Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell

Alberto E. Pereda, T. D. Bell, D. S. Faber

Research output: Contribution to journalArticle

56 Citations (Scopus)

Abstract

Large myelinated club endings of the goldfish eighth nerve arise in the sacculus and establish mixed electrotonic and chemical synapses with the distal part of the Mauthner (M-) cell's lateral dendrite. We show here, using paired pre- and postsynaptic recordings, that depolarizing currents generated postsynaptically (specifically, the mixed synaptic potential produced by activation of part of the afferent population) can in some cases excite the presynaptic fibers and cause them to backfire. Strikingly, while in some systems functional properties prevent the antidromic spread of depolarizing currents, physiological properties of these afferents and the gap junctions promote backfiring: the amplitude of the coupling potential recorded from an afferent fiber is voltage dependent, increasing with depolarization and being reduced during hyperpolarization. Two mechanisms, with different kinetics, underlie this voltage dependence. One, a nonlinear membrane property of the afferent fiber itself, enhances the coupling potential as the afferent membrane depolarizes. The second mechanism, which is less sensitive to voltage and is symmetric about the resting potential, most likely represents voltage dependence of the junctional membrane. Additionally, we also show retrograde diffusion of low molecular weight substances, as the fluorescent dye Lucifer yellow and the tracer Neurobiotin were found in the terminals of afferent fibers after being injected postsynaptically into the M-cell. These results suggest that the gap junctions in these primary afferents are not only involved in fast anterograde synaptic transmission but also provide the substrate for a retrograde intercellular communication. The electrical coupling may modify the input-output relation between eighth nerve afferents and the lateral dendrite by synchronizing the population of already active fibers and by promoting the recruitment of new fibers via backfiring, such that weaker inputs produce relatively larger responses.

Original languageEnglish (US)
Pages (from-to)5943-5955
Number of pages13
JournalJournal of Neuroscience
Volume15
Issue number9
StatePublished - 1995
Externally publishedYes

Fingerprint

Gap Junctions
Communication
Dendrites
Membranes
Electrical Synapses
Synaptic Potentials
Goldfish
Fluorescent Dyes
Synaptic Transmission
Membrane Potentials
Population
Molecular Weight

Keywords

  • dye coupling
  • electrical synapses
  • gap junctions
  • Mauthner cell
  • retrograde communication
  • synaptic plasticity

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell. / Pereda, Alberto E.; Bell, T. D.; Faber, D. S.

In: Journal of Neuroscience, Vol. 15, No. 9, 1995, p. 5943-5955.

Research output: Contribution to journalArticle

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