Slow Synaptic Transmission in Frog Sympathetic Ganglia
10.1242/jeb.124.1.259
Crossref journal-article
The Company of Biologists
Journal of Experimental Biology (237)
Abstract

ABSTRACT Bullfrog ganglia contain two classes of neurone, B and C cells, which receive different inputs and exhibit different slow synaptic potentials. B cells, to which most effort has been directed, possess slow and late slow EPSPs. The sEPSP reflects a muscarinic action of acetylcholine released from boutons on B cells, whereas the late sEPSP is caused by a peptide (similar to teleost LHRH) released from boutons on C cells. During either sEPSP there is a selective reduction in two slow potassium conductances, designated ‘M’ and ‘AHP’. The M conductance is voltage dependent and the AHP conductance is calcium dependent. Normally they act synergistically to prevent repetitive firing of action potentials during maintained stimuli. Computer simulation of the interactions of these conductances with the other five voltagedependent conductances present in the membrane allows a complete reconstruction of the effects of slow synaptic transmission on electrical behaviour.

Bibliography

Adams, P. R., Jones, S. W., Pennefather, P., Brown, D. A., Koch, C., & Lancaster, B. (1986). Slow Synaptic Transmission in Frog Sympathetic Ganglia. Journal of Experimental Biology, 124(1), 259–285.

Authors 6
  1. P. R. Adams (first)
  2. S. W. Jones (additional)
  3. P. Pennefather (additional)
  4. D. A. Brown (additional)
  5. C. Koch (additional)
  6. B. Lancaster (additional)
References 80 Referenced 64
  1. 10.1111/j.1476-5381.1980.tb14547.x / Br. J. Pharmac / Luteinizing hormone-releasing factor and muscarinic agonists act on the same voltage-sensitive K+-current in bullfrog sympathetic neurones by Adams (1980)
  2. 10.1113/jphysiol.1982.sp014412 / J. Physiol., Lond / Synaptic inhibition of the M-current: Slow excitatory postsynaptic potential mechanism in bullfrog sympathetic neurones by Adams (1982)
  3. {'key': '2023051712530761100_JEXBIO_124_1_259C3', 'first-page': '215a', 'article-title': 'Effects of phorbol ester on slow potassium currents of bullfrog ganglion cells', 'volume': '49', 'author': 'Adams', 'year': '1986', 'journal-title': 'Biophys. J'} / Biophys. J / Effects of phorbol ester on slow potassium currents of bullfrog ganglion cells by Adams (1986)
  4. 10.1113/jphysiol.1982.sp014357 / J. Physiol., Lond / M-currents and other potassium currents in bullfrog sympathetic neurones by Adams (1982)
  5. 10.1113/jphysiol.1982.sp014411 / J. Physiol., Lond / Pharmacological inhibition of the M-current by Adams (1982)
  6. {'key': '2023051712530761100_JEXBIO_124_1_259C6', 'article-title': 'Calcium-activated potassium channels in bullfrog sympathetic ganglion cells', 'volume-title': 'In Calcium in Biological Systems', 'author': 'Adams', 'year': '1984'} / In Calcium in Biological Systems / Calcium-activated potassium channels in bullfrog sympathetic ganglion cells by Adams (1984)
  7. 10.1111/j.1476-5381.1983.tb11004.x / Br.J. Pharmac / Substance P inhibits the M-current in bullfrog sympathetic neurones by Adams (1983)
  8. 10.1038/296746a0 / Nature, Lond / Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones by Adams; (1982)
  9. {'key': '2023051712530761100_JEXBIO_124_1_259C9', 'article-title': 'Voltage-dependent currents of vertebrate neurones and their role in membrane excitability', 'volume-title': 'Advances in Neurology', 'author': 'Adams', 'year': '1986'} / Advances in Neurology / Voltage-dependent currents of vertebrate neurones and their role in membrane excitability by Adams (1986)
  10. 10.1016/S0006-3495(85)83930-8 / Biophys. J / Spike after hyperpolarization (AHPs) in bullfrog sympathetic ganglion “B” cells by Adams (1985)
  11. 10.1113/jphysiol.1984.sp015264 / J. Physiol., Lond / Slow excitatory post-synaptic currents in bullfrog sympathetic neurones by Akasu (1984)
  12. 10.1016/0006-8993(83)91157-5 / Brain Res / Modulatory actions of ATP on membrane potentials of bullfrog sympathetic ganglion cells by Akasu (1983)
  13. 10.1016/0304-3940(83)90240-9 / Neurosci. Letts / Substance P inhibits the action potentials in bullfrog sympathetic ganglion cells by Akasu (1983)
  14. 10.1113/jphysiol.1982.sp014370 / J. Physiol., Lond / Properties of calcium-activated potassium channels in cultured rat muscle by Barrett (1982)
  15. {'key': '2023051712530761100_JEXBIO_124_1_259C15', 'first-page': '500', 'article-title': 'Slow voltage dependent potassium conductance in sensory neurons is muscarine insensitive', 'volume': '9', 'author': 'Barry', 'year': '1983', 'journal-title': 'Soc. Neurosci. Abstr.'} / Soc. Neurosci. Abstr. / Slow voltage dependent potassium conductance in sensory neurons is muscarine insensitive by Barry (1983)
  16. 10.1016/0304-3940(84)90558-5 / Neurosci. Letts / Patch-clamp study of the tetrodotoxin-resistant sodium current in group C sensory neurones by Bossu (1984)
  17. 10.1038/317538a0 / Nature, Lond / Uncoupling of cardiac muscarinic and /J-adrenergic receptors from ion channels by aguarme nucleotide analogue by Breitwieser (1985)
  18. 10.1038/283673a0 / Nature, Lond / Muscarinic suppression of a novel voltage-sensitive K+-current in a vertebrate neurone by Brown (1980)
  19. {'key': '2023051712530761100_JEXBIO_124_1_259C19', 'first-page': '252', 'article-title': 'Calcium-dependence of a component of transient outward current in bullfrog ganglion cells', 'volume': '8', 'author': 'Brown', 'year': '1982', 'journal-title': 'Soc. Neurosci. Abstr'} / Soc. Neurosci. Abstr / Calcium-dependence of a component of transient outward current in bullfrog ganglion cells by Brown (1982)
  20. 10.1113/jphysiol.1985.sp015554 / J. Physiol., Lond, (in press) / Two components of muscarine-sensitive membrane current in rat sympathetic neurones by Brown (1985)
  21. 10.1113/jphysiol.1985.sp015556 / J. Physiol., Lond / Effects of apamin, quinine and neuromuscular blockers on calcium-activated potassium channels in guinea-pig hepatocytes by Cook (1985)
  22. 10.1113/jphysiol.1984.sp015285 / J. Physiol., Lond / Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells by Cole (1984)
  23. 10.1113/jphysiol.1971.sp009366 / J. Physiol., Lond / Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma by Connor (1971)
  24. 10.1113/jphysiol.1983.sp014491 / J. Physiol., Lond / A reclassification of B and C neurones in the 9th and 10th paravertebral sympathetic ganglia of the bullfrog by Dodd (1983)
  25. 10.1113/jphysiol.1983.sp014494 / J. Physiol., Lond / Muscarinic inhibition of sympathetic C neurones in the bullfrog by Dodd (1983)
  26. 10.1113/jphysiol.1981.sp013865 / J. Physiol., Lond / Evidence for the existence of three types of potassium channels in the frog Ranvier node membrane by Dubois (1981)
  27. 10.1016/0143-4179(80)90006-2 / Neuropeptides / Characterization of LRF-like immunoreactivity in the frog sympathetic ganglia: non-identity with LRF decapeptide by Eiden (1980)
  28. 10.1038/313577a0 / Nature, Lond / Functional innervation of cultured hippocampal neurones by cholinergic afferents from co-cultured septal expiants by Gahwiler (1985)
  29. {'key': '2023051712530761100_JEXBIO_124_1_259C29', 'article-title': 'Current and voltage responses from human neocortical neurones in vitro', 'volume-title': 'J. Physiol., Lond. (in press)', 'author': 'Halltwell', 'year': '1986'} / J. Physiol., Lond. (in press) / Current and voltage responses from human neocortical neurones in vitro by Halltwell (1986)
  30. 10.1016/0006-8993(82)90954-4 / Brain Res / Voltage-clamp analysis of muscarinic excitation in hippocampal neurons by Halliwell (1982)
  31. 10.1083/jcb.86.1.6 / J. Cell Biol / Distribution of muscarinic acetylcholine receptors and presynaptic nerve terminals in amphibian heart by Hartzell (1980)
  32. {'key': '2023051712530761100_JEXBIO_124_1_259C32', 'first-page': '577', 'article-title': 'Muscarine increases tyrosine 3-monoxy-genase activity and phospholipid metabolism in the superior cervical ganglion of the rat', 'volume': '229', 'author': 'Horwitz', 'year': '1984', 'journal-title': 'J. Pharmac. exp. Ther'} / J. Pharmac. exp. Ther / Muscarine increases tyrosine 3-monoxy-genase activity and phospholipid metabolism in the superior cervical ganglion of the rat by Horwitz (1984)
  33. 10.1002/j.1460-2075.1982.tb01293.x / EMBO J / The Ca2+-dependent slow K+ conductance in cultured rat muscle cells: characterization with apamin by Hugues (1982)
  34. 10.1113/jphysiol.1982.sp014228 / J. Physiol., Lond / Peptidergic transmission in sympathetic ganglia of the frog by Jan (1982)
  35. 10.1073/pnas.76.3.1501 / Proc. natn. Acad. Sci. U.S.A / A peptide as possible transmitter in sympathetic ganglia of the frog by Jan (1979)
  36. 10.1073/pnas.77.8.5008 / Proc. natn. Acad. Sci. U.S.A / Further evidence for peptidergic transmission in sympathetic ganglia by Jan (1980)
  37. 10.1016/0143-4160(83)90019-2 / Cell Calcium / Calcium-activated potassium channels in liver cells by Jenkinson (1983)
  38. {'key': '2023051712530761100_JEXBIO_124_1_259C38', 'first-page': '207', 'article-title': 'Muscarinic and peptidergic actions on C cells of bullfrog sympathetic ganglia', 'volume': '10', 'author': 'Jones', 'year': '1984', 'journal-title': 'Soc. Neurosci. Abstr'} / Soc. Neurosci. Abstr / Muscarinic and peptidergic actions on C cells of bullfrog sympathetic ganglia by Jones (1984)
  39. 10.1113/jphysiol.1985.sp015785 / J. Physiol., Lond / Muscarinic and peptidergic excitation of bullfrog sympathetic neurones by Jones (1985)
  40. 10.1523/JNEUROSCI.04-02-00420.1984 / J. Neurosci / Teleost luteinizing hormone-releasing hormone: action on bullfrog sympathetic ganglia is consistent with role as neurotransmitter by Jones (1984)
  41. 10.1113/jphysiol.1982.sp014455 / J. Physiol., Lond / Voltage-clamp analysis of peptidergic slow depolarizations in bullfrog sympathetic ganglion cells by Katayama (1982)
  42. 10.2170/jjphysiol.34.945 / Jap. J. Physiol / Modulation of receptor sensitivity and action potentials by transmitters in vertebrate neurones by Koketsu (1984)
  43. 10.1113/jphysiol.1980.sp013079 / J. Physiol., Lond / Release of calcium ions linked to the activation of potassium conductance in a caffeine-treated sympathetic neurone by Kuba (1980)
  44. 10.1016/0301-0082(78)90010-2 / Png. Neurobiol / Synaptic events in sympathetic ganglia by Kuba (1978)
  45. 10.1007/BF00592737 / Pflûgers Arch. ges. Physiol / Characteristics of fast excitatory postsynaptic currents in bullfrog sympathetic ganglion cells by Kuba (1979)
  46. 10.1113/jphysiol.1983.sp014805 / J. Physiol., Lond / Peptidergic and muscarinic excitation at amphibian sympathetic synapses by Kuffler (1983)
  47. 10.1152/jn.1986.55.6.1268 / J. Neurophysiol, (in press) / Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons by Lancaster (1986)
  48. {'key': '2023051712530761100_JEXBIO_124_1_259C48', 'article-title': 'Potassium currents in bullfrog ganglion cells evoked by brief depolarizations', 'volume-title': 'J. Physiol., Lond. (in press)', 'author': 'Lancaster', 'year': '1986'} / J. Physiol., Lond. (in press) / Potassium currents in bullfrog ganglion cells evoked by brief depolarizations by Lancaster (1986)
  49. 10.1073/pnas.78.11.7200 / Proc. natn. Acad. Sci. U.S.A / Kinetic parameters for acetylcholine interaction in intact neuromuscular junction by Land (1981)
  50. 10.1085/jgp.75.1.39 / J. gen. Physiol / Voltage clamp study of fast excitatory synaptic currents in bullfrog sympathetic ganglion cells by Macdermott (1980)
  51. 10.1038/296746a0 / Nature, Lond / Action potential repolarization may involve a transient, Ca2+-sensitive outward current in a vertebrate neurone by Macdermott (1982)
  52. 10.1113/jphysiol.1984.sp015378 / J. Physiol., Lond / Control of the repetitive discharge of rat CAI pyramidal neurones in vitro by Madison (1984)
  53. 10.1073/pnas.78.3.1948 / Proc. natn. Acad. Sci. U.S.A / Synaptic localization of a bungarotoxin binding which blocks nicotinic transmission at frog sympathetic neurones by Marshall (1981)
  54. 10.1038/317621a0 / Nature, Lond / Presynaptic control of synaptic channel kinetics in sympathetic neurones by Marshall (1985)
  55. 10.1038/291497a0 / Nature, Lond / Ca-dependent K channels with large unitary conductance in chromaffin cell membranes by Marty (1981)
  56. 10.1007/BF01170825 / J. Neurocytol / Plasma membrane structure at the axon hillock, initial segment and cell body of frog dorsal root ganglion cells by Matsumoto (1985)
  57. 10.1038/313316a0 / Nature, Lond / Charybdotoxin, a protein inhibitor of single Ca2+-activated IK channels from mammalian skeletal muscle by Miller (1985)
  58. 10.1085/jgp.82.4.511 / J, gen. Physiol / Gating kinetic of Ca2+ activated K+ channels from rat muscle incorporated into planar lipid bilayer membranes: Evidence for two voltage dependent Ca2+ binding reactions by Moczydlowski (1983)
  59. 10.1085/jgp.58.1.36 / J. gen. Physiol / TWO fast transient current components during voltage clamp on snail neurones by Neher (1971)
  60. 10.1016/0006-8993(84)90412-8 / Brain Res / ( + )-Tubocurarine blocks the Ca2+-dependent K+-channel of the bullfrog sympathetic ganglion cell by Nohmi (1984)
  61. 10.1038/316440a0 / Nature, Lond / Three types of neuronal calcium channel with different calcium agonist sensitivity by Nowycky (1983)
  62. 10.1113/jphysiol.1985.sp015724 / J. Physiol., Lond / Calcium-activated potassium channels in rat muscle inactivate from a short duration open state by Pallotta (1985)
  63. {'key': '2023051712530761100_JEXBIO_124_1_259C63', 'first-page': '148', 'article-title': 'Modulation of repetitive firing in bullfrog sympathetic ganglion cells by two distinct K currents, IM and IAHP. SOC.', 'volume': '11', 'author': 'Pennefather', 'year': '1985', 'journal-title': 'Neurosci. Abstr'} / Neurosci. Abstr / Modulation of repetitive firing in bullfrog sympathetic ganglion cells by two distinct K currents, IM and IAHP. SOC. by Pennefather (1985)
  64. 10.1073/pnas.82.9.3040 / Proc. natn. Acad. Sci. U.S.A / Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cells by Pennefather (1985)
  65. 10.1038/317536a0 / Nature, Lond / GTP-binding proteins couple cardiac muscarinic receptors to a K channel by Pfaffinger (1985)
  66. 10.1016/0006-291X(84)91355-X / Biochem. biophys. Res. Commun / The coexistence in rat muscle cells of two distinct classes of Ca2+-dependent K+ channels with different pharmacological properties and different physiological functions by Romey (1984)
  67. 10.1038/303250a0 / Nature, Lond / Acetylcholine activation of single muscarinic K+ channels in isolated pacemaker cells of the mammalian heart by Sakmann (1983)
  68. 10.1113/jphysiol.1983.sp014649 / J. Physiol., Lond / Ion currents in Drosophila flight muscle by Salkoff (1983)
  69. 10.1113/jphysiol.1983.sp014882 / J. Physiol., Lond / The number of synaptic boutons terminating on Xenopus cardiac ganglion cells is directly correlated with cell size by Sargent (1983)
  70. 10.1073/pnas.80.9.2794 / Proc. natn. Acad. Sci. U.S.A / Characterization of a teleost gonadotropin-releasing hormone by Sherwood (1983)
  71. 10.1126/science.188131 / Science / Synaptic transmission: Long-term potentiation by a post-synaptic mechanism by Schulman (1976)
  72. 10.1038/304350a0 / Nature, Lond / Detection of intracellular Ca2+ transients in sympathetic neurones using arsenazo III by Smith (1983)
  73. 10.1038/306067a0 / Nature, Lond / Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol 1,4,5-trisphosphate by Streb (1983)
  74. 10.1016/0165-1838(84)90049-3 / J, auton. nerv. Syst / Muscarinic agonists depress calcium dependent gK in bullfrog sympathetic neurons by Tokimasa (1984)
  75. 10.1016/0006-8993(85)91197-7 / Brain Res / Spontaneous muscarinic suppression of the Ca-activated K-current in bullfrog sympathetic neurons by Tokimasa (1985)
  76. 10.1016/0006-8993(84)90987-9 / Brain Res / Calcium entry through acetylcholine-channels can activate potassium conductance in bullfrog sympathetic neurons by Tokimasa (1984)
  77. {'key': '2023051712530761100_JEXBIO_124_1_259C77', 'first-page': '143', 'article-title': 'Hyperpolarization following activation of K+ channels by excitatory postsynaptic potentials', 'volume': '308', 'author': 'Tosaka', 'year': '1983', 'journal-title': 'Nature, Lond'} / Nature, Lond / Hyperpolarization following activation of K+ channels by excitatory postsynaptic potentials by Tosaka (1983)
  78. 10.1016/S0006-291X(85)80160-1 / Biochem. biophys. Res. Commun / Tumor promoter phorbol 12-myristate, 13-acetate inhibits phosphoinositide hydrolysis and cytosolic Ca2+ rise induced by the activation of muscarinic receptors in PC12 cells by Vicentini (1985)
  79. 10.1126/science.170.3959.755 / Science / Slow synaptic excitation in sympathetic ganglion cells: evidence for synaptic inactivation of potassium conductance by Weight (1970)
  80. 10.1016/0006-8993(77)90988-X / Brain Res / Synaptic innervation of sympathetic ganglion cells in the bullfrog by Weitsen (1977)
Dates
Type When
Created 4 years, 4 months ago (April 23, 2021, 7:19 p.m.)
Deposited 2 years, 3 months ago (May 17, 2023, 8:55 a.m.)
Indexed 1 year ago (Aug. 12, 2024, 7:18 a.m.)
Issued 39 years ago (Sept. 1, 1986)
Published 39 years ago (Sept. 1, 1986)
Published Online 39 years ago (Sept. 1, 1986)
Published Print 39 years ago (Sept. 1, 1986)
Funders 0

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@article{Adams_1986, title={Slow Synaptic Transmission in Frog Sympathetic Ganglia}, volume={124}, ISSN={1477-9145}, url={http://dx.doi.org/10.1242/jeb.124.1.259}, DOI={10.1242/jeb.124.1.259}, number={1}, journal={Journal of Experimental Biology}, publisher={The Company of Biologists}, author={Adams, P. R. and Jones, S. W. and Pennefather, P. and Brown, D. A. and Koch, C. and Lancaster, B.}, year={1986}, month=sep, pages={259–285} }