Electrical coupling betweenAplysiabag cell neurons: characterization and role in synchronous firing

Abstract

In neuroendocrine cells, hormone release often requires a collective burst of action potentials synchronized by gap junctions. This is the case for the electrically coupled bag cell neurons in the reproductive system of the marine snail, Aplysia californica. These neuroendocrine cells are found in two clusters, and fire a synchronous burst, called the afterdischarge, resulting in neuropeptide secretion and the triggering of ovulation. However, the physiology and pharmacology of the bag cell neuron electrical synapse are not completely understood. As such, we made dual whole cell recordings from pairs of electrically coupled cultured bag cell neurons. The junctional current was nonrectifying and not influenced by postsynaptic voltage. Furthermore, junctional conductance was voltage independent and, not surprisingly, strongly correlated with coupling coefficient magnitude. The electrical synapse also acted as a low-pass filter, although under certain conditions, electrotonic potentials evoked by presynaptic action potentials could drive postsynaptic spikes. If coupled neurons were stimulated to spike simultaneously, they presented a high degree of action potential synchrony compared with not-coupled neurons. The electrical synapse failed to pass various intracellular dyes, but was permeable to Cs(+), and could be inhibited by niflumic acid, meclofenamic acid, or 5-nitro-2-(3-phenylpropylamino)benzoic acid. Finally, extracellular and sharp-electrode recording from the intact bag cell neuron cluster showed that these pharmacological uncouplers disrupted both electrical coupling and afterdischarge generation in situ. Thus electrical synapses promote bag cell neuron firing synchrony and may allow for electrotonic spread of the burst through the network, ultimately contributing to propagation of the species.

Hydrogen Peroxide Gates a Voltage-Dependent Cation Current inAplysiaNeuroendocrine Cells

“…ACh may facilitate H 2 O 2 -dependent opening of the voltage-dependent cation channel, either through direct depolarization or initiating an as yet unidentified intracellular pathway. Work by our laboratory and others indicates that if one bag cell neuron is bursting within the cluster, all other neurons also spike synchronously (Kupfermann and Kandel, 1970;Brown and Mayeri, 1989;Dargaei et al, 2014). Thus, it is reasonable to assume that the H 2 O 2 -induced afterdischarge-like response represents en masse firing of the cluster.…”

“…Because bath-applying H 2 O 2 alone causes a burst in a minority of clusters, we speculate H 2 O 2 may need to work in concert with ACh, a known input transmitter that gates an ionotropic receptor on bag cell neurons (White and Magoski, 2012;White et al, 2014). Pressure-ejecting ACh onto one side of the cluster depolarizes a neuron recorded on the opposite side; this is because of the transfer of cholinergic current through electrotonic coupling between neurons within the cluster (Kupfermann and Kandel, 1970;Dargaei et al, 2014;White et al, 2018). When H 2 O 2 is bath-applied subsequent to the ACh pressure-ejection, it consistently provokes an afterdischarge-like burst.…”

Clustered organization and region‐specific identities of estrogen‐producing neurons in the forebrain of Zebra Finches (Taeniopygia guttata)

“…More broadly, electrical coupling is a feature of neuroendocrine secretion patterns in many species. Neuronal synchronization is dependent on functional gap junctions for the pulsatile release of GnRH in the hypothalamus (Pinet‐Charvet et al, ), for reproductive neurohormone release in aplysia (Dargaei, Colmers, Hodgson, & Magoski, ), and for coordinated neurosecretion in the supraoptic nucleus (Yang & Hatton, ) and suprachiasmatic nucleus (Colwell, ; Long, Jutras, Connors, & Burwell, ).…”

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.…”