Electrotonic coupling among neuroendocrine cells in Aplysia

Abstract

1. We have discovered and characterized direct electrotonic synaptic coupling among a population of neuroendocrine (bag) cells in the parietovisceral ganglion of the marine gastropod Aplysia dactylomela. Pairs of ipsilateral and contralateral bag cells were impaled in vitro with microelectrodes. Current pulses applied through the electrometer amplifier to either cell influenced the other cell via electrotonic connections. 2. The coupling between bag cells was relatively weak when measured at the somata; the mean ratio of postsynaptic/presynaptic response amplitudes is 0.0075. Junctional rectification was not detected. The latency between pre- and postjunctional responses was long, up to 50 ms, a delay comparable to that for chemical synaptic transmission among neurons in this ganglion. Low-Ca2+/high-Mg2+ bathing solutions did not block transmission between bag cells, but did block chemical synaptic potentials in other identified neurons. 3. Postjunctional electrotonic responses had markedly slow time courses compared to the prejunctional responses, a characteristic that permitted summation of otherwise undetectable electrotonic PSPs and the demonstration of coupling between the two (bilateral) clusters of bag cells. 4. Based on extracellular recordings of their compound action potentials, the neurites of A. dactylomela bag cells extended a shorter distance (approximately 3 mm) along the connective than the neurites of A. californica or A. brasiliana. 5. Electrolytic lesions made along the neurites during intrasomatic coupling measurements significantly shortened the duration of postjuctional electrotonic responses, indicating that the neurites are widely electrically interconnected and, as a population, have a large effective membrane capacitance. The lesions furthermore revealed that an important site of electrotonic coupling is at the base of the pleurovisceral connective just rostral to the bag cell cluster. 6. The small-amplitude, long-latency and prolonged time course of postjunctional responses are interpreted to indicate remote and widespread coupling sites among the bag cells. This electrotonic coupling underlies the synchronized firing of the bag cells.