Electrical coupling between Aplysia bag cell neurons: characterization and role in synchronous firing

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.

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An Electrically Coupled Network of Skeletal Muscle in Zebrafish Distributes Synaptic Current

The Journal of General Physiology ◽

10.1085/jgp.200609501 ◽

2006 ◽

Vol 128 (1) ◽

pp. 89-102 ◽

Cited By ~ 19

Author(s):

Victor M. Luna ◽

Paul Brehm

Keyword(s):

Skeletal Muscle ◽

Patch Clamp ◽

Action Potentials ◽

Electrical Coupling ◽

Slow Muscle ◽

Synaptic Current ◽

Pass Filter ◽

Low Pass Filter ◽

Low Pass ◽

Muscle Types

Fast and slow skeletal muscle types are readily distinguished in larval zebrafish on the basis of differences in location and orientation. Additionally, both muscle types are compact, rendering them amenable to in vivo patch clamp study of synaptic function. Slow muscle mediates rhythmic swimming, but it does so purely through synaptic drive, as these cells are unable to generate action potentials. Our patch clamp recordings from muscle pairs of zebrafish reveal a network of electrical coupling in slow muscle that allows sharing of synaptic current within and between segmental boundaries of the tail. The synaptic current exhibits slow kinetics (τdecay ∼4 ms), which further facilitates passage through the low pass filter, a consequence of the electrically coupled network. In contrast to slow muscle, fast skeletal muscle generates action potentials to mediate the initial rapid component of the escape response. The combination of very weak electrical coupling and synaptic kinetics (τdecay <1 ms) too fast for the network low pass filter minimizes intercellular sharing of synaptic current in fast muscle. These differences between muscle types provide insights into the physiological role(s) of electrical coupling in skeletal muscle. First, intrasegmental coupling among slow muscle cells allows effective transfer of synaptic currents within tail segments, thereby minimizing differences in synaptic depolarization. Second, a fixed intersegmental delay in synaptic current transit, resulting from the low pass filter properties of the slow muscle network, helps coordinate the rostral–caudal wave of contraction.

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Ca2+-induced uncoupling of Aplysia bag cell neurons

Journal of Neurophysiology ◽

10.1152/jn.00603.2014 ◽

2015 ◽

Vol 113 (3) ◽

pp. 808-821 ◽

Cited By ~ 3

Author(s):

Zahra Dargaei ◽

Dominic Standage ◽

Christopher J. Groten ◽

Gunnar Blohm ◽

Neil S. Magoski

Keyword(s):

Time Course ◽

Electrical Coupling ◽

Egg Laying ◽

Neuroendocrine Cells ◽

Electrical Synapse ◽

Electrical Transmission ◽

Synchronous Firing ◽

Cell Recording ◽

Intracellular Ca ◽

Bag Cell Neurons

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.

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The Parameters and Properties of a Group of Electrically Coupled Neurones in the Central Nervous System of a Hydrozoan Jellyfish

Journal of Experimental Biology ◽

10.1242/jeb.93.1.33 ◽

1981 ◽

Vol 93 (1) ◽

pp. 33-50

Author(s):

A. N. Spencer

Keyword(s):

Action Potentials ◽

Electrical Coupling ◽

Membrane Resistance ◽

Initiation Site ◽

Pass Filter ◽

Low Pass Filter ◽

Polyorchis Penicillatus ◽

Low Pass ◽

Motor Neurones ◽

Spontaneous Action

1. Swimming of the jellyfish Polyorchis penicillatus is controlled by a network of large, electrically coupled, motor neurones in the inner nervering (Fig. 3). Recordings from pairs of neurones, even at widely separated positions, display essentially the same electrical activity (Fig. 1). 2. Electrical coupling between neurones is via gap-junctions and is very strong, giving the network a space constant of approximately 7.1 mm (Figs. 2, 4, 5). The network acts as a low-pass filter progressively attenuating signals with frequencies greater than 1 Hz (Figs. 4, 6). 3. I/V experiments demonstrate that the neurones show rectifying properties since membrane resistance decreases noticeably with depolarizations greater than about 25 mV (Figs. 7, 8). 4. A number of electrical constants of the network were measured or calculated: rm = 3.55 MΩ cm−1, Rm = 98 kΩ cm2, ri = 7 MΩ cm−1, Rinput = 2.5 MΩ, Cm = 1.52 μF cm−2. 5. Stimulated action potentials are conducted in the network at approximately 112 cm s−1 while spontaneous action potentials have velocities up to 200 cm s−1. As an action potential propagates from its initiation site its duration decreases from about 30 ms to 8 ms when it reaches the opposite side of the margin. 6. Epithelial impulses, which mediate crumpling, cause large i.p.s.p.s in the motor network that can inhibit swimming for several seconds.

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Persistent Electrical Coupling and Locomotory Dysfunction in the Zebrafish Mutant shocked

Journal of Neurophysiology ◽

10.1152/jn.00454.2004 ◽

2004 ◽

Vol 92 (4) ◽

pp. 2003-2009 ◽

Cited By ~ 12

Author(s):

Victor M. Luna ◽

Meng Wang ◽

Fumihito Ono ◽

Michelle R. Gleason ◽

Julia E. Dallman ◽

...

Keyword(s):

Neuromuscular Junctions ◽

Electrical Coupling ◽

Muscle Cells ◽

Wild Type ◽

Pass Filter ◽

Low Pass Filter ◽

Autonomous Function ◽

Low Pass ◽

Muscle Excitability ◽

Synaptic Responses

On initial formation of neuromuscular junctions, slow synaptic signals interact through an electrically coupled network of muscle cells. After the developmental onset of muscle excitability and the transition to fast synaptic responses, electrical coupling diminishes. No studies have revealed the functional importance of the electrical coupling or its precisely timed loss during development. In the mutant zebrafish shocked ( sho) electrical coupling between fast muscle cells persists beyond the time that it would normally disappear in wild-type fish. Recordings from sho indicate that muscle depolarization in response to motor neuron stimulation remains slow due to the low-pass filter characteristics of the coupled network of muscle cells. Our findings suggest that the resultant prolonged muscle depolarizations contribute to the premature termination of swimming in sho and the delayed acquisition of the normally rapid touch-triggered movements. Thus the benefits of gap junctions during early synapse development likely become a liability if not inactivated by the time that muscle would normally achieve fast autonomous function.

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