Regulation of Electrical Bursting in a Spatiotemporal Model of a GnRH Neuron

Bulletin of Mathematical Biology

Volumn 75, Issue 10, 2013, Pages 1941-1960

  Chen, Xingjiang ^a   Iremonger, Karl ^b   Herbison, Allan ^b   Kirk, Vivien ^a   Sneyd, James ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Bursting; Cable model; Diffusion; Gonadotropin releasing hormone

Indexed keywords

MAMMALIA;

GONADORELIN;

ACTION POTENTIAL; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOLOGY; CALCIUM SIGNALING; CYTOLOGY; HYPOTHALAMUS; MATHEMATICAL PHENOMENA; NERVE CELL; NERVE CONDUCTION; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; COMPUTATIONAL BIOLOGY; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; MATHEMATICAL CONCEPTS; MODELS, NEUROLOGICAL; NEURAL CONDUCTION; NEURONS;

EID: 84885084117     PISSN: 00928240     EISSN: 15229602     Source Type: Journal    
DOI: 10.1007/s11538-013-9877-7     Document Type: Article

References (53)

1. Alle, H., & Geiger, J. R. P. (2006). Combined analog and action potential coding in hippocampal mossy fibers. Science, 311, 1290-1293.
2. Andersen, P., Soleng, A. F., & Raastad, M. (2000). The hippocampal lamella hypothesis revisited. Brain Res., 886, 165-171.
3. Antic, S. D. (2003). Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol., 550(1), 35-50.
4. Campbell, R. E., & Suter, K. J. (2010). Redefining the gonadotrophin-releasing hormone neurone dendrite. J. Neuroendocrinol., 22, 650-658.
5. Campbell, R. E., Han, S. K., & Herbison, A. E. (2005). Biocytin filling of adult gonadotropin releasing hormone neurons in situ reveals extensive, spiny, dendritic processes. Endocrinology, 146, 1163-1169.
6. Campbell, R. E., Gaidamaka, G., Han, S. K., & Herbison, A. E. (2009). Dendro-dendritic bundling and shared synapses between gonadotropin-releasing hormone neurons. Proc. Natl. Acad. Sci. USA, 106, 10835-10840.
7. Casale, A. E., & McCormick, D. A. (2011). Active action potential propagation but not initiation in thalamic interneuron dendrites. J. Neurosci., 31(50), 18289-18302.
8. Christian, C. A., & Moenter, S. M. (2008). Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology, 149(6), 3130-3136.
9. Chu, Z., & Moenter, S. M. (2006). 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., 26(46), 11961-11973.
10. Chu, Z., Takagi, H., & Moenter, S. M. (2010). Hyperpolarization-activated currents in gonadotropin-releasing hormone (GnRH) neurons contribute to intrinsic excitability and are regulated by gonadal steroid feedback. J. Neurosci., 30(40), 13373-13383.
11. Constantin, J., & Charles, A. (1999). Spontaneous action potentials initiate rhythmic intercellular calcium waves in immortalized hypothalamic (GT1-1) neurons. J. Neurophysiol., 82, 429-435.
12. Cserscik, D., Farkas, I., Hrabovszky, E., & Liposits, Z. (2012). A simple integrative electrophysiological model of bursting GnRH neurons. J. Comput. Neurosci., 32, 119-136.
13. Debanne, D., Campanac, E., Bialowas, A., Carlier, E., & Alcaraz, G. (2011). Axon physiology. Physiol. Rev., 91, 555-602.
14. Djurisic, M., Antic, S., Chen, W. R., & Zecevic, D. (2004). Voltage imaging from dendrites of mitral cells: EPSP attenuation and spike trigger zones. J. Neurosci., 24(30), 6703-6714.
15. Duan, W., Lee, K., Herbison, A. E., & Sneyd, J. (2011). A mathematical model of adult GnRH neurons in mouse brain and its bifurcation analysis. J. Theor. Biol., 276, 22-34.
16. Fletcher, P., & Li, Y. (2009). An integrated model of electrical spiking, bursting, and calcium oscillations in GnRH neurons. Biophys. J., 96, 4514-4524.
17. Foust, A., Popovic, M., Zecevic, D., & McCormick, D. A. (2010). Action potentials initiate in the axon initial segment and propagate through axon collaterals reliably in cerebellar Purkinje neurons. J. Neurosci., 30(20), 6891-6902.
18. Gerhold, L. M., & Wise, P. M. (2006). Vasoactive intestinal polypeptide regulates dynamic changes in astrocyte morphometry: impact on gonadotropin-releasing hormone neurons. Endocrinology, 147(5), 2197-2202.
19. Gerhold, L. M., Rosewell, K. L., & Wise, P. M. (2005). Suppression of vasoactive intestinal polypeptide in the suprachiasmatic nucleus leads to aging-like alterations in cAMP rhythms and activation of gonadotropin-releasing hormone neurons. J. Neurosci., 25(1), 62-67.
20. Gin, E., Falcke, M., Wagner, L. E. II., Yule, D. I., & Sneyd, J. (2009). A kinetic model of the inositol trisphosphate receptor based on single-channel data. Biophys. J., 96, 4053-4062.
21. Herbison, A. E. (2006). Physiology of the GnRH neuronal network. In J. D. Neill (Ed.), Knobil and Neill's physiology of reproduction (3rd ed.) (pp. 1415-1482). San Diego: Academic Press.
22. A receptor activation on gonadotrophin-releasing hormone neurones: towards and emerging consensus. J. Neuroendocrinol., 23, 557-569.
23. Herbison, A. E., Pape, J. R., Skynner, S. X., & Sim, J. A. (2001). Molecular and cellular properties of GnRH neurons revealed through transgenics in the mouse. Mol. Cell. Endocrinol., 185, 185-194.
24. Iremonger, K. J., & Herbison, A. E. (2012). Initiation and propagation of action potentials in GnRH neuron dendrites. J. Neurosci., 32(1), 151-158.
25. Jasoni, C. L., Todman, M. G., Strumia, M. M., & Herbison, A. E. (2007). Cell type-specific expression of a genetically encoded calcium indicator reveals intrinsic calcium oscillations in adult gonadotropin-releasing hormone neurons. J. Neurosci., 27, 860-867.
26. Keener, J., & Sneyd, J. (2008). Mathematical physiology (2nd ed.). New York: Springer.
27. Kole, M. H. P., Letzkus, J. J., & Stuart, G. (2007). Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron, 55, 633-647.
28. Kole, M. H. P., Ilschner, S. U., Kampa, B. M., Williams, S. R., Ruben, P. C., & Stuart, G. J. (2008). Action potential generation requires a high sodium channel density in the axon initial segment. Nat. Neurosci., 11, 178-186.
29. Kress, G. J., Dowling, M., Meeks, J. P., & Mennerick, S. (2008). High threshold, proximal initiation, and slow conduction velocity of action potentials in dentate granule neuron mossy fibers. J. Neurophysiol., 100, 281-291.
30. Krueppel, R., Remy, S., & Beck, H. (2011). Dendritic integration in hippocampal dentate granule cells. Neuron, 71, 512-528.
31. 2+ mobilizing and adenylyl cyclase-coupled receptors. J. Neurosci., 20, 9290-9297.
32. Lee, K., Duan, W., Sneyd, J., & Herbison, A. E. (2010). The slow calcium-activated afterhyperpolarization currents control burst firing dynamics in gonadotropin-releasing hormone neurons. J. Neurosci., 20(18), 6214-6224.
33. Lee, K., Liu, X., & Herbison, A. E. (2012). Burst firing in gonadotropin-releasing hormone neurons does not require ionotropic GABA or glutamate receptor activation. J. Neuroendocrinol. doi: 10. 1111/j. 1365-2826. 2012. 02360. x.
34. Liu, X., Porteous, R., d'Anglemont de Tassigny, X., Colledge, W. H., Millar, R., Petersen, S. L., & Herbison, A. E. (2011). Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neuron excitability. J. Neurosci., 31(7), 2421-2430.
35. Martinez, D. L. E. G., Choi, A. L., & Weiner, R. I. (1992). Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: intrinsic properties of the GT1-1 GnRH neuronal cell line. Proc. Natl. Acad. Sci. USA, 89, 1852-1855.
36. Meeks, J. P., & Mennerick, S. (2007). Action potential initiation and propagation in CA3 pyramidal axons. J. Neurophysiol., 97, 3460-3472.
37. Mellon, P. L., Windle, J. J., Goldsmith, P. C., Padula, C. A., Roberts, J. L., & Weiner, R. I. (1990). Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron, 5, 1-10.
38. Moenter, S. M., DeFazio, A. R., Pitts, G. R., & Nunemaker, C. S. (2003). Mechanisms underlying episodic gonadotropin-releasing hormone secretion. Front. Neuroendocrinol., 24, 79-93.
39. 2+. Proc. Natl. Acad. Sci. USA, 98, 3197-3202.
40. Nevian, T., Larkum, M. E., Polsky, A., & Schiller, J. (2007). Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat. Neurosci., 10(2), 206-214.
41. Palmer, L. M., Clark, B. A., Gründemann, J., Roth, A., Stuart, G. J., & Häusser, M. (2010). Initiation of simple and complex spikes in cerebellar Purkinje cells. J. Physiol., 588(10), 1709-1717.
42. Roberts, C. B., Best, J. A., & Suter, K. J. (2006). Dendritic processing of excitatory synaptic input in hypothalamic gonadotropin releasing-hormone (GnRH) neurons. Endocrinology, 147, 1545-1555.
43. Roberts, C. B., Campbell, R. E., Herbison, A. E., & Suter, K. J. (2008). Dendritic action potential initiation in hypothalamic gonadotropin-releasing hormone neurons. Endocrinology, 149, 3355-3360.
44. Roberts, C., O'Boyle, M., & Suter, K. (2009). Dendrites determine the contribution of after depolarization potentials (ADPs) to generation of repetitive action potentials in hypothalamic gonadotropin releasing-hormone (GnRH) neurons. J. Comput. Neurosci., 26, 39-53.
45. Sasaki, T., Matsuki, N., & Ikegaya, Y. (2011). Action-potential modulation during axonal conduction. Science, 331, 599.
46. Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. (2008). Action potential initiation and propagation in hippocampal mossy fibre axons. J. Physiol., 586(7), 1849-1857.
47. Shu, Y., Hasenstaub, A., Duque, A., Yu, Y., & McCormick, D. A. (2006). Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature, 441, 761-765.
48. Shu, Y., Duque, A., Yu, Y., Haider, B., & McCormick, D. D. (2007). Properties of action-potential initiation in neocortical pyramidal cells: evidence from whole cell axon recordings. J. Neurophysiol., 97, 746-760.
49. Spergel, D., Kruth, U., Hanley, D., Sprengel, R., & Seeburg, P. (1999). GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J. Neurophysiol., 19, 2037-2050.
50. Suter, K. J., Wuarin, J. P., Smith, B. N., Dudek, F. E., & Moenter, S. M. (2000). Whole-cell recordings from hypothalamic slices reveal burst firing in gonadotropin-releasing hormone (GnRH) neurons identified with green fluorescent protein (GFP) in transgenic mice. Endocrinology, 141, 3731-3736.
51. van Goor, F., Krsmanovic, L., Catt, K., & Stojilkovic, S. (1999a). Coordinate regulation of gonadotropin-releasing hormone neuronal firing patterns by cytosolic calcium and store depletion. Proc. Natl. Acad. Sci. USA, 96, 4101-4106.
52. van Goor, F., Krsmanovic, L., Catt, K., & Stojilkovic, S. (1999b). Control of action potential-driven calcium influx in GT1 neurons by the activation status of sodium and calcium channels. Mol. Endocrinol., 13, 587-603.
53. 2+ signaling in GnRH-secreting neurons. Biophys. J., 79, 1310-1323.