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J Neurosci. 2014 Jun 11;34(24):8358-72. doi: 10.1523/JNEUROSCI.4493-13.2014.

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

Author information

1
Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, and Section on Structural Cell Biology, National Institute on Deafness and Other Communication Disorders, Bethesda, Maryland 20892.
2
Vollum Institute, Oregon Health & Science University, Portland, Oregon 97239, and.
3
Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, and.
4
Section on Structural Cell Biology, National Institute on Deafness and Other Communication Disorders, Bethesda, Maryland 20892.
5
Synaptic Physiology Section, National Institute of Neurological Disorders and Stroke, and Howard Hughes Medical Institute/University of Washington, Department of Biophysics and Physiology, Seattle, Washington 98195 wgrimes8@gmail.com.

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.

KEYWORDS:

auditory; diffusion; glutamate; hair cell; ribbon synapse; synapse

PMID:
24920639
PMCID:
PMC4051984
DOI:
10.1523/JNEUROSCI.4493-13.2014
[Indexed for MEDLINE]
Free PMC Article
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