:10.1371/journal.pone.0062776
74. Karigo T, Uenoyama Y, Oishi S, Fujii N, Mitani Y, Kanda S, et al. Effects of kisspeptins on LH secretion and GnRH1 neuronal activities in goldfish and medaka. 2nd World Conference Kisspeptin Singaling in the Brain. Tokyo (2012).
75. Muske L. Evolution of gonadotropin-releasing hormone (GnRH) neuronal systems. Brain Behav Evol (1993) 42:215-30. doi:10.1159/000316219
76. Millar RP. GnRH II and type II GnRH receptors. Trends Endocrinol Metab (2003) 14:35-43. doi:10.1016/S1043-2760(02)00016-4
77. Kauffman AS. Emerging functions of gonadotropin-releasing hormone II in mammalian physiology and behaviour. J Neuroendocrinol (2004) 16:794-806. doi:10.1111/j.1365-2826.2004.01229.x
78. Kauffman AS, Wills A, Millar RP, Rissman EF. Evidence that the type-2 gonadotrophin-releasing hormone (GnRH) receptor mediates the behavioural effects of GnRH-II on feeding and reproduction in musk shrews. J Neuroendocrinol (2005) 17:489-97. doi:10.1111/j.1365-2826.2005.01334.x
79. Kauffman AS, Bojkowska K, Wills A, Rissman EF. Gonadotropin-releasing hormone-II messenger ribonucleic acid and protein content in the mammalian brain are modulated by food intake. Endocrinology (2006) 147:5069-77. doi:10.1210/en.2006-0615
80. Matsuda K, Nakamura K, Shimakura SI, Miura T, Kageyama H, Uchiyama M, et al. Inhibitory effect of chicken gonadotropin-releasing hormone II on food intake in the goldfish. Carassius auratus. Horm Behav (2008) 54:83-9. doi:10.1016/j.yhbeh.2008.01.011
81. Oka Y, Matsushima T. Gonadotropin-releasing hormone (GnRH)-immunoreactive terminal nerve cells have intrinsic rhythmicity and project widely in the brain. J Neurosci (1993) 13:2161-76.
82. Abe H, Oka Y. Modulation of pacemaker activity by salmon gonadotropin-releasing hormone (sGnRH) in terminal nerve (TN)-GnRH neurons. J Neurophysiol (2000) 83:3196-200.
83. Umatani C, Abe H, Oka Y. Neuropeptide RFRP inhibits the pacemaker activity of terminal nerve GnRH neurons. J Neurophysiol (2013) 109:2354-63. doi:10.1152/jn.00712.2012
84. Schwanzel-Fukuda MS, Silverman AJ. The nervus terminalis of the guinea pig: a new luteinizing hrmone-releasing hormone (LHRH) neuronal system. J Comp Neurol (1980) 191:213-25. doi:10.1002/cne.901910205
85. Demski LS, Schwanzel-Fukuda M. The terminal nerve (nervus terminalis): structure, function, and evolution. Ann N Y Acad Sci (1987) 159:ix-xi. doi:10.1111/j.1749-6632.1987.tb36281.x
86. Demski LS, Northcutt RG. The terminal nerve: A new chemosensory system in vertebrates? Science (1983) 220:435-7. doi:10.1126/science.6836287
87. Fujita I, Sorensen PW, Stacey NE, Hara TJ. The olfactory system, not the terminal nerve, functions as the primary chemosensory pathway mediating responses to sex pheromones in male goldfish. Brain Behav Evol (1991) 38:313-21. doi:10.1159/000114397
88. Oka Y. Gonadotropin-releasing-hormone (GnRH) cells of the terminal nerve as a model neuromodulator system. Neurosci Lett (1992) 142:119-22. doi:10.1016/0304-3940(92)90353-9
89. Huang L, Li L. Characterization of voltage-activated ionic currents in the GnRH-containing terminalis nerve in transgenic zebrafish. Brain Res (2011) 1367:43-9. doi:10.1016/j.brainres.2010.10.024
90. Oka Y. Tetrodotoxin-resistant persistent Na+ current underlying pacemaker potentials of fish gonadotrophin-releasing hormone neurones. J Physiol (1995) 482:1-6.
91. Oka Y. Characterization of TTX-resistant persistent Na+ current underlying pacemaker potentials of fish gonadotropin-releasing hormone (GnRH) neurons. J Neurophysiol (1996) 75:2397-404.
92. + currents underlying pacemaker potentials of fish gonadotropin-releasing hormone cells. J Neurophysiol (1999) 81:643-53.
93. Fujita I, Satou M, Ueda K. Ganglion cells of the terminal nerve: morphology and electrophysiology. Brain Res (1985) 335:148-52. doi:10.1016/0006-8993(85)90286-0
94. Schwanzel-Fukuda M, Morrell JIP. Ontogenesis of neurons producing luteinizing hormone-releasing hormone (LHRH) in the nervus terminalis of the rat. J Comp Neurol (1985) 238:348-64. doi:10.1002/cne.902380309
95. Schwanzel-Fukuda M, Garcia MS, Morrell JIP. Distribution of luteinizing hormone-releasing hormone in the nervus terminalis and brain of the mouse detected by immunocytochemistry. J Comp Neurol (1987) 255:231-44. doi:10.1002/cne.902550207
96. Wirsig CRL. The terminal nerve projects centrally in the hamster. Neuroscience (1986) 19:709-17. doi:10.1016/0306-4522(86)90294-0
97. Wirsig CR, Leonard CM. Terminal nerve damage impairs the mating behavior of the male hamster. Brain Res (1987) 417:293-303. doi:10.1016/0006-8993(87)90454-9
98. Oka Y, Ichikawa M. Ultrastructure of the ganglion-cells of the terminal nerve in the dwarf gourami (Colisa lalia). J Comp Neurol (1991) 304:161-71. doi:10.1002/cne.903040202
99. Hajdu P, Ikemoto T, Akazome Y, Park MK, Oka Y. Terminal nerve gonadotrophin-releasing hormone (GnRH) neurones express multiple GnRH receptors in a teleost, the dwarf gourami (Colisa lalia). J Neuroendocrinol (2007) 19:475-9. doi:10.1111/j.1365-2826.2007.01553.x
100. Abe H, Oka Y. Mechanisms of the modulation of pacemaker activity by GnRH peptides in the terminal nerve-GnRH neurons. Zoolog Sci (2002) 19:111-28. doi:10.2108/zsj.19.111
101. 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) 149:3540-8. doi:10.1210/en.2008-0299
102. Michon L, Nlend Nlend R, Bavamian S, Bischoff L, Boucard N, Caille D, et al. Involvement of gap junctional communication in secretion. Biochim Biophys Acta (2005) 1719:82-101. doi:10.1016/j.bbamem.2005.11.003
103. Bartheld CS, Meyer DL. Tracing of single fibers of the nervus terminalis in the goldfish brain. Cell Tiss Res (1986) 245:143-58.
104. Amano M, Oka Y, Aida K, Okumoto N, Kawashima S, Hasegawa Y. Immunocytochemical demonstration of Salmon Gnrh and chicken Gnrh-Ii in the brain of Masu Salmon, Oncorhynchus masou. J Comp Neurol (1991) 314:587-97. doi:10.1002/cne.903140313
105. Kim MH, Oka Y, Amano M, Kobayashi M, Okuzawa K, Hasegawa Y, et al. Immunocytochemical localization of sGnRH and cGnRH-II in the brain of goldfish. Carassius auratus. J Comp Neurol (1995) 356:72-82. doi:10.1002/cne.903560105
106. 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) 355:354-68. doi:10.1002/cne.903550303
107. González-Martínez D, Zmora N, Mañanos E, Saligaut D, Zanuy S, Zohar Y, et al. Immunohistochemical localization of three different prepro-GnRHs in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides. J Comp Neurol (2002) 446:95-113. doi:10.1002/cne.10190
108. Kiya T, Oka Y. Glutamate receptors in the terminal nerve gonadotropin-releasing hormone neurons of the dwarf gourami (teleost). Neurosci Lett (2003) 345:113-6. doi:10.1016/S0304-3940(03)00503-2
109. Nakane R, Oka Y. Excitatory action of GABA in the terminal nerve gonadotropin-releasing hormone neurons. J Neurophysiol (2010) 103:1375-84. doi:10.1152/jn.00910.2009
110. Wirsig-Wiechmann CR, Oka Y. The terminal nerve ganglion cells project to the olfactory mucosa in the dwarf gourami. Neurosci Res (2002) 44:337-41. doi:10.1016/S0168-0102(02)00150-5
111. 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) 104:3518-29. doi:10.1152/jn.01027.2009
112. Clarke IJ, Qi Y, Puspita Sari I, Smith JT. Evidence that RF-amide related peptides are inhibitors of reproduction in mammals. Front Neuroendocrinol (2009) 30:371-8. doi:10.1016/j.yfrne.2009.04.001
113. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, et al. Characterization of the potent gonadotropin-releasing activity of RF9, a selective antagonist of RF-amide-related peptides and neuropeptide FF receptors: physiological and pharmacological implications. Endocrinology (2010) 151:1902-13. doi:10.1210/en.2009-1259
114. Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H. Discovery and Evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J Neuroendocrinol (2010) 22:716-27. doi:10.1111/j.1365-2826.2010.02018.x
115. Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3 (RFRP-3), a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone (GnRH) neuron firing in the mouse. Endocrinology (2009) 159:2799-804. doi:10.1210/en.2008-1623
116. Matsumoto S, Yamamoto N, Akazome Y, Yamada S, Tsukamura H, Maeda K, et al. Possible novel function of metastin neurons as dual neuromodulators in the vertebrate brain. Zool Sci (2006) 23:1189.
117. Yamamoto N, Ito H. Afferent sources to the ganglion of the terminal nerve in teleosts. J Comp Neurol (2000) 428:355-75. doi:10.1002/1096-9861(20001211)428:2<355::AID-CNE12>3.0.CO;2-W
118. Yamamoto N, Oka Y, Kawashima S. Lesions of gonadotropin-releasing hormone-immunoreactive terminal nerve cells: effects on the reproductive behavior of male dwarf gouramis. Neuroendocrinology (1997) 65:403-12. doi:10.1159/000127203
119. Wirsig CRL. Terminal nerve damage impairs the mating behavior of the male hamster. Brain Res (1987) 417:293-303. doi:10.1016/0006-8993(87)90454-9
120. Dutton A, Dyball REJ. Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol (1979) 290:433-40.
121. Liu X, Porteous R, D'Anglemont De Tassigny X, Colledge WH, Millar R, Petersen SL, et al. Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neuron excitability. J Neurosci (2011) 31:2421-30. doi:10.1523/JNEUROSCI.5759-10.2011
122. Kawai T, Abe H, Oka Y. Burst generation mediated by cholinergic input in terminal nerve-gonadotrophin releasing hormone neurones of the goldfish. J Physiol (2013). doi:10.1113/jphysiol.2013.258343
123. 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) 104:3540-50. doi:10.1152/jn.00639.2010
124. Akazome Y, Kanda S, Oka Y. Expression of vesicular glutamate transporter-2.1 in medaka terminal nerve gonadotrophin-releasing hormone neurones. J Neuroendocrinol (2011) 23:570-6. doi:10.1111/j.1365-2826.2011.02142.x
125. Hrabovszky E, Turi GF, Kallo I, Liposits Z. Expression of vesicular glutamate transporter-2 in gonadotropin-releasing hormone neurons of the adult male rat. Endocrinology (2004) 145:4018-21. doi:10.1210/en.2004-0589
126. Constantin S, Jasoni CL, Wadas B, Herbison AE. γ-Aminobutyric acid and glutamate differentially regulate intracellular calcium concentrations in mouse gonadotropin-releasing hormone neurons. Endocrinology (2010) 151:262-70. doi:10.1210/en.2009-0817
127. Fenno L, Yizhar O, Deisseroth K. The development and application of optogenetics. Ann Rev Neurosci (2011) 34:389-412. doi:10.1146/annurev-neuro-061010-113817
128. Boch J. TALEs of genome targeting. Nat Biotech (2011) 29:135-6. doi:10.1038/nbt.1767
129. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell (2013) 153:910-8. doi:10.1016/j.cell.2013.04.025