Acetylcholine-evoked after discharge in Aplysia bag cell neurons

Journal of Neurophysiology

Volumn 107, Issue 10, 2012, Pages 2672-2685

  White, Sean H ^a   Magoski, Neil S ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

conotoxin ImI; Mecamylamine; Nicotinic receptor; Plateau potential; Synaptic input

Indexed keywords

ACETYLCHOLINE; ALPHA CONOTOXIN MII; CARBACHOL; CHOLINE; GLYCINE; GUANOSINE 5' O (2 THIODIPHOSPHATE); HEXAMETHONIUM; MECAMYLAMINE; NEOSTIGMINE; NICOTINE; PEPTIDE HORMONE; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE; STRYCHNINE; TETRAMETHYLAMMONIUM; ALPHA CONOTOXIN IMI; ALPHA-CONOTOXIN IMI; CONOTOXIN; NICOTINIC AGENT;

AFTERDISCHARGE; ANIMAL CELL; APLYSIA; ARTICLE; CHOLINERGIC SYNAPSE; CONTROLLED STUDY; DEPOLARIZATION; MEMBRANE CONDUCTANCE; NERVE CELL; NERVE POTENTIAL; NONHUMAN; OVULATION; PRIORITY JOURNAL; ACTION POTENTIAL; ANIMAL; CELL CULTURE; DRUG EFFECT; MEMBRANE POTENTIAL; PHYSIOLOGY; SYNAPSE;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; APLYSIA; CELLS, CULTURED; CONOTOXINS; HEXAMETHONIUM; MECAMYLAMINE; MEMBRANE POTENTIALS; NEURONS; NICOTINIC AGONISTS; SYNAPSES;

EID: 84861114778     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00745.2011     Document Type: Article

References (111)

1. Alevizos A, Weiss KR, Koester J. Synaptic actions of identified peptidergic neuron R15 in Aplysia. II. Contraction of pleuroabdominal connectives mediated by motoneuron-L7. J Neurosci 11: 1275-1281, 1991.
2. Alkondon M, Pereira EF, Cortes WS, Maelicke A, Albuquerque EX. Choline is a selective agonist of alpha 7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9: 2734-2742, 1997.
3. Alkondon M, Pereira EF, Wonnacott S, Albuquerque EX. Blockade of nicotinic currents in hippocampal-neurons defines methyllycaconitine as a potent and specific receptor antagonist. Mol Pharmacol 41: 802-808, 1992.
4. Andrew RD, Dudek FE. Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism. Science 221: 1050-1052, 1983.
5. Arch S. Biosynthesis of the egg-laying hormone (ELH) in the bag cell neurons of Aplysia californica. J Gen Physiol 60: 102-119, 1972.
6. Ascher P. Inhibitory and excitatory effects of dopamine on Aplysia neurones. J Physiol 225: 173-209, 1972.
7. Ascher P, Large WA, Rang HP. Two modes of action of ganglionic blocking drugs. Br J Pharmacol 66: 79, 1979.
8. Ascher P, Marty A, Neild TO. Life time and elementary conductance of channels mediating excitatory effects of acetylcholine in Aplysia neurons. J Physiol 278: 177-206, 1978a.
9. Ascher P, Marty A, Neild TO. The mode of action of antagonists of excitatory response to acetylcholine in Aplysia neurons. J Physiol 278: 207-235, 1978b.
10. Begnoche VL, Moore SK, Blum N, Van GC, Mayeri E. Sign stimulus activates a peptidergic neural system controlling reproductive behavior in Aplysia. J Neurophysiol 75: 2161-2166, 1996.
11. Berry MS, Cottrell GA. Excitatory, inhibitory and biphasic synaptic potentials mediated by an identified dopamine-containing neuron. J Physiol 244: 589-612, 1975.
12. Bhattacharya BK, Feldberg W. Comparison of the effects of eserine and neostigmine on the leech muscle preparation. Br J Pharmacol 13: 151-155, 1958.
13. Bodmer R, Levitan IB. Sensitivity of Aplysia neurons in primary culture to putative neurotransmitters. J Neurobiol 15: 429-440, 1984.
14. Bradley K, Easton DM, Eccles JC. An investigation of primary or direct inhibition. J Physiol 122: 474-488, 1953.
15. Brezina V. Guanosine 5'-triphosphate analogue activates potassium current modulated by neurotransmitters in Aplysia neurones. J Physiol 407: 15-40, 1988.
16. Brierley MJ, Staras K, Benjamin PR. Behavioral function of glutamatergic interneurons in the feeding system of Lymnaea: plateauing properties and synaptic connections with motor neurons. J Neurophysiol 78: 3386-3395, 1997.
17. Brown RO, Pulst SM, Mayeri E. Neuroendocrine bag cells of Aplysia are activated by bag cell peptide-containing neurons in the pleural ganglion. J Neurophysiol 61: 1142-1152, 1989.
18. 2+ signalling. Nat Rev Neurosci 8: 182-193, 2007.
19. Byrne JH. Identification and initial characterization of a cluster of command and pattern-generating neurons underlying respiratory pumping in Aplysia californica. J Neurophysiol 49: 491-508, 1983.
20. Carpenter DO, Greene LA, Shain W, Vogel Z. Effects of eserine and neostigmine on interaction of alpha-bungarotoxin with Aplysia acetylcholine receptors. Mol Pharmacol 12: 999-1006, 1976.
21. Chiu AY, Hunkapiller MW, Heller E, Stuart DK, Hood LE, Strumwasser F. Purification and primary structure of the neuropeptide egg-laying hormone of Aplysia californica. Proc Natl Acad Sci USA 76: 6656-6660, 1979.
22. Chiu AY, Strumwasser F. An immunohistochemical study of the neuropep-tidergic bag cells of Aplysia. J Neurosci 1: 812-826, 1981.
23. Chiu AY, Strumwasser F. Two neuronal populations in the head ganglia of Aplysia californica with egg-laying hormone-like immunoreactivity. Brain Res 294: 83-93, 1984.
24. Coggeshall RE. A light and electron microscope study of abdominal ganglion of Aplysia californica. J Neurophysiol 30: 1263-1288, 1967.
25. Curtis DR, Hosli L, Johnston GA. Inhibition of spinal neurones by glycine. Nature 215: 1502-1503, 1967.
26. Dembrow NC, Jing J, Brezina V, Weiss KR. A specific synaptic pathway activates a conditional plateau potential underlying protraction phase in the Aplysia feeding central pattern generator. J Neurosci 24: 5230-5238, 2004.
27. Dembrow NC, Jing J, Proekt A, Romero A, Vilim FS, Cropper EC, Weiss KR. A newly identified buccal interneuron initiates and modulates feeding motor programs in Aplysia. J Neurophysiol 90: 2190-2204, 2003.
28. Eckstein F, Cassel D, Levkovitz H, Lowe M, Selinger Z. Guanosine 5'-O-(2-thiodiphosphate)-inhibitor of adenylate-cyclase stimulation by guanine-nucleotides and fluoride ions. J Biol Chem 254: 9829-9834, 1979.
29. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178, 2002.
30. Elliott CJ, Kemenes G. Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. II. N1 interneurons make cholinergic synapses with feeding motoneurons. Philos Trans R Soc Lond B Biol Sci 336: 167-180, 1992.
31. Elliott CJ, Stow RA, Hastwell C. Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. I, Cholinergic receptors on feeding neurons. Philos Trans R Soc Lond B Biol Sci 336: 157-166, 1992.
32. Faber DS, Klee MR. Strychnine interactions with acetylcholine, dopamine and serotonin receptors in Aplysia neurons. Brain Res 65: 109-126, 1974.
33. Ferguson GP, ter Maat A, Parsons DW, Pinsker HM. Egg laying in Aplysia. I. Behavioral patterns and muscle activity of freely behaving animals after selectively elicited bag cell discharges. J Comp Physiol A 164: 835-847, 1989a.
34. Ferguson GP, ter Maat A, Pinsker HM. Egg laying in Aplysia. II. Organization of central and peripheral pathways for initiating neurosecretory activity and behavioral patterns. J Comp Physiol A 164: 849-857, 1989b.
35. Fisher T, Lin CH, Kaczmarek LK. The peptide FMRFa terminates a discharge in Aplysia bag cell neurons by modulating calcium, potassium, and chloride conductances. J Neurophysiol 69: 2164-2173, 1993.
36. Fisher TE, Levy S, Kaczmarek LK. Transient changes in intracellular calcium associated with a prolonged increase in excitability in neurons of Aplysia californica. J Neurophysiol 71: 1254-1257, 1994.
37. Frazier WT, Kandel ER, Kupfermann I, Waziri R, Coggeshall RE. Morphological and functional properties of identified neurons in abdominal ganglion of Aplysia californica. J Neurophysiol 30: 1288-1352, 1967.
38. 2+ dependence by multiple modulators. J Neurophysiol 102: 259-271, 2009.
39. Gardner D, Kandel ER. Physiological and kinetic-properties of cholinergic receptors activated by multi-action interneurons in buccal ganglia of Aplysia. J Neurophysiol 40: 333-348, 1977.
40. 2+ entry through a non-selective cation channel in Aplysia bag cell neurons. Neuroscience 162:1023-1038, 2009.
41. Giller E, Schwartz JH. Choline acetyltransferase: regional distribution in the abdominal ganglion of Aplysia. Science 161: 908-911, 1968.
42. Giller E, Schwartz JH. Acetylcholinesterase in identified neurons of abdominal ganglion of Aplysia californica. J Neurophysiol 34: 108-123, 1971.
43. Haj-Dahmane S, Andrade R. Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J Neurosci 16: 3848-3861, 1996.
44. Haskins JT, Price CH, Blankenship JE. A light and electron microscopic investigation of the neurosecretory bag cells of Aplysia. J Neurocytol 10: 729-747, 1981.
45. Hung AY, Magoski NS. Activity-dependent initiation of a prolonged depolarization in Aplysia bag cell neurons: role for a cation channel. J Neurophysiol 97: 2465-2479, 2007.
46. Hurwitz I, Kupfermann I, Weiss KR. Fast synaptic connections from CBIs to pattern-generating neurons in Aplysia: initiation and modification of motor programs. J Neurophysiol 89: 2120-2136, 2003.
47. Jennings KR, Host JJ, Kaczmarek LK, Strumwasser F. Serotonergic inhibition of afterdischarge in peptidergic bag cells. J Neurobiol 12: 579-590, 1981.
48. Johnson DS, Martinez J, Elgoyhen AB, Heinemann SF, McIntosh JM. Alpha-Conotoxin ImI exhibits subtype-specific nicotinic acetylcholine receptor blockade: preferential inhibition of homomeric alpha 7 and alpha 9 receptors. Mol Pharmacol 48: 194-199, 1995.
49. Kaczmarek LK, Jennings K, Strumwasser F. Neurotransmitter modulation, phosphodiesterase inhibitor effects, and cyclic AMP correlates of afterdischarge in peptidergic neurites. Proc Natl Acad Sci USA 75: 5200-5204, 1978.
50. Kaczmarek LK, Jennings KR, Strumwasser F. An early sodium and a late calcium phase in the afterdischarge of peptide-secreting neurons of Aplysia. Brain Res 238: 105-115, 1982.
51. Kaczmarek LK, Strumwasser F. The expression of long lasting afterdischarge by isolated Aplysia bag cell neurons. J Neurosci 1: 626-634, 1981.
52. Kauer JA, Kaczmarek LK. Peptidergic neurons of Aplysia lose their response to cyclic adenosine 3':5'-monophosphate during a prolonged refractory period. J Neurosci 5: 1339-1345, 1985.
53. Kehoe J. Ionic mechanisms of a two-component cholinergic inhibition in Aplysia neurones. J Physiol 225: 85-114, 1972a.
54. Kehoe J. The physiological role of three acetylcholine receptors in synaptic transmission in Aplysia. J Physiol 225: 147-172, 1972b.
55. Kehoe J. Three acetylcholine receptors in Aplysia neurones. J Physiol 225: 115-146, 1972c.
56. + conductance increase in Aplysia neurons that appears to be independent of G-proteins. Neuron 13: 691-702, 1994.
57. Kehoe J, McIntosh JM. Two distinct nicotinic receptors, one pharmacologically similar to the vertebrate alpha 7-containing receptor, mediate Cl~ currents in Aplysia neurons. J Neurosci 18: 8198-8213, 1998.
58. Koester J. Chemically and electrically coupled interneurons mediate respiratory pumping in Aplysia. J Neurophysiol 62: 1113-1126, 1989.
59. Koester J, Alevizos A. Innervation of the kidney of Aplysia by L10, the LUQ cells, and an identified peripheral motoneuron. J Neurosci 9: 4078-4088, 1989.
60. Kupfermann I, Kandel ER. Electrophysiological properties and functional interconnections of two symmetrical neurosecretory clusters (bag cells) in abdominal ganglion of Aplysia. J Neurophysiol 33: 865-876, 1970.
61. Laurienti PJ, Blankenship JE. Properties of cholinergic responses in isolated parapodial muscle fibers of Aplysia. J Neurophysiol 82: 778-786, 1999.
62. Lemos JR, Levitan IB. Intracellular injection of guanyl nucleotides alters the serotonin-induced increase in potassium conductance in Aplysia neuron R15. J Gen Physiol 83: 269-285, 1984
63. 2+-dependent regulation of a non-selective cation channel from Aplysia bag cell neurones. J Physiol 575: 491-506, 2006.
64. Magoski NS. Regulation of an Aplysia bag cell neuron cation channel by closely associated protein kinase A and a protein phosphatase. J Neurosci 24: 6833-6841, 2004.
65. Magoski NS, Bauce LG, Syed NI, Bulloch AGM. Dopaminergic transmission between identified neurons from the mollusk, Lymnaea stagnalis. J Neurophysiol 74: 1287-1300, 1995.
66. Magoski NS, Kaczmarek LK. Association/dissociation of a channel-kinase complex underlies state-dependent modulation. J Neurosci 25: 8037-8047, 2005.
67. 2+ release in Aplysia bag cell neurones. J Physiol 522: 271-283, 2000.
68. Marty A, Neild T, Ascher P. Voltage sensitivity of acetylcholine currents in Aplysia neurones in the presence of curare. Nature 261: 501-503, 1976.
69. Mayeri E, Brownell P, Branton WD. Multiple, prolonged actions of neuroendocrine bag cells on neurons in Aplysia. II. Effects on beating pacemaker and silent neurons. J Neurophysiol 42: 1185-1197, 1979a.
70. Mayeri E, Brownell P, Branton WD, Simon SB. Multiple, prolonged actions of neuro-endocrine bag cells on neurons in Aplysia. I. Effects on bursting pacemaker neurons. J Neurophysiol 42: 1165-1184, 1979b.
71. McCaman RE, Dewhurst SA. Choline acetyltransferase in individual neurons of Aplysia californica. J Neurochem 17: 1421-1426, 1970.
72. McIntosh JM, Yoshikami D, Mahe E, Nielsen DB, Rivier JE, Gray WR, Olivera BM. A nicotinic acetylcholine-receptor ligand of unique specificity, alpha-conotoxin-ImI. J Biol Chem 269: 16733-16739, 1994.
73. Mogg AJ, Whiteaker P, McIntosh JM, Marks M, Collins AC, Wonnacott S. Methyllycaconitine is a potent antagonist of alpha-conotoxin-MII-sensi-tive presynaptic nicotinic acetylcholine receptors in rat striatum. J Pharmacol Exp Ther 302: 197-204, 2002.
74. Painter SD, Kalman VK, Nagle GT, Blankenship JE. Localization of immunoreactive alpha-bag-cell peptide in the central nervous system of Aplysia. J Comp Neurol 287: 515-530, 1989.
75. Papke RL, Bencherif M, Lippiello P. An evaluation of neuronal nicotinic acetylcholine receptor activation by quaternary nitrogen compounds indicates that choline is selective for the alpha 7 subtype. Neurosci Lett 213: 201-204, 1996.
76. Paton WDM, Zaimis EJ. Clinical potentialities of certain bisquaternary salts causing neuromuscular and ganglionic block. Nature 162:810, 1948.
77. Piomelli D, Shapiro E, Feinmark SJ, Schwartz JH. Metabolites of arachi-donic-acid in the nervous-system of Aplysia-possible mediators of synaptic modulation. J Neurosci 7: 3675-3686, 1987a.
78. Piomelli D, Volterra A, Dale N, Siegelbaum SA, Kandel ER, Schwartz JH, Belardetti F. Lipoxygenase metabolites of arachidonic-acid as second messengers for presynaptic inhibition of Aplysia sensory cells. Nature 328: 38-43, 1987b.
79. Redman RS, Berry RW. Temperature-dependent stimulation and inhibition of adenylate cyclase by Aplysia bag cell peptides. Brain Res Mol Brain Res 17: 245-250, 1993.
80. Rubakhin SS, Li LJ, Moroz TP, Sweedler JV. Characterization of the Aplysia californica cerebral ganglion F cluster. J Neurophysiol 81: 1251-1260, 1999.
81. Schaefer M, Brownell PH. Modulation of a respiratory motor program by peptide-secreting neurons in Aplysia. J Neurobiol 17: 121-126, 1986.
82. 3H]acetylcholine in rat brain. Mol Pharmacol 22: 56-62, 1982.
83. Shope SB, McPherson D, Rock MK, Blankenship JE. Functional and morphological evidence for the existence of neurites from abdominal ganglion bag cell neurons in the head-ring ganglia of Aplysia. J Comp Physiol A 168: 539-552, 1991.
84. Sigvardt KA, Rothman BS, Brown RO, Mayeri E. The bag cells of Aplysia as a multitransmitter system: identification of alpha bag cell peptide as a second neurotransmitter. J Neurosci 6: 803-813, 1986.
85. Slater NT, Filbert M, Carpenter DO. Multiple interactions of anticholinesterases with Aplysia acetylcholine responses. Brain Res 375: 407-412, 1986.
86. Smock T, Arch S. A cytochemical study of the bag cell organs of Aplysia californica. J Histochem Cytochem 25: 1345-1350, 1977.
87. Soinila S, Mpitsos GJ. Immunohistochemistry of diverging and converging neurotransmitter systems in mollusks. Biol Bull 181: 484-499, 1991.
88. Stone CA, Torchiana ML, Navarro A, Beyer KH. Ganglionic blocking properties of 3-methylamino-isocamphane hydrochloride (mecamylamine)-a secondary amine. J Pharmacol Exp Ther 117: 169-183, 1956.
89. Straub VA, Staras K, Kemenes G, Benjamin PR. Endogenous and network properties of Lymnaea feeding central pattern generator interneurons. J Neurophysiol 88: 1569-1583, 2002.
90. Strumwasser F, Kaczmarek LK, Chiu AY, Heller E, Jennings KR, Viele DP. Peptides controlling behavior in Aplysia. Soc Gen Physiol Ser 35: 197-218, 1980.
91. Susswein AJ, Rosen SC, Gapon S, Kupfermann I. Characterization of buccal motor programs elicited by a cholinergic agonist applied to the cerebral ganglion of Aplysia californica. J Comp Physiol A 179: 509-524, 1996.
92. Swayne LA, Mezghrani A, Varrault A, Chemin J, Bertrand G, Dalle S, Bourinet E, Lory P, Miller RJ, Nargeot J, Monteil A. The NALCN ion channel is activated by M3 muscarinic receptors in a pancreatic beta-cell line. EMBO Rep 10: 873-880, 2009.
93. Tahvildari B, Alonso AA, Bourque CW. Ionic basis of ON and OFF persistent activity in layer III lateral entorhinal cortical principal neurons. J Neurophysiol 99: 2006-2011, 2008.
94. Tai C, Hines DJ, Choi HB, MacVicar BA. Plasma membrane insertion of TRPC5 channels contributes to the cholinergic plateau potential in hip-pocampal CA1 pyramidal neurons. Hippocampus 21: 958-967, 2011.
95. Tam AKH, Gardam KE, Lamb S, Kachoei BA, Magoski NS. Role for protein kinase c in controlling Aplysia bag cell neuron excitability. Neuro-science 179: 41-55, 2011.
96. 2+ current contributes to a prolonged depolarization in Aplysia bag cell neurons. J Neurophysiol 102: 3753-3765, 2009.
97. Tauc L, Gerschenfeld HM. Cholinergic transmission mechanisms for both excitation and inhibition in molluscan central synapses. Nature 192: 366-367, 1961.
98. ter Maat A, Roubos EW, Lodder JC, Buma P. Integration of biphasic synaptic input by electrotonically coupled neuroendocrine caudodorsal cells in the pond snail. J Neurophysiol 49: 1392-1409, 1983.
99. ter Maat A, Lodder JC. A biphasic cholinergic input on the ovulation hormone producing caudo-dorsal cells of the fresh-water snail Lymnaea stagnalis. Comp Biochem Physiol C 66: 115-119, 1980.
100. Tieman TL, Steel DJ, Gor Y, Kehoe J, Schwartz JH, Feinmark SJ. A pertussis toxin-sensitive 8-lipoxygenase pathway is activated by a nicotinic acetylcholine receptor in Aplysia neurons. J Neurophysiol 85: 2150-2158, 2001.
101. Ueki S, Domino EF, Koketsu K. Effects of mecamylamine on the Golgi recurrent collateral-Renshaw-cell synapse in spinal cord. Exp Neurol 3: 141-148, 1961.
102. van Nierop P, Keramidas A, Bertrand S, van Minnen J, Gouwenberg Y, Bertrand D, Smit AB. Identification of molluscan nicotinic acetylcholine receptor (nAChR) subunits involved in formation of cation- and anion-selective nAChRs. J Neurosci 25: 10617-10626, 2005.
103. Ward JM, Cockcroft VB, Lunt GG, Smillie FS, Wonnacott S. Methylly-caconitine-a selective probe for neuronal alpha-bungarotoxin binding-sites. FEBS Lett 270: 45-48, 1990.
104. Wayne NL, Lee W, Kim YJ. Persistent activation of calcium-activated and calcium-independent protein kinase C in response to electrical afterdis-charge from peptidergic neurons of Aplysia. Brain Res 834: 211-213, 1999.
105. Weiss S, Goldberg JI, Edstrom JP, Lukowiak K. Cholinergic receptors in the Aplysia gill. J Neurobiol 15: 325-332, 1984.
106. 2+-sensitive nonspecific cation channel underlying prolonged repetitive firing in Aplysia neurons. J Neurosci 16: 3661-3671, 1996.
107. 2+/calmodulin-CaMKII pathway in dopamine neurons. Neurosci Res 47: 225-232, 2003.
108. Yan HD, Villalobos C, Andrade R. TRPC channels mediate a muscarinic receptor-induced afterdepolarization in cerebral cortex. J Neurosci 29: 10038-10046, 2009.
109. + current contributes to the long-lasting refractory period of Aplysia bag cell neurons. J Neurosci 22: 10134-10141, 2002.
110. Zhang Z, Reboreda A, Alonso A, Barker PA, Seguela P. TRPC channels underlie cholinergic plateau potentials and persistent activity in entorhinal cortex. Hippocampus 21: 386-397, 2011.
111. Zhang Z, Seguela P. Metabotropic induction of persistent activity in layers II/III of anterior cingulate cortex. Cereb Cortex 20: 2948-2957, 2010.