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The Journal of Neuroscience, April 21, 2004, 24(16):3999-4010; doi:10.1523/JNEUROSCI.0077-04.2004

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Cellular/Molecular
Voltage-Dependent Enhancement of Electrical Coupling by a Subthreshold Sodium Current

Sebastián Curti and Alberto E. Pereda

Department of Neuroscience, Albert Einstein College of Medicine, Yeshiva University, Bronx, New York 10461

Voltage-dependent changes in electrical coupling are often attributed to a direct effect on the properties of gap junction channels. Identifiable auditory afferents terminate as mixed (electrical and chemical) synapses on the distal portion of the lateral dendrite of the goldfish Mauthner cells, a pair of large reticulospinal neurons involved in the organization of sensory-evoked escape responses. At these afferents, the amplitude of the coupling potential produced by the retrograde spread of signals from the postsynaptic Mauthner cell is dramatically enhanced by depolarization of the presynaptic terminal. We demonstrate here that this voltage-dependent enhancement of electrical coupling does not represent a property of the junctions themselves but the activation of a subthreshold sodium current present at presynaptic terminals that acts to amplify the synaptic response. We also provide evidence that this amplification operates under physiological conditions, enhancing synaptic communication from the Mauthner cells to the auditory afferents where electrical and geometrical properties of the coupled cells are unfavorable for retrograde transmission. Retrograde electrical communication at these afferents may play an important functional role by promoting cooperativity between afferents and enhancing transmitter release. Thus, the efficacy of an electrical synapse can be dynamically modulated in a voltage-dependent manner by properties of the nonjunctional membrane. Finally, asymmetric amplification of electrical coupling by intrinsic membrane properties, as at the synapses between auditory afferents and the Mauthner cell, may ensure efficient communication between neuronal processes of dissimilar size and shape, promoting neuronal synchronization.

Key words: gap junctions; persistent sodium current; Mauthner; electrical synapse; synchronization; auditory; synaptic plasticity

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Received Nov 13, 2003; revised March 9, 2004; accepted March 9, 2004.

This article has been cited by other articles:

				S. Curti, L. Gomez, R. Budelli, and A. E. Pereda Subthreshold Sodium Current Underlies Essential Functional Specializations at Primary Auditory Afferents J Neurophysiol, April 1, 2008; 99(4): 1683 - 1699. [Abstract] [Full Text] [PDF]

				T. M. Szabo, S. A. Weiss, D. S. Faber, and T. Preuss Representation of Auditory Signals in the M-Cell: Role of Electrical Synapses J Neurophysiol, April 1, 2006; 95(4): 2617 - 2629. [Abstract] [Full Text] [PDF]

				B. L. Antonsen, J. Herberholz, and D. H. Edwards The Retrograde Spread of Synaptic Potentials and Recruitment of Presynaptic Inputs J. Neurosci., March 23, 2005; 25(12): 3086 - 3094. [Abstract] [Full Text] [PDF]

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