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Chemical synaptic activity modulates nearby electrical synapses.

ABSTRACT: Most electrically coupled neurons also receive numerous chemical synaptic inputs. Whereas chemical synapses are known to be highly dynamic, gap junction-mediated electrical transmission often is considered to be less modifiable and variable. By using simultaneous pre- and postsynaptic recordings, we demonstrate at single mixed electrical and chemical synapses that fast chemical transmission interacts with gap junctions within the same ending to regulate their conductance. Such localized interaction is activity-dependent and could account for the large variation in strength of electrical coupling at auditory afferent synapses terminating on the Mauthner cell lateral dendrite. Thus, interactions between chemical and electrical synapses can regulate the degree of electrical coupling, making it possible for a given neuron to independently modify coupling at different electrical synapses with its neighbors.

SUBMITTER: Smith M

PROVIDER: S-EPMC153644 | biostudies-literature | 2003 Apr

REPOSITORIES: biostudies-literature

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Chemical synaptic activity modulates nearby electrical synapses.

Smith Mackenzie M Pereda Alberto E AE

Proceedings of the National Academy of Sciences of the United States of America 20030331 8

Most electrically coupled neurons also receive numerous chemical synaptic inputs. Whereas chemical synapses are known to be highly dynamic, gap junction-mediated electrical transmission often is considered to be less modifiable and variable. By using simultaneous pre- and postsynaptic recordings, we demonstrate at single mixed electrical and chemical synapses that fast chemical transmission interacts with gap junctions within the same ending to regulate their conductance. Such localized interact ...[more]

PMID: 12668761

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Project description:BackgroundA large number of invertebrate models, including the snail Helix, emerged as particularly suitable tools for investigating the formation of synapses and the specificity of neuronal connectivity. Helix neurons can be individually identified and isolated in cell culture, showing well-conserved size, position, biophysical properties, synaptic connections, and physiological functions. Although we previously showed the potential usefulness of Helix polysynaptic circuits, a full characterization of synaptic connectivity and its dynamics during network development has not been performed.ResultsIn this paper, we systematically investigated the in vitro formation of polysynaptic circuits, among Helix B2 and the serotonergic C1 neurons, from a morphological and functional point of view. Since these cells are generally silent in culture, networks were chemically stimulated with either high extracellular potassium concentrations or, alternatively, serotonin. Potassium induced a transient depolarization of all neurons. On the other hand, we found prolonged firing activity, selectively maintained following the first serotonin application. Statistical analysis revealed no significant changes in neuronal dynamics during network development. Moreover, we demonstrated that the cell-selective effect of serotonin was also responsible for short-lasting alterations in C1 excitability, without long-term rebounds.Estimation of the functional connections by means of cross-correlation analysis revealed that networks under elevated KCl concentrations exhibited strongly correlated signals with short latencies (about 5 ms), typical of electrically coupled cells. Conversely, neurons treated with serotonin were weakly connected with longer latencies (exceeding 20 ms) between the interacting neurons. Finally, we clearly demonstrated that these two types of correlations (in terms of strength/latency) were effectively related to the presence of electrical or chemical connections, by comparing Micro-Electrode Array (MEA) signal traces with intracellularly recorded cell pairs.ConclusionsNetworks treated with either potassium or serotonin were predominantly interconnected through electrical or chemical connections, respectively. Furthermore, B2 response and short-term increase in C1 excitability induced by serotonin is sufficient to trigger spontaneous activity with chemical connections, an important requisite for long-term maintenance of firing activity.

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Chemical synaptic activity modulates nearby electrical synapses.

Publications

Chemical synaptic activity modulates nearby electrical synapses.

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