Potassium currents and their modulation by muscarine and substance P in neuronal cultures from adult guinea pig celiac ganglia

S. Vanner, R. J. Evans, Steven Matsumoto, A. Surprenant

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Abstract

1. Intracellular microelectrode and whole-cell patch-clamp recordings were obtained from adult guinea pig celiac ganglion neurons grown in tissue culture for 7-14 days. Over 90% of neurons showed phasic-type action- potential discharge with the use of either type of recording electrode; they stained immunohistochemically for catecholamines, tyrosine hydroxylase, and neuropeptide Y. Input resistance (140 MΩ) and action-potential amplitude (103 mV) were significantly greater with whole-cell than with microelectrode recordings, but other passive electrical properties were similar. 2. Five potassium currents were characterized: an apamin-sensitive afterhyperpolarizing current (I(AHP)), an apamin and tetraethylammonium- insensitive slow I(AHP), an M-like current, a transient outward I(A) current, and a delayed rectifier I(K) current. A hyperpolarization-activated cationic I(h) current was also present. The first three currents were not observed with whole-cell recordings. 3. Cadmium (200 μM), cobalt (1 mM), lanthanum (30 μM), or a low calcium/high magnesium solution blocked both I(AHP)s and the M-like current; barium (1 mM) also blocked these currents. 4. Kinetics of the M-like current were best described by a double exponential fit to deactivating tail currents with time constants of 50 and 390 ms at -50 mV. The apamin-sensitive and slow I(AHP) decayed exponentially with time constants of 145 ms and 3.5 s, respectively. There was no correlation between occurrence of M-like current (95% of neurons) and slow I(AHP) (40% of neurons), not any correlation between magnitude of M-like current and I(AHP) in those cells exhibiting both currents. 5. Muscarine and substance P (SP) caused depolarizations or inward currents (under voltage clamp) at the resting potential (-55 mV) associated with a decreased membrane conductance. The slow I(AHP) and the M-like current, but not the apamin-sensitive I(AHP) nor the I(A), were blocked by muscarine and SP (IC50 3 μM and 100 nM, respectively). Muscarine and SP also decreased a 'leak' potassium current. 6. We conclude that celiac neurons express two calcium-dependent I(AHP) currents and a calcium-dependent M-current; these are seen by the fine-tipped intracellular microelectrodes but not by whole-cell patch electrodes. These currents are not required for spike frequency accommodation. Muscarine and SP reduce these currents, as well as a voltage-independent leakage potassium current.

Original languageEnglish (US)
Pages (from-to)1632-1644
Number of pages13
JournalJournal of Neurophysiology
Volume69
Issue number5
StatePublished - 1993

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Muscarine
Sympathetic Ganglia
Apamin
Substance P
Potassium
Guinea Pigs
Neurons
Microelectrodes
Calcium
Action Potentials
Electrodes
Lanthanum
Tetraethylammonium
Neuropeptide Y
Tyrosine 3-Monooxygenase
Patch-Clamp Techniques
Barium
Cobalt
Cadmium
Abdomen

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Potassium currents and their modulation by muscarine and substance P in neuronal cultures from adult guinea pig celiac ganglia. / Vanner, S.; Evans, R. J.; Matsumoto, Steven; Surprenant, A.

In: Journal of Neurophysiology, Vol. 69, No. 5, 1993, p. 1632-1644.

Research output: Contribution to journalArticle

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abstract = "1. Intracellular microelectrode and whole-cell patch-clamp recordings were obtained from adult guinea pig celiac ganglion neurons grown in tissue culture for 7-14 days. Over 90{\%} of neurons showed phasic-type action- potential discharge with the use of either type of recording electrode; they stained immunohistochemically for catecholamines, tyrosine hydroxylase, and neuropeptide Y. Input resistance (140 MΩ) and action-potential amplitude (103 mV) were significantly greater with whole-cell than with microelectrode recordings, but other passive electrical properties were similar. 2. Five potassium currents were characterized: an apamin-sensitive afterhyperpolarizing current (I(AHP)), an apamin and tetraethylammonium- insensitive slow I(AHP), an M-like current, a transient outward I(A) current, and a delayed rectifier I(K) current. A hyperpolarization-activated cationic I(h) current was also present. The first three currents were not observed with whole-cell recordings. 3. Cadmium (200 μM), cobalt (1 mM), lanthanum (30 μM), or a low calcium/high magnesium solution blocked both I(AHP)s and the M-like current; barium (1 mM) also blocked these currents. 4. Kinetics of the M-like current were best described by a double exponential fit to deactivating tail currents with time constants of 50 and 390 ms at -50 mV. The apamin-sensitive and slow I(AHP) decayed exponentially with time constants of 145 ms and 3.5 s, respectively. There was no correlation between occurrence of M-like current (95{\%} of neurons) and slow I(AHP) (40{\%} of neurons), not any correlation between magnitude of M-like current and I(AHP) in those cells exhibiting both currents. 5. Muscarine and substance P (SP) caused depolarizations or inward currents (under voltage clamp) at the resting potential (-55 mV) associated with a decreased membrane conductance. The slow I(AHP) and the M-like current, but not the apamin-sensitive I(AHP) nor the I(A), were blocked by muscarine and SP (IC50 3 μM and 100 nM, respectively). Muscarine and SP also decreased a 'leak' potassium current. 6. We conclude that celiac neurons express two calcium-dependent I(AHP) currents and a calcium-dependent M-current; these are seen by the fine-tipped intracellular microelectrodes but not by whole-cell patch electrodes. These currents are not required for spike frequency accommodation. Muscarine and SP reduce these currents, as well as a voltage-independent leakage potassium current.",
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N2 - 1. Intracellular microelectrode and whole-cell patch-clamp recordings were obtained from adult guinea pig celiac ganglion neurons grown in tissue culture for 7-14 days. Over 90% of neurons showed phasic-type action- potential discharge with the use of either type of recording electrode; they stained immunohistochemically for catecholamines, tyrosine hydroxylase, and neuropeptide Y. Input resistance (140 MΩ) and action-potential amplitude (103 mV) were significantly greater with whole-cell than with microelectrode recordings, but other passive electrical properties were similar. 2. Five potassium currents were characterized: an apamin-sensitive afterhyperpolarizing current (I(AHP)), an apamin and tetraethylammonium- insensitive slow I(AHP), an M-like current, a transient outward I(A) current, and a delayed rectifier I(K) current. A hyperpolarization-activated cationic I(h) current was also present. The first three currents were not observed with whole-cell recordings. 3. Cadmium (200 μM), cobalt (1 mM), lanthanum (30 μM), or a low calcium/high magnesium solution blocked both I(AHP)s and the M-like current; barium (1 mM) also blocked these currents. 4. Kinetics of the M-like current were best described by a double exponential fit to deactivating tail currents with time constants of 50 and 390 ms at -50 mV. The apamin-sensitive and slow I(AHP) decayed exponentially with time constants of 145 ms and 3.5 s, respectively. There was no correlation between occurrence of M-like current (95% of neurons) and slow I(AHP) (40% of neurons), not any correlation between magnitude of M-like current and I(AHP) in those cells exhibiting both currents. 5. Muscarine and substance P (SP) caused depolarizations or inward currents (under voltage clamp) at the resting potential (-55 mV) associated with a decreased membrane conductance. The slow I(AHP) and the M-like current, but not the apamin-sensitive I(AHP) nor the I(A), were blocked by muscarine and SP (IC50 3 μM and 100 nM, respectively). Muscarine and SP also decreased a 'leak' potassium current. 6. We conclude that celiac neurons express two calcium-dependent I(AHP) currents and a calcium-dependent M-current; these are seen by the fine-tipped intracellular microelectrodes but not by whole-cell patch electrodes. These currents are not required for spike frequency accommodation. Muscarine and SP reduce these currents, as well as a voltage-independent leakage potassium current.

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