PT  - JOURNAL ARTICLE
AU  - Christopher C. Beekharry
AU  - Yueling Gu
AU  - Neil S. Magoski
TI  - Protein kinase C enhances electrical synaptic transmission by acting on junctional and postsynaptic Ca<sup>2+</sup> currents
AID  - 10.1523/JNEUROSCI.2619-17.2018
DP  - 2018 Feb 13
TA  - The Journal of Neuroscience
PG  - 2619-17
4099  - http://www.jneurosci.org/content/early/2018/02/13/JNEUROSCI.2619-17.2018.short
4100  - http://www.jneurosci.org/content/early/2018/02/13/JNEUROSCI.2619-17.2018.full
AB  - By synchronizing neuronal activity electrical transmission influences the coordination, pattern, and/or frequency of firing. In the hemaphroditic marine-snail, Aplysia calfornica, the neuroendocrine bag cell neurons use electrical synapses to synchronize a 30-min afterdischarge of action potentials for the release of reproductive hormone. During the afterdischarge, protein kinase C (PKC) is activated, although its impact on bag cell neuron electrical transmission is unknown. This was investigated here by monitoring electrical synapses between paired cultured bag cell neurons using dual whole-cell recording. Voltage-clamp revealed a largely voltage-independent junctional current, which was enhanced by treating with a PKC activator, phorbol-12-myristate-13-acetate (PMA), prior to recording. We also examined the transfer of presynaptic action potential-like waveforms (generated in voltage-clamp) to the postsynaptic cell (measured in current-clamp). For control pairs, the presynaptic spike-like waveforms mainly evoked electrotonic potentials (ETPs); however, when PKC was triggered these stimuli consistently produced postsynaptic action potentials. To assess whether this involved changes to postsynaptic responsiveness, single bag cell neurons were injected with junctional-like current mimicking that evoked by a presynaptic action potential. Unlike control neurons, which were less likely to spike, cells in PMA always fired action potentials to the junctional-like current. Furthermore, PKC activation increased a postsynaptic voltage-gated Ca2+ current, which was recruited even by modest depolarization associated with an ETP. While PKC inhibits gap junctions in most systems, bag cell neurons are rather unique, as the kinase potentiates the electrical synapse; in turn, this synergizes with augmented postsynaptic Ca2+ current to promote synchronous firing.SIGNIFICANCE STATEMENTElectrical coupling is a fundamental form of communication. For the bag cell neurons of Aplysia, electrical synapses coordinate a prolonged burst of action potentials known as the afterdischarge. We looked at how protein kinase C, which is upregulated with the afterdischarge, influences information transfer across the synapse. The kinase activation increased junctional current, a remarkable finding given that this enzyme is largely considered inhibitory for gap junctions. There was also an augmentation in the ability of a presynaptic neuron to provoke postsynaptic action potentials. This increased excitability was, in part, due to enhanced postsynaptic voltage-dependent Ca2+ current. Thus, protein kinase C improves the fidelity of electrotonic transmission and promotes synchronous firing by modulating both junctional and membrane conductances.