Ca2+-induced uncoupling of Aplysia bag cell neurons

• Published in: Journal of neurophysiology Vol. 113; no. 3; pp. 808 - 821
• Main Authors: Dargaei, Zahra, Standage, Dominic, Groten, Christopher J, Blohm, Gunnar, Magoski, Neil S
• Format: Journal Article
• Language: English
• Published: United States 01.02.2015
• Subjects: Action Potentials; Animals; Aplysia; Calcium - metabolism; Calcium Signaling; Calcium-Calmodulin-Dependent Protein Kinase Type 2 - antagonists & inhibitors; Electrical Synapses - metabolism; Electrical Synapses - physiology; Endoplasmic Reticulum - metabolism; Mitochondria - metabolism; Models, Neurological; Neurons - drug effects; Neurons - metabolism; Neurons - physiology; Protein Kinase C - antagonists & inhibitors; Synaptic Transmission; electrical coupling; calcium; neuroendocrine cell; junctional current; protein kinase C
• ISSN: 1522-1598
• DOI: 10.1152/jn.00603.2014

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.