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The Journal of Neuroscience, August 27, 2003, 23(21):7940-7949
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Binary Spiking in Auditory Cortex
Michael R. DeWeese, Michael Wehr, andAnthony M. Zador Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724
Neurons are often assumed to operate in a highly unreliable manner: a neuron can signal the same stimulus with a variable number of action potentials. However, much of the experimental evidence supporting this view was obtained in the visual cortex. We have, therefore, assessed trial-to-trial variability in the auditory cortex of the rat. To ensure single-unit isolation, we used cell-attached recording. Tone-evoked responses were usually transient, often consisting of, on average, only a single spike per stimulus. Surprisingly, the majority of responses were not just transient, but were also binary, consisting of 0 or 1 action potentials, but not more, in response to each stimulus; several dramatic examples consisted of exactly one spike on 100% of trials, with no trial-to-trial variability in spike count. The variability of such binary responses differs from comparably transient responses recorded in visual cortical areas such as area MT, and represent the lowest trial-to-trial variability mathematically possible for responses of a given firing rate. Our study thus establishes for the first time that transient responses in auditory cortex can be described as a binary process, rather than as a highly variable Poisson process. These results demonstrate that cortical architecture can support a more precise control of spike number than was previously recognized, and they suggest a re-evaluation of models of cortical processing that assume noisiness to be an inevitable feature of cortical codes.
Key words: auditory cortex; Poisson spiking; neural coding; neural reliability; neural computation; cell-attached recording
Received May 22, 2003; revised June 27, 2003; accepted June 30, 2003.
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