Ca²⁺-induced uncoupling ofAplysiabag cell neurons

Abstract

Electrical transmission is a dynamically regulated form of communication and key to synchronizing neuronal activity. The bag cell neurons of Aplysia are a group of electrically coupled neuroendocrine cells that initiate ovulation by secreting egg-laying hormone during a prolonged period of synchronous firing called the afterdischarge. Accompanying the afterdischarge is an increase in intracellular Ca2+ and the activation of protein kinase C (PKC). We used whole cell recording from paired cultured bag cell neurons to demonstrate that electrical coupling is regulated by both Ca2+ and PKC. Elevating Ca2+ with a train of voltage steps, mimicking the onset of the afterdischarge, decreased junctional current for up to 30 min. Inhibition was most effective when Ca2+ entry occurred in both neurons. Depletion of Ca2+ from the mitochondria, but not the endoplasmic reticulum, also attenuated the electrical synapse. Buffering Ca2+ with high intracellular EGTA or inhibiting calmodulin kinase prevented uncoupling. Furthermore, activating PKC produced a small but clear decrease in junctional current, while triggering both Ca2+ influx and PKC inhibited the electrical synapse to a greater extent than Ca2+ alone. Finally, the amplitude and time course of the postsynaptic electrotonic response were attenuated after Ca2+ influx. A mathematical model of electrically connected neurons showed that excessive coupling reduced recruitment of the cells to fire, whereas less coupling led to spiking of essentially all neurons. Thus a decrease in electrical synapses could promote the afterdischarge by ensuring prompt recovery of electrotonic potentials or making the neurons more responsive to current spreading through the network.

Diacylglycerol‐mediated regulation of Aplysia bag cell neuron excitability requires protein kinase C

“…; Dargaei et al . , ). Acetylcholine chloride (Sigma‐Aldrich), d ‐ myo ‐inositol 1,4,5‐trisphosphate trisodium salt (IP 3 ; Sigma‐Aldrich), gadolinium(III) chloride hexahydrate (Gd 3+ ; Sigma‐Aldrich), and H‐7 dihydrochloride (H7; Tocris) were dissolved in H 2 O.…”

Hydrogen peroxide and phosphoinositide metabolites synergistically regulate a cation current to influence neuroendocrine cell bursting

“…Because electrical coupling within the cluster is extensive and spiking is synchronous (Dargaei et al. 2014, 2015), one neuron can report the activity of the entire cluster. The initial resting membrane potential of the neurons before acetylcholine was not significantly different between groups (Fig.…”