Specialized postsynaptic morphology enhances neurotransmitter dilution and high-frequency signaling at an auditory synapse

Cole W. Graydon, Soyoun Cho, Jeffrey S. Diamond, Bechara Kachar, Henrique von Gersdorff, William N. Grimes

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Sensory processing in the auditory system requires that synapses, neurons, and circuits encode information with particularly high temporal and spectral precision. In the amphibian papillia, sound frequencies up to 1 kHz are encoded along a tonotopic array of hair cells and transmitted to afferent fibers via fast, repetitive synaptic transmission, thereby promoting phase locking between the presynaptic and postsynaptic cells. Here, we have combined serial section electron microscopy, paired electrophysiological recordings, and Monte Carlo diffusion simulations to examine novel mechanisms that facilitate fast synaptic transmission in the inner ear of frogs (Rana catesbeiana and Rana pipiens). Three-dimensional anatomical reconstructions reveal specialized spine-like contacts between individual afferent fibers and hair cells that are surrounded by large, open regions of extracellular space. Morphologically realistic diffusion simulations suggest that these local enlargements in extracellular space speed transmitter clearance and reduce spillover between neighboring synapses, thereby minimizing postsynaptic receptor desensitization and improving sensitivity during prolonged signal transmission. Additionally, evoked EPSCs in afferent fibers are unaffected by glutamate transporter blockade, suggesting that transmitter diffusion and dilution, and not uptake, play a primary role in speeding neurotransmission and ensuring fidelity at these synapses.

Original languageEnglish (US)
Pages (from-to)8358-8372
Number of pages15
JournalJournal of Neuroscience
Volume34
Issue number24
DOIs
StatePublished - Jan 1 2014

Fingerprint

Synaptic Transmission
Synapses
Neurotransmitter Agents
Extracellular Space
Rana pipiens
Amino Acid Transport System X-AG
Rana catesbeiana
Amphibians
Inner Ear
Anura
Electron Microscopy
Spine
Neurons

Keywords

  • Auditory
  • Diffusion
  • Glutamate
  • Hair cell
  • Ribbon synapse
  • Synapse

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Specialized postsynaptic morphology enhances neurotransmitter dilution and high-frequency signaling at an auditory synapse. / Graydon, Cole W.; Cho, Soyoun; Diamond, Jeffrey S.; Kachar, Bechara; von Gersdorff, Henrique; Grimes, William N.

In: Journal of Neuroscience, Vol. 34, No. 24, 01.01.2014, p. 8358-8372.

Research output: Contribution to journalArticle

Graydon, Cole W. ; Cho, Soyoun ; Diamond, Jeffrey S. ; Kachar, Bechara ; von Gersdorff, Henrique ; Grimes, William N. / Specialized postsynaptic morphology enhances neurotransmitter dilution and high-frequency signaling at an auditory synapse. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 24. pp. 8358-8372.
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