Computational model of the serotonergic modulation of sensory neurons in Aplysia

Journal of Neurophysiology

Volumn 82, Issue 6, 1999, Pages 2914-2935

  Baxter, Douglas A ^a   Canavier, Carmen C ^a,c   Clark Jr , John W ^b   Byrne, John H ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b Rice University   (United States)

^c UNIVERSITY OF NEW ORLEANS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; PHORBOL ESTER; POTASSIUM; PROTEIN KINASE C; SEROTONIN;

APLYSIA; ARTICLE; CALCIUM CURRENT; CONTROLLED STUDY; HODGKIN HUXLEY EQUATION; ION CONDUCTANCE; LEARNING; MATHEMATICAL MODEL; MEMBRANE CURRENT; MEMORY; MODULATION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE POTENTIAL; POTASSIUM CURRENT; PRIORITY JOURNAL; SENSORY NERVE CELL; SEROTONINERGIC SYSTEM; VOLTAGE CLAMP; WITHDRAWAL REFLEX;

EID: 0033377610     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.82.6.2914     Document Type: Article

References (90)

1. ABRAMS, T. W., CASTELLUCCI, V. F., CAMARDO, J. S., KANDEL, E. R., AND LLOYD, P. E. Two endogenous neuropeptides modulate the gill and siphon withdrawal reflex in Aplysia by presynaptic facilitation involving cAMP-dependent closure of a serotonin-sensitive potassium channel. Proc. Natl. Acad. Sci. USA 81: 7956-7960, 1984.
2. ADAMS, D. J. AND GAGE, P. W. Characteristics of sodium and calcium conductance changes produced by membrane depolarization in an Aplysia neuron. J. Physiol (Lond.) 289: 143-161, 1979a.
3. ADAMS, D. J. AND GAGE, P. W. Ionic currents in response to membrane depolarization in an Aplysia neurone. J. Physiol. (Lond.) 289: 115-141, 1979b.
4. ALMERS, W. Gating currents and charge movements in excitability membranes. Rev. Physiol. Biochem. Pharmocol. 82: 96-190, 1978.
5. ANDRESEN, M. C. AND BROWN, A. M. Photoresponses of a sensitive extraretinal photoreceptor in Aplysia. J. Physiol. (Lond.) 287: 267-282, 1979.
6. BACSKAI, B. J., HOCHNER, B., MAHAUT-SMITH, M., ADAMS, S. R., KAANG, B. K., KANDEL, E. R., AND TSIEN, R. Y. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neruons. Science 260: 222-226, 1993.
7. BAXTER, D. A. AND BYRNE, J. H. Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia. J. Neurophysiol. 62: 655-679, 1989.
8. BAXTER, D. A. AND BYRNE, J. H. Differential effects of cAMP and serotonin on membrane current, action potential duration, and excitability in somata of pleural sensory neurons of Aplysia. J. Neurophysiol. 64: 978-990, 1990a.
9. + currents by forskolin is not mediated via cAMP in pleural sensory neurons of Aplysia. J. Neurophysiol. 64: 1474-1483, 1990b.
10. BAXTER, D. A. AND BYRNE, J. H. Java implementation of SNNAP (Simulator for Neural Networks and Action Potentials) expands access to neural simulation software. Soc. Neurosci. Abstr. 25: 246, 1999.
11. BELARDETTI, F., SCHACHER, S., AND SIEGELBAUM, S. A. Action potentials, macroscopic, and single channel currents recorded from growth cones of Aplysia neurons in culture. J. Physiol. (Lond.) 374: 289-313, 1986.
12. BERNIER, L., CASTELLUCCI, V. F., KANDEL, E. R., AND SCHWARTZ, J. H. Facilitatory transmitter causes a selective and prolonged increase in adensoine 3′: 5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex in Aplysia. J. Neurosci. 2: 1682-1691, 1982.
13. 2+ imaging in Aplysia sensory neurons. Biophys. J. 63: 1146-1164, 1992.
14. 2+ current of the sensory neurons in. Aplysia. J. Neurosci. 13: 1839-1851, 1993.
15. BREZINA, V., ECKERT, R., AND ERXLEBEN, C. Modulation of potassium conductances by an endogenous neuropeptide in neurones of Aplysia californica. J. Physiol. (Lond.) 382: 267-290, 1987.
16. BYRNE, J. H. Analysis of ionic conductance mechanisms in motor cells mediating inking behavior in Aplysia californica. J. Neurophysiol. 43: 630-650, 1980a.
17. BYRNE, J. H. Quantitative aspects of ionic conductance mechanisms contributing to firing pattern of motor cells mediating inking behavior in Aplysia californica. J. Neurophysiol. 43: 651-668, 1980b.
18. BYRNE, J. H. AND KANDEL, E. R. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16: 425-435, 1996.
19. CANAVIER, C. C., CLARK, J. W., AND BYRNE, J. H. Simulation of the bursting activity of neuron R15 in Aplysia: role of ionic currents, calcium balance, and modulatory transmitters. J. Neurophysiol. 66: 2107-2124, 1991.
20. CASTELLUCCI, V. F., NAIRN, A., GREENGARD, P, SCHWARTZ, J. H., AND KANDEL, E. R. Inhibitor of adenosine 3′: 5′-monophosphate-dependent protein kinase blocks presynaptic facilitation in Aplysia. J. Neurosci. 2: 1673-1681, 1982.
21. CLEARY, L. J., LEE, W. L., AND BYRNE, J. H. Cellular correlates of long-term sensitization in Aplysia. J. Neurosci. 18: 5988-5998, 1998.
22. CRITZ, S. D., BAXTER, D. A., AND BYRNE, J. H. Modulatory effects of serotonin, FMRFamide, and myomodulin on the duration of action potentials, excitability, and membrane currents in tail sensory neurons of Aplysia. J. Neurophysiol. 66: 1912-1926, 1991.
23. K,Ca by phorbol ester-mediated activation of PKC in pleural sensory neurons of Aplsyia. J. Neurophysiol. 68: 1079-1086, 1992.
24. DALE, N., KANDEL, E. R., AND SCHACHER, S. Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis. J. Neurosci. 7: 2232-2238, 1987.
25. ECKERT, R. AND CHAD, J. E. Inactivation of Ca channels. Prog. Biophys. Mol. Biol. 44: 215-267, 1984.
26. EDMONDS, B., KLEIN, M., DALE, N., AND KANDEL, E. R. Contributions of two types of calcium channels to synaptic transmission and plasticity. Science 250: 1142-1147, 1990.
27. ELIOT, L. S., HAWKINS, R. D, KANDEL, E. R., AND SCHACHER, S. Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture. J. Neurosci. 14: 368-383, 1994.
28. 2+ influx in presynaptic facilitation. Nature 361: 634-637, 1993.
29. 2+ currents in identifiable cerebral A neurons of Aplysia. Cell. Mol. Neurobiol. 4: 97-115, 1984.
30. 2+ current underlying the action potential in bag cells of two species of Aplysia. J. Exp. Biol. 198: 2337-2347, 1995.
31. GHIRARDI, M. BRAHA, O., HOCHNER, B. MONTAROLO, P. G., KANDEL, E. R., AND DALE, N. Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron 9: 479-489, 1992.
32. GILLY, W. R., GILLETTE, R., AND MCFARLANE, M. Fast and slow activation kinetics of voltage-gated sodium channels in molluscan neurons. J. Neurophysiol. 77: 2373-2384, 1997.
33. GINGRICH, K. J. AND BYRNE, J. H. Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neruons mediating gill-withdrawal reflex in Aplysia. J. Neurophysiol. 53: 652-659, 1985.
34. GINGRICH, K. J., BAXTER, D. A., AND BYRNE, J. H. Mathematical model of cellular mechanisms contributing to presynaptic facilitation. Brain Res. Bull. 21: 513-520, 1988.
35. + currents, increasing spike duration and excitability in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 89: 11481-11485, 1992.
36. GORMAN, A.L.F. AND MARMOR, M. F. Temperature dependence of the sodium-potassium permeability ratio of a molluscan neurone. J. Physiol. (Lond.) 210: 919-931, 1970.
37. GORMAN, A.L.F. AND MIROLLI, M. The passive electrical properties of the membrane of a molluscan neurone. J. Physiol. (Lond.) 227: 35-40, 1972.
38. HERMAN, A. AND GORMAN, A.L.F. Effects of tetraethylammonium on potassium currents in a molluscan neuron. J. Gen. Physiol. 78: 87-110, 1981.
39. HILLE, B. Ionic Channels of Excitable Membrane (2nd ed.). Sunderland, MA: Sinauer, 1992.
40. + current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc. Natl. Acad. Sci. USA 89: 11476-11480, 1992.
41. HOCHNER, R., KLEIN, M., SCHACHER, S., AND KANDEL, E. R. Action-potential duration and the modulation of transmitter release from the sensory neurons of Aplysia in presynaptic facilitation and behavioral sensitization. Proc. Natl. Acad. Sci. USA 83: 8410-8414, 1986a.
42. HOCHNER, R., KLEIN, M., SCHACHER, S., AND KANDEL, E. R. Additional component in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proc. Natl. Acad. Sci. USA 83: 8794-8798, 1986b.
43. B and serotonin differ in efficacy both in modulating cellular properties and in activating adenylyl cyclase: implications for mechanisms underlying presynaptic facilitation. Brain Res. 616: 188-199, 1993.
44. JOHNSTON, D. Voltage, temperature and ionic dependence of the slow outward current in Aplysia burst-firing neurons. J. Physiol. (Lond.) 298: 145-157, 1980.
45. JOYNER, R. W. Temperature effects on neuronal elements. Fed. Proc. 40: 2814-2818, 1981.
46. KANDEL, E. R. AND SCHWARTZ, J. H. Molecular biology of learning: modulation of transmitter release. Science 218: 433-443, 1982.
47. KLEIN, M. Differential cyclic AMP dependence of facilitation at Aplysia sensorimotor synapses as a function of prior stimulation: augmentation versus restoration of transmitter release. J. Neurosci. 13: 3793-3801, 1993.
48. KLEIN, M., CAMARDO, J., AND KANDEL, E. R. Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proc. Natl. Acad. Sci. USA 79: 5713-5717, 1982.
49. KLEIN, M., HOCHNER, B., AND KANDEL, E. R. Facilitatory transmitters and cAMP can modulate accommodation as well as transmitter release in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 83: 7994-7998, 1986.
50. 2+ current: mechanism for behavioral sensitization in Aplysia californica. Proc. Natl. Acad. Sci. USA 75: 3512-3516, 1978.
51. 2+ current. J. Exp. Biol. 89: 117-157, 1980.
52. MANSEAU, F., SOSSIN, W. S., AND CASTELLUCCI, V. F. Long-term changes in excitability induced by protein kinase C activation in Aplysia sensory neurons. J. Neurophysiol. 79: 1210-1218, 1998.
53. MERCER, A. R., EMPTAGE, N. J., AND CAREW, T. J. Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. Science 254: 1811-1813, 1991.
54. MICHAEL, D., MARTIN, K. C., SEGER, R., NING, M.-M, BASTON, R., AND KANDEL, E. R. Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc. Natl. Acad. Sci. USA 95: 1864-1869, 1998.
55. MIROLLI, M. AND TALBOTT, S. The geometrical factors determining the electrotonic properties of a molluscan neurone. J. Physiol. (Lond.) 227: 19-34, 1972.
56. NAKANISHI, K., ZHANG, F., BAXTER, D. A., ESKIN, A., AND BYRNE, J. H. Role of calcium-calmodulin dependent protein kinase II modulation of sensorimotor synapses in. Aplysia. J. Neurophysiol. 78: 409-416, 1997.
57. B). Neurosci. Lett. 55: 113-118, 1985.
58. PARTRIDGE, L. D. AND CONNOR, J. A. A mechanism for minimizing temperature effects on repetitive firing frequency. Am. J. Physiol. 234 (Cell Physiol. 3): C155-C161, 1978.
59. PIERONI, J. P. AND BYRNE, J. H. Differential effects of serotonin, FMRMamide, small cardioactive peptide on multiple, distributed processes modulating sensorimotor synaptic transmission in Aplysia. J. Neurosci. 12: 2633-2647, 1992.
60. POLLOCK, J. D. AND CAMARDO, J. Regulation of single potassium channels by serotonin in the cell bodies of the tail mechanosensory neurons of Aplysia californica. Brain Res. 410: 367-370, 1987.
61. POLLOCK, J. D., CAMARDO, J., AND BERNIER, L. Serotonin and cyclic adenosine 3′: 5′-monophosphate modulate the S potassium current in tail sensory neurons in the pleural ganglion of Aplysia. J. Neurosci. 5: 1862-1871, 1985.
62. ROMEY, G., CHICHEPORTICHE, R., AND LAZDUNSKI, M. Transition temperatures of the electrical activity of ion channels in the nerve membrane. Biochim. Biophys. Acta 602: 610-20, 1980.
63. SACKTOR, T. C. AND SCHWARTZ, J. H. Sensitizing stimuli cause translocation of protein kinase C in Aplsyia sensory neurons. Proc. Natl. Acad. Sci. USA 87: 2036-2039, 1990.
64. SAH, P., GIBB, A. J., AND GAGE, P. W. The sodium current underlying action potentials in guinea pig hippocampal CA1 neurons. J. Gen. Physiol. 91: 373-398, 1988.
65. SCHOLZ, K. P. AND BYRNE, J. H. Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235: 1249-1254, 1987.
66. + channels in Aplysia sensory neurons. J. Physiol. (Lond.) 440: 601-621, 1991.
67. + channels of Aplysia sensory neurons in cell-free membrane patches. Nature. 313: 392-395, 1985.
68. SHUSTER, M. J. AND SIEGELBAUM, S. A. Pharmacological characterization of the serotonin-sensitive potassium channel of Aplysia sensory neurons. J. Gen. Physiol. 90: 587-608, 1987.
69. SIEGELBAUM, S. A., BELARDETTI, F., CAMARDO, J. S., AND SHUSTER, M. J. Modulation of the serotonin-sensitive potassium channel in Aplysia sensory neurone cell body and growth cone. J. Exp. Biol. 124: 287-306, 1986.
70. + channels in Aplysia sensory neurons. Nature 299: 413-417, 1982.
71. 2+-independent protein kinase C Apl II. Learn. Mem. 3: 389-401, 1997.
72. SOSSIN, W. S., SACKTOR, T. C., AND SCHWARTZ, J. H. Persistent activation of protein kinase C during the development of long-term facilitation in Aplysia. Learn. Mem. 1: 189-202, 1994.
73. 2+-activated PKCs in Aplysia neurons by 5-HT. J. Neurosci. 12: 1160-1168, 1992.
74. STARK, L. L. AND CAREW, T. J. Developmental dissociation of serotonin-induced spike broadening and synaptic facilitation in Aplysia sensory neurons. J. Neurosci. 19: 334-346, 1999.
75. STARK, L. L., MERCER, A. R., EMPTAGE, N. J., AND CAREW, T. W. Pharmacological and kinetic characterization of two functional classes of serotonergic modulation in Aplysia sensory neurons. J. Neurophysiol. 75: 855-865, 1996.
76. SUGITA, S., BAXTER, D. A., AND BYRNE, J. H. Activators of protein kinase C mimic serotonin-induced modulation of a voltage-dependent potassium current in pleural sensory neurons of Aplysia. J. Neurophysiol. 72: 1240-1249, 1994a.
77. SUGITA, S., BAXTER, D. A., AND BYRNE, J. H. cAMP-independent effects of 8-(4-parachlorophenylthio)-cyclic AMP on spike duration and membrane currents in pleural sensory neurons of Aplysia. J. Neurophysiol. 72: 1250-1259, 1994b.
78. SUGITA, S., BAXTER, D. A., AND BYRNE, J. H. Modulation of a cAMP/protein kinase A cascade by protein kinase C in sensory neurons of Aplysia. J. Neurosci. 17: 7237-7244, 1997a.
79. SUGITA, S., BAXTER, D. A., AND BYRNE, J. H. Differential effects of 4-amino-pyridine, serotonin and phorbol esters on facilitation of sensorimotor connections in Aplysia. J. Neurophysiol. 77: 177-185, 1997b.
80. SUGITA, S., GOLDSMITH, J. R., BAXTER, D. A., AND BYRNE, J. H. Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation in sensorimotor connections of Aplysia. J. Neurophysiol. 68: 643-651, 1992.
81. THOMPSON, S. M., MASUKAWA, L. A., AND PRINCE, D. A. Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro. J. Neurosci. 5: 817-824, 1985.
82. THOMPSON, S., SMITH, S. J., AND JOHNSON, J. W. Slow outward tail currents in molluscan bursting pacemaker neurons: two components differing in temperature sensitivity. J. Neurosci. 6: 3169-3176, 1986.
83. TSIEN, R. W., LIPSCOMBE, D., MADISON, D. V., BLEY, K. R., AND FOX, A. P. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci. 11: 431-438, 1988.
84. + current in tail sensory neurons of Aplysia: role of serotonin and cAMP. J. Neurophysiol. 61: 32-44, 1989.
85. WALTERS, E. T., BYRNE, J. H., CAREW, T. J., AND KANDEL, E. R. Mechanoafferent neurons innervating the tail of Aplysia. II. Modulation by sensitizing stimulation. J. Neurophysiol. 50: 1543-1559, 1983.
86. WHITE, J. A., BAXTER, D. A., AND BYRNE, J. H. Analysis of the modulation by serotonin of a voltage-dependent potassium current in sensory neurons of Aplysia. Biophysical J. 66: 710-718, 1994.
87. WRIGHT, W. G. AND KIRSCHMAN, D. Direct comparison of serotonin effects on siphon versus tail sensory neurons in Aplysia. Learn. Mem. 2: 178-184, 1995.
88. WRIGHT, W. G., KIRSCHMAN, D., ROZEN, D., AND MAYNARD, B. Phyolgenetic analysis of learning-related neuromodulation in molluscan mechanosensory neurons. Evolution 50: 2248-2263, 1996.
89. YAMADA, W. M., KOCH, C., AND ADAMS, P. R. Multipe channels and calcium dynamics. In: Methods in Neronal Modeling: From Ions to Networks, Second Edition, edited by C. Koch and I. Segev. Cambridge, MA: The MIT Press, 1998, p. 137-170.
90. ZIV, I., BAXTER, D. A., AND BYRNE, J. H. Simulator for neural networks and action potentials: description and application. J. Neurophysiol. 71: 294-308, 1994.