Burst Firing in Gonadotrophin-Releasing Hormone Neurones does not Require Ionotrophic GABA or Glutamate Receptor Activation

Journal of Neuroendocrinology

Volumn 24, Issue 12, 2012, Pages 1476-1483

  Lee, K ^a   Liu, X ^a   Herbison, A E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Burst firing; GABA; Glutamate; GnRH; LHRH

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMPA RECEPTOR; BICUCULLINE; GLUTAMATE RECEPTOR; GONADORELIN; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PICROTOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BURST FIRING; CLUSTER ANALYSIS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CONDUCTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CELLS, CULTURED; GABA-A RECEPTOR ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GONADOTROPIN-RELEASING HORMONE; MALE; MICE; MICE, TRANSGENIC; N-METHYLASPARTATE; NEURONS; ORGAN CULTURE TECHNIQUES; RECEPTORS, GABA-A; RECEPTORS, IONOTROPIC GLUTAMATE; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

EID: 84869835968     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02360.x     Document Type: Article

References (55)

1. Herbison AE. Physiology of the GnRH neuronal network. In: Neill JD, ed. Knobil and Neill's Physiology of Reproduction, 3rd ed. San Diego, CA: Academic Press, 2006: 1415-1482.
2. Leng G, Brown D. The origins and significance of pulsatility in hormone secretion from the pituitary. J Neuroendocrinol 1997; 9: 493-513.
3. Brown CH, Bourque CW. Mechanisms of rhythmogenesis: insights from hypothalamic vasopressin neurons. Trends Neurosci 2006; 29: 108-115.
4. Moenter SM, Anthony DeFazio R, Pitts GR, Nunemaker CS. Mechanisms underlying episodic gonadotropin-releasing hormone secretion. Front Neuroendocrinol 2003; 24: 79-93.
5. Kelly MJ, Wagner EJ. GnRH neurons and episodic bursting activity. Trends Endocrinol Metab 2002; 13: 409-410.
6. Kuehl-Kovarik MC, Pouliot WA, Halterman GL, Handa RJ, Dudek FE, Partin KM. Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J Neurosci 2002; 22: 2313-2322.
7. Kuehl-Kovarik MC, Partin KM, Handa RJ, Dudek FE. Spike-dependent depolarizing afterpotentials contribute to endogenous bursting in gonadotropin releasing hormone neurons. Neuroscience 2005; 134: 295-300.
8. Chu Z, Moenter SM. Physiologic regulation of a tetrodotoxin-sensitive sodium influx that mediates a slow afterdepolarization potential in gonadotropin-releasing hormone neurons: possible implications for the central regulation of fertility. J Neurosci 2006; 26: 11961-11973.
9. Lee K, Duan W, Sneyd J, Herbison AE. Two slow calcium-activated afterhyperpolarization currents control burst firing dynamics in gonadotropin-releasing hormone neurons. J Neurosci 2010; 30: 6214-6224.
10. Kato M, Tanaka N, Usui S, Sakuma Y. The SK channel blocker apamin inhibits slow afterhyperpolarization currents in rat gonadotropin-releasing hormone neurones. J Physiol 2006; 574: 431-442.
11. Liu X, Herbison AE. Small-conductance calcium-activated potassium channels control excitability and firing dynamics in gonadotropin-releasing hormone (GnRH) neurons. Endocrinology 2008; 149: 3598-3604.
12. Bond CT, Maylie J, Adelman JP. SK channels in excitability, pacemaking and synaptic integration. Curr Opin Neurobiol 2005; 15: 305-311.
13. Sah P, Faber ES. Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 2002; 66: 345-353.
14. Haug T, Storm JF. Protein kinase A mediates the modulation of the slow Ca(2+)-dependent K(+) current, I(sAHP), by the neuropeptides CRF, VIP, and CGRP in hippocampal pyramidal neurons. J Neurophysiol 2000; 83: 2071-2079.
15. Nissen R, Hu B, Renaud LP. Regulation of spontaneous phasic firing of rat supraoptic vasopressin neurones in vivo by glutamate receptors. J Physiol 1995; 484: 415-424.
16. Voisin DL, Herbison AE, Poulain DA. Central inhibitory effects of muscimol and bicuculline on the milk ejection reflex in the anaesthetized rat. J Physiol 1995; 483: 211-224.
17. Brown CH, Bull PM, Bourque CW. Phasic bursts in rat magnocellular neurosecretory cells are not intrinsically regenerative in vivo. Eur J Neurosci 2004; 19: 2977-2983.
18. Israel JM, Poulain DA, Oliet SH. Glutamatergic inputs contribute to phasic activity in vasopressin neurons. J Neurosci 2010; 30: 1221-1232.
19. A receptor signalling in native GnRH neurons. Eur J Neurosci 2000; 12: 3497-3504.
20. Spergel DJ, Kruth U, Hanley DF, Sprengel R, Seeburg PH. GABA-and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurone in transgenic mice. J Neurosci 1999; 19: 2037-2050.
21. Sullivan SD, Moenter SM. Gamma-aminobutyric acid neurons integrate and rapidly transmit permissive and inhibitory metabolic cues to gonadotropin-releasing hormone neurons. Endocrinology 2004; 145: 1194-1202.
22. Herbison AE, Moenter SM. Depolarising and hyperpolarising actions of GABA(A) receptor activation on gonadotrophin-releasing hormone neurones: towards an emerging consensus. J Neuroendocrinol 2011; 23: 557-569.
23. Lee K, Porteous R, Campbell RE, Luscher B, Herbison AE. Knockdown of GABA(A) receptor signaling in GnRH neurons has minimal effects upon fertility. Endocrinology 2010; 151: 4428-4436.
24. Penatti CA, Davis MC, Porter DM, Henderson LP. Altered GABAA receptor-mediated synaptic transmission disrupts the firing of gonadotropin-releasing hormone neurons in male mice under conditions that mimic steroid abuse. J Neurosci 2010; 30: 6497-6506.
25. Liu X, Porteous R, d'Anglemont de Tassigny X, Colledge WH, Millar R, Petersen SL, Herbison AE. Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neuron excitability. J Neurosci 2011; 31: 2421-2430.
26. Liu X, Herbison AE. Estrous cycle- and sex-dependent changes in pre- and postsynaptic GABAB control of GnRH neuron excitability. Endocrinology 2011; 152: 4856-4864.
27. Moenter SM, DeFazio RA. Endogenous gamma-aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology 2005; 146: 5374-5379.
28. Han SK, Todman MG, Herbison AE. Endogenous GABA release inhibits the firing of adult gonadotropin-releasing hormone neurons. Endocrinology 2004; 145: 495-499.
29. Bhattarai JP, Park SA, Park JB, Lee SY, Herbison AE, Ryu PD, Han SK. Tonic extrasynaptic GABA(A) receptor currents control gonadotropin-releasing hormone neuron excitability in the mouse. Endocrinology 2011; 152: 1551-1561.
30. Abe H, Terasawa E. Firing pattern and rapid modulation of activity by estrogen in primate luteinizing hormone releasing hormone-1 neurons. Endocrinology 2005; 146: 4312-4320.
31. Nunemaker CS, Straume M, DeFazio RA, Moenter SM. Gonadotropin-releasing hormone neurons generate interacting rhythms in multiple time domains. Endocrinology 2003; 144: 823-831.
32. 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: 3731-3736.
33. Constantin S, Wray S. Gonadotropin-releasing hormone-1 neuronal activity is independent of cyclic nucleotide-gated channels. Endocrinology 2008; 149: 279-290.
34. Moore JP Jr, Shang E, Wray S. In situ GABAergic modulation of synchronous gonadotropin releasing hormone-1 neuronal activity. J Neurosci 2002; 22: 8932-8941.
35. Constantin S, Klenke U, Wray S. The calcium oscillator of GnRH-1 neurons is developmentally regulated. Endocrinology 2010; 151: 3863-3873.
36. Nunemaker CS, DeFazio RA, Moenter SM. Estradiol-sensitive afferents modulate long-term episodic firing patterns of GnRH neurons. Endocrinology 2002; 143: 2284-2292.
37. Penatti CA, Oberlander JG, Davis MC, Porter DM, Henderson LP. Chronic exposure to anabolic androgenic steroids alters activity and synaptic function in neuroendocrine control regions of the female mouse. Neuropharmacology 2011; 61: 653-664.
38. Lobb CJ, Wilson CJ, Paladini CA. A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons. J Neurophysiol 2010; 104: 403-413.
39. Shao LR, Dudek FE. Both synaptic and intrinsic mechanisms underlie the different properties of population bursts in the hippocampal CA3 area of immature versus adult rats. J Physiol 2009; 587: 5907-5923.
40. Cope DW, Hughes SW, Crunelli V. GABAA receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 2005; 25: 11553-11563.
41. Duan W, Lee K, Herbison AE, Sneyd J. A mathematical model of adult GnRH neurons in mouse brain and its bifurcation analysis. J Theor Biol 2011; 276: 22-34.
42. Chu Z, Takagi H, Moenter SM. Hyperpolarization-activated currents in gonadotropin-releasing hormone (GnRH) neurons contribute to intrinsic excitability and are regulated by gonadal steroid feedback. J Neurosci 2010; 30: 13373-13383.
43. Bosma MM. Ion channel properties and episodic activity in isolated immortalized gonadotropin-releasing hormone (GnRH) neurons. J Membr Biol 1993; 136: 85-96.
44. Krsmanovic LZ, Mores N, Navarro CE, Arora KK, Catt KJ. An agonist-induced switch in G protein coupling of the gonadotropin-releasing hormone receptor regulates pulsatile neuropeptide secretion. Proc Natl Acad Sci USA 2003; 100: 2969-2974.
45. Campbell RE, Gaidamaka G, Han SK, Herbison AE. Dendro-dendritic bundling and shared synapses between gonadotropin-releasing hormone neurons. Proc Natl Acad Sci USA 2009; 106: 10835-10840.
46. Campbell RE, Ducret E, Porteous R, Liu X, Herde MK, Wellerhaus K, Sonntag S, Willecke K, Herbison AE. Gap junctions between neuronal inputs but not gonadotropin-releasing hormone neurons control estrous cycles in the mouse. Endocrinology 2011; 152: 2290-2301.
47. Han SK, Chong W, Li LH, Lee IS, Murase K, Ryu PD. Noradrenaline excites and inhibits GABAergic transmission in parvocellular neurons of rat hypothalamic paraventricular nucleus. J Neurophysiol 2002; 87: 2287-2296.
48. Xu C, Xu XZ, Nunemaker CS, Moenter SM. Dose-dependent switch in response of gonadotropin-releasing hormone (GnRH) neurons to GnRH mediated through the type I GnRH receptor. Endocrinology 2004; 145: 728-735.
49. Christian CA, Moenter SM. Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology 2008; 149: 3130-3136.
50. Bhattarai JP, Kaszas A, Park SA, Yin H, Park SJ, Herbison AE, Han SK, Abraham IM. Somatostatin inhibition of gonadotropin-releasing hormone neurons in female and male mice. Endocrinology 2010; 151: 3258-3266.
51. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone (GnRH) neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25: 11349-11356.
52. Xu J, Kirigiti MA, Cowley MA, Grove KL, Smith MS. Suppression of basal spontaneous gonadotropin-releasing hormone neuronal activity during lactation: role of inhibitory effects of neuropeptide Y. Endocrinology 2009; 150: 333-340.
53. Todman MG, Han SK, Herbison AE. Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience 2005; 132: 703-712.
54. Clasadonte J, Poulain P, Beauvillain JC, Prevot V. Activation of neuronal nitric oxide release inhibits spontaneous firing in adult gonadotropin-releasing hormone neurons: a possible local synchronizing signal. Endocrinology 2008; 149: 587-596.
55. Farkas I, Kallo I, Deli L, Vida B, Hrabovszky E, Fekete C, Moenter SM, Watanabe M, Liposits Z. Retrograde endocannabinoid signaling reduces GABAergic synaptic transmission to gonadotropin-releasing hormone neurons. Endocrinology 2010; 151: 5818-5829.