Electrotonic synapses between Aplysia neurons in situ and in culture: Aspects of regulation and measurements of permeability

R. Bodmer, Vytautas Verselis, I. B. Levitan, David C. Spray

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Abstract

Properties of electrotonic synapses between L14 neurons in the abdominal ganglion of the marine mollusc Aplysia californica were examined in situ and between unidentified buccal neurons maintained in tissue culture. In culture, depolarizing postsynaptic potentials in response to a train of action potentials showed apparent facilitation with increasing spike number, which was attributable to the low-pass filter properties of electrotonic transmission via gap junctions and to network properties. Gap junctional conductance (g(j)), calculated from current-clamp data or measured directly under voltage clamp, indicated no significant dependence of g(j) on transjunctional or inside-outside potential in situ or in culture. Octanol, a local anesthetic agent that reduces g(j) in many other systems, had no effect on g(j) between Aplysia neurons. The effect of intracellular acidification, a treatment that rapidly and reversibly uncouples a variety of cell types, reduced g(j) between Aplysia neurons but did not completely abolish it. The relationship between intracellular pH (pH(i)), measured with ion-sensitive microelectrodes, and g(j) was steeper in cultured neurons than in situ was and maximally reduced by 70-80%, as compared to 50% or less in situ at the lowest pH(i) values tested. The coupling coefficient (k) was reduced less by low pH(i) than was g(j), which could be explained by a simultaneous increase in nonjunctional membrane resistance. Permeability properties of Aplysia electrotonic synapses to a variety of tracer molecules were also examined between identified L14 neurons in situ and in dissociated buccal, abdominal, and bag neurons in culture. The fluorescent dyes Lucifer yellow, 6-carboxyfluorescein, and dichlorofluorescein (1.2-1.4 nm maximal diameters) did not spread detectably from an injected neuron to its electrically coupled neighbors, regardless of the strength of electrotonic coupling. However, the smaller tetraalkylammonium ions TMA and TEA (diameters 0.66 and 0.8 nm, concentrations measured with ion-selective electrodes), could be detected in neighboring cells within minutes. In culture, transfer of the tetraalkylammonium ions was slow and not easily detectable in cell pairs where g(j) was low (< 20 nS). The permeability was as high as 10-10 cm3/sec in situ and 10-12 cm3/sec in culture, and values were roughly correlated with simultaneously measured values of g(j). Electrotonic synapses in the nervous system of Aplysia, therefore, have a quantitatively different spectrum of sensitivities than has been found for gap junctions of other systems and appear to possess reduced permeability to tracer molecules.

Original languageEnglish (US)
Pages (from-to)1656-1670
Number of pages15
JournalJournal of Neuroscience
Volume8
Issue number5
StatePublished - 1988

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Electrical Synapses
Aplysia
Permeability
Neurons
Cheek
Gap Junctions
Ions
Ion-Selective Electrodes
Octanols
Synaptic Potentials
Mollusca
Microelectrodes
Local Anesthetics
Fluorescent Dyes
Ganglia
Nervous System
Action Potentials
Anesthetics

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

@article{d650583bdd4c46ca99a5151e02b4e7a2,
title = "Electrotonic synapses between Aplysia neurons in situ and in culture: Aspects of regulation and measurements of permeability",
abstract = "Properties of electrotonic synapses between L14 neurons in the abdominal ganglion of the marine mollusc Aplysia californica were examined in situ and between unidentified buccal neurons maintained in tissue culture. In culture, depolarizing postsynaptic potentials in response to a train of action potentials showed apparent facilitation with increasing spike number, which was attributable to the low-pass filter properties of electrotonic transmission via gap junctions and to network properties. Gap junctional conductance (g(j)), calculated from current-clamp data or measured directly under voltage clamp, indicated no significant dependence of g(j) on transjunctional or inside-outside potential in situ or in culture. Octanol, a local anesthetic agent that reduces g(j) in many other systems, had no effect on g(j) between Aplysia neurons. The effect of intracellular acidification, a treatment that rapidly and reversibly uncouples a variety of cell types, reduced g(j) between Aplysia neurons but did not completely abolish it. The relationship between intracellular pH (pH(i)), measured with ion-sensitive microelectrodes, and g(j) was steeper in cultured neurons than in situ was and maximally reduced by 70-80{\%}, as compared to 50{\%} or less in situ at the lowest pH(i) values tested. The coupling coefficient (k) was reduced less by low pH(i) than was g(j), which could be explained by a simultaneous increase in nonjunctional membrane resistance. Permeability properties of Aplysia electrotonic synapses to a variety of tracer molecules were also examined between identified L14 neurons in situ and in dissociated buccal, abdominal, and bag neurons in culture. The fluorescent dyes Lucifer yellow, 6-carboxyfluorescein, and dichlorofluorescein (1.2-1.4 nm maximal diameters) did not spread detectably from an injected neuron to its electrically coupled neighbors, regardless of the strength of electrotonic coupling. However, the smaller tetraalkylammonium ions TMA and TEA (diameters 0.66 and 0.8 nm, concentrations measured with ion-selective electrodes), could be detected in neighboring cells within minutes. In culture, transfer of the tetraalkylammonium ions was slow and not easily detectable in cell pairs where g(j) was low (< 20 nS). The permeability was as high as 10-10 cm3/sec in situ and 10-12 cm3/sec in culture, and values were roughly correlated with simultaneously measured values of g(j). Electrotonic synapses in the nervous system of Aplysia, therefore, have a quantitatively different spectrum of sensitivities than has been found for gap junctions of other systems and appear to possess reduced permeability to tracer molecules.",
author = "R. Bodmer and Vytautas Verselis and Levitan, {I. B.} and Spray, {David C.}",
year = "1988",
language = "English (US)",
volume = "8",
pages = "1656--1670",
journal = "Journal of Neuroscience",
issn = "0270-6474",
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TY - JOUR

T1 - Electrotonic synapses between Aplysia neurons in situ and in culture

T2 - Aspects of regulation and measurements of permeability

AU - Bodmer, R.

AU - Verselis, Vytautas

AU - Levitan, I. B.

AU - Spray, David C.

PY - 1988

Y1 - 1988

N2 - Properties of electrotonic synapses between L14 neurons in the abdominal ganglion of the marine mollusc Aplysia californica were examined in situ and between unidentified buccal neurons maintained in tissue culture. In culture, depolarizing postsynaptic potentials in response to a train of action potentials showed apparent facilitation with increasing spike number, which was attributable to the low-pass filter properties of electrotonic transmission via gap junctions and to network properties. Gap junctional conductance (g(j)), calculated from current-clamp data or measured directly under voltage clamp, indicated no significant dependence of g(j) on transjunctional or inside-outside potential in situ or in culture. Octanol, a local anesthetic agent that reduces g(j) in many other systems, had no effect on g(j) between Aplysia neurons. The effect of intracellular acidification, a treatment that rapidly and reversibly uncouples a variety of cell types, reduced g(j) between Aplysia neurons but did not completely abolish it. The relationship between intracellular pH (pH(i)), measured with ion-sensitive microelectrodes, and g(j) was steeper in cultured neurons than in situ was and maximally reduced by 70-80%, as compared to 50% or less in situ at the lowest pH(i) values tested. The coupling coefficient (k) was reduced less by low pH(i) than was g(j), which could be explained by a simultaneous increase in nonjunctional membrane resistance. Permeability properties of Aplysia electrotonic synapses to a variety of tracer molecules were also examined between identified L14 neurons in situ and in dissociated buccal, abdominal, and bag neurons in culture. The fluorescent dyes Lucifer yellow, 6-carboxyfluorescein, and dichlorofluorescein (1.2-1.4 nm maximal diameters) did not spread detectably from an injected neuron to its electrically coupled neighbors, regardless of the strength of electrotonic coupling. However, the smaller tetraalkylammonium ions TMA and TEA (diameters 0.66 and 0.8 nm, concentrations measured with ion-selective electrodes), could be detected in neighboring cells within minutes. In culture, transfer of the tetraalkylammonium ions was slow and not easily detectable in cell pairs where g(j) was low (< 20 nS). The permeability was as high as 10-10 cm3/sec in situ and 10-12 cm3/sec in culture, and values were roughly correlated with simultaneously measured values of g(j). Electrotonic synapses in the nervous system of Aplysia, therefore, have a quantitatively different spectrum of sensitivities than has been found for gap junctions of other systems and appear to possess reduced permeability to tracer molecules.

AB - Properties of electrotonic synapses between L14 neurons in the abdominal ganglion of the marine mollusc Aplysia californica were examined in situ and between unidentified buccal neurons maintained in tissue culture. In culture, depolarizing postsynaptic potentials in response to a train of action potentials showed apparent facilitation with increasing spike number, which was attributable to the low-pass filter properties of electrotonic transmission via gap junctions and to network properties. Gap junctional conductance (g(j)), calculated from current-clamp data or measured directly under voltage clamp, indicated no significant dependence of g(j) on transjunctional or inside-outside potential in situ or in culture. Octanol, a local anesthetic agent that reduces g(j) in many other systems, had no effect on g(j) between Aplysia neurons. The effect of intracellular acidification, a treatment that rapidly and reversibly uncouples a variety of cell types, reduced g(j) between Aplysia neurons but did not completely abolish it. The relationship between intracellular pH (pH(i)), measured with ion-sensitive microelectrodes, and g(j) was steeper in cultured neurons than in situ was and maximally reduced by 70-80%, as compared to 50% or less in situ at the lowest pH(i) values tested. The coupling coefficient (k) was reduced less by low pH(i) than was g(j), which could be explained by a simultaneous increase in nonjunctional membrane resistance. Permeability properties of Aplysia electrotonic synapses to a variety of tracer molecules were also examined between identified L14 neurons in situ and in dissociated buccal, abdominal, and bag neurons in culture. The fluorescent dyes Lucifer yellow, 6-carboxyfluorescein, and dichlorofluorescein (1.2-1.4 nm maximal diameters) did not spread detectably from an injected neuron to its electrically coupled neighbors, regardless of the strength of electrotonic coupling. However, the smaller tetraalkylammonium ions TMA and TEA (diameters 0.66 and 0.8 nm, concentrations measured with ion-selective electrodes), could be detected in neighboring cells within minutes. In culture, transfer of the tetraalkylammonium ions was slow and not easily detectable in cell pairs where g(j) was low (< 20 nS). The permeability was as high as 10-10 cm3/sec in situ and 10-12 cm3/sec in culture, and values were roughly correlated with simultaneously measured values of g(j). Electrotonic synapses in the nervous system of Aplysia, therefore, have a quantitatively different spectrum of sensitivities than has been found for gap junctions of other systems and appear to possess reduced permeability to tracer molecules.

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