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The dynamic range of voltage-dependent gap junction signaling is maintained by I_h-induced membrane potential depolarization.

ABSTRACT: Like their chemical counterparts, electrical synapses show complex dynamics such as rectification and voltage dependence that interact with other electrical processes in neurons. The consequences arising from these interactions for the electrical behavior of the synapse, and the dynamics they create, remain largely unexplored. Using a voltage-dependent electrical synapse between a descending modulatory projection neuron (MCN1) and a motor neuron (LG) in the crustacean stomatogastric ganglion, we find that the influence of the hyperpolarization-activated inward current (I_h) is critical to the function of the electrical synapse. When we blocked I_h with CsCl, the apparent voltage dependence of the electrical synapse shifted by 18.7 mV to more hyperpolarized voltages, placing the dynamic range of the electrical synapse outside of the range of voltages used by the LG motor neuron (-60.2 mV to -44.9 mV). With dual electrode current- and voltage-clamp recordings, we demonstrate that this voltage shift is not due to a change in the properties of the gap junction itself, but is a result of a sustained effect of I_h on the presynaptic MCN1 axon terminal membrane potential. I_h-induced depolarization of the axon terminal membrane potential increased the electrical postsynaptic potentials and currents. With I_h present, the axon terminal resting membrane potential is depolarized, shifting the dynamic range of the electrical synapse toward the functional range of the motor neuron. We thus demonstrate that the function of an electrical synapse is critically influenced by a voltage-dependent ionic current (I_h).NEW & NOTEWORTHY Electrical synapses and voltage-gated ionic currents are often studied independently from one another, despite mounting evidence that their interactions can alter synaptic behavior. We show that the hyperpolarization-activated inward ionic current shifts the voltage dependence of electrical synaptic transmission through its depolarizing effect on the membrane potential, enabling it to lie within the functional membrane potential range of a motor neuron. Thus, the electrical synapse's function critically depends on the voltage-gated ionic current.

SUBMITTER: Stein W

PROVIDER: S-EPMC8917912 | biostudies-literature | 2022 Mar

REPOSITORIES: biostudies-literature

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The dynamic range of voltage-dependent gap junction signaling is maintained by <i>I</i><sub>h</sub>-induced membrane potential depolarization.

Stein Wolfgang W DeMaegd Margaret L ML Braun Lena Yolanda LY Vidal-Gadea Andrés G AG Harris Allison L AL Städele Carola C

Journal of neurophysiology 20220216 3

Like their chemical counterparts, electrical synapses show complex dynamics such as rectification and voltage dependence that interact with other electrical processes in neurons. The consequences arising from these interactions for the electrical behavior of the synapse, and the dynamics they create, remain largely unexplored. Using a voltage-dependent electrical synapse between a descending modulatory projection neuron (MCN1) and a motor neuron (LG) in the crustacean stomatogastric ganglion, we ...[more]

PMID: 35171723

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Project description:Gap junctions are composed of a family of structural proteins called connexins, which oligomerize into intercellular channels and function to exchange low molecular weight metabolites and ions between adjacent cells. We have cloned a new member of the connexin family from lens cDNA, with a predicted molecular mass of 46 kD, called rat connexin46 (Cx46). Since a full-length cDNA corresponding to the 2.8-kb mRNA was not obtained, the stop codon and surrounding sequences were confirmed from rat genomic DNA. The RNA coding for this protein is abundant in lens fibers and detectable in both myocardium and kidney. Western analysis of both rat and bovine lens membrane proteins, using the anti-MP70 monoclonal antibody 6-4-B2-C6 and three anti-peptide antibodies against Cx46 demonstrates that Cx46 and MP70 are different proteins. Immunocytochemistry demonstrates that both proteins are localized in the same lens fiber junctional maculae. Synthesis of Cx46 in either reticulocyte lysate or Xenopus oocytes yields a 46-kD polypeptide; all anti-Cx46 antisera recognize a protein in rat lens membranes 5-10 kD larger, suggesting substantive lenticular posttranslational processing of the native translation product. Oocytes that have synthesized Cx46 depolarize and lyse within 24 h, a phenomenon never observed after expression of rat connexins 32 or 43 (Cx32 and Cx43). Lysis is prevented by osmotically buffering the oocytes with 5% Ficoll. Ficoll-buffered oocytes expressing Cx46 are permeable to Lucifer Yellow but not FITC-labeled BSA, indicating the presence of selective membrane permeabilities. Cx43-expressing oocytes are impermeable to Lucifer Yellow. Voltage-gated whole cell currents are measured in oocytes injected with dilute concentrations of Cx46 but not Cx43 mRNA. These currents are activated at potentials positive to -10 mV. Unlike other connexins expressed in Xenopus oocytes, these results suggest that unprocessed Cx46 induces nonselective channels in the oolemma that are voltage dependent and opened by large depolarizations.

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The dynamic range of voltage-dependent gap junction signaling is maintained by I_h-induced membrane potential depolarization.

Publications

The dynamic range of voltage-dependent gap junction signaling is maintained by <i>I</i><sub>h</sub>-induced membrane potential depolarization.

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The dynamic range of voltage-dependent gap junction signaling is maintained by Ih-induced membrane potential depolarization.

Publications

The dynamic range of voltage-dependent gap junction signaling is maintained by <i>I</i><sub>h</sub>-induced membrane potential depolarization.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets

The dynamic range of voltage-dependent gap junction signaling is maintained by I_h-induced membrane potential depolarization.