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The Journal of Neuroscience, June 13, 2007, 27(24):6461-6472; doi:10.1523/JNEUROSCI.5239-06.2007

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Behavioral/Systems/Cognitive
Adaptation Reduces Spike-Count Reliability, But Not Spike-Timing Precision, of Auditory Nerve Responses

Michael Avissar,^1,2 Adam C. Furman,² James C. Saunders,² and Thomas D. Parsons^1,2

¹Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, and ²Department of Otorhinolaryngology, Head and Neck Surgery, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Correspondence should be addressed to Dr. Thomas D. Parsons, University of Pennsylvania, 382 West Street Road, Kennett Square, PA 19348. Email: thd{at}vet.upenn.edu

Sensory systems use adaptive coding mechanisms to filter redundant information from the environment to efficiently represent the external world. One such mechanism found in most sensory neurons is rate adaptation, defined as a reduction in firing rate in response to a constant stimulus. In auditory nerve, this form of adaptation is likely mediated by exhaustion of release-ready synaptic vesicles in the cochlear hair cell. To better understand how specific synaptic mechanisms limit neural coding strategies, we examined the trial-to-trial variability of auditory nerve responses during short-term rate-adaptation by measuring spike-timing precision and spike-count reliability. After adaptation, precision remained unchanged, whereas for all but the lowest-frequency fibers, reliability decreased. Modeling statistical properties of the hair cell–afferent fiber synapse suggested that the ability of one or a few vesicles to elicit an action potential reduces the inherent response variability expected from quantal neurotransmitter release, and thereby confers the observed count reliability at sound onset. However, with adaptation, depletion of the readily releasable pool of vesicles diminishes quantal content and antagonizes the postsynaptic enhancement of reliability. These findings imply that during the course of short-term adaptation, coding strategies that employ a rate code are constrained by increased neural noise because of vesicle depletion, whereas those that employ a temporal code are not.

Key words: auditory nerve; neural adaptation; hair cell; ribbon synapse; spike timing; neural variability

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Received Dec. 4, 2006; revised May 8, 2007; accepted May 9, 2007.

Correspondence should be addressed to Dr. Thomas D. Parsons, University of Pennsylvania, 382 West Street Road, Kennett Square, PA 19348. Email: thd{at}vet.upenn.edu

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