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The Journal of Neuroscience, December 5, 2007, 27(49):13384-13392; doi:10.1523/JNEUROSCI.2816-07.2007

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Behavioral/Systems/Cognitive
Counting on Inhibition and Rate-Dependent Excitation in the Auditory System

Christofer J. Edwards, Christopher J. Leary, and Gary J. Rose

University of Utah, Department of Biology, Salt Lake City, Utah 84112

Correspondence should be addressed to Dr. Gary J. Rose, Department of Biology, University of Utah, 257 South 1400 East Room 204, Salt Lake City, UT 84112. Email: rose{at}bioscience.utah.edu

The intervals between acoustic elements are important in audition. Although neurons have been recorded that show interval tuning, the underlying mechanisms are unclear. The anuran auditory system is well suited for addressing this problem. One class of midbrain neurons in anurans responds selectively over a narrow range of pulse-repetition rates (PRRs) and only after several sound pulses have occurred with the "correct" timing. This "interval-counting" process can be reset by a single incorrect interval. Here we show, from whole-cell patch recordings of midbrain neurons in vivo, that these computations result from interplay between inhibition and rate-dependent excitation. An individual pulse or slowly repeated pulses elicited inhibition and subthreshold excitation. Excitation was markedly enhanced, however, when PRR was increased over a neuron-specific range. Spikes were produced when the enhanced excitation overcame the inhibition. Interval-number thresholds were positively correlated with the strength of inhibition and number of intervals required to augment the excitation. Accordingly, interval-number thresholds decreased when inhibition was attenuated by loading cells with cesium fluoride. The selectivity of these neurons for the interpulse interval, and therefore PRR, was related to the time course of excitatory events and the rate dependence of enhancement; for cells that were tuned to longer intervals, EPSPs were broader, and enhancement occurred at slower PRRs. The frequency tuning of the inhibition generally spanned that of the excitation, consistent with its role in temporal computation. These findings provide the first mechanistic understanding of interval selectivity and counting in the nervous system.

Key words: intracellular; torus semicircularis; temporal coding; amplitude modulation; inferior colliculus; anuran; auditory; acoustic; in vivo; interval; neuroethology; patch clamp

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Received June 20, 2007; revised Sept. 26, 2007; accepted Oct. 2, 2007.

Correspondence should be addressed to Dr. Gary J. Rose, Department of Biology, University of Utah, 257 South 1400 East Room 204, Salt Lake City, UT 84112. Email: rose{at}bioscience.utah.edu

This article has been cited by other articles:

				C. J. Leary Hormones and acoustic communication in anuran amphibians Integr. Comp. Biol., October 1, 2009; 49(4): 452 - 470. [Abstract] [Full Text] [PDF]

				B. A. Carlson Temporal-Pattern Recognition by Single Neurons in a Sensory Pathway Devoted to Social Communication Behavior J. Neurosci., July 29, 2009; 29(30): 9417 - 9428. [Abstract] [Full Text] [PDF]

				F. Creutzig, S. Wohlgemuth, A. Stumpner, J. Benda, B. Ronacher, and A. V. M. Herz Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron J. Neurosci., February 25, 2009; 29(8): 2575 - 2580. [Abstract] [Full Text] [PDF]

				C. J. Edwards, C. J. Leary, and G. J. Rose Mechanisms of Long-Interval Selectivity in Midbrain Auditory Neurons: Roles of Excitation, Inhibition, and Plasticity J Neurophysiol, December 1, 2008; 100(6): 3407 - 3416. [Abstract] [Full Text] [PDF]

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