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The Journal of Neuroscience, December 10, 2008, 28(50):13649-13661; doi:10.1523/JNEUROSCI.1792-08.2008

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Cellular/Molecular
Spike-Rate Coding and Spike-Time Coding Are Affected Oppositely by Different Adaptation Mechanisms

Steven A. Prescott^1,2 and Terrence J. Sejnowski^1,3

¹Howard Hughes Medical Institute, Computational Neurobiology Laboratory, Salk Institute, La Jolla, California 92037, ²Department of Neurobiology, University of Pittsburgh, Pittsburgh, Pennsylvania 15213, and ³Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093

Correspondence should be addressed to Steven A. Prescott, Department of Neurobiology, University of Pittsburgh, 200 Lothrop Street, Pittsburgh, PA 15213. Email: prescott{at}neurobio.pitt.edu

Spike-frequency adaptation causes reduced spiking during prolonged stimulation, but the full impact of adaptation on neural coding is far more complex, especially if one takes into account the diversity of biophysical mechanisms mediating adaptation and the different ways in which neural information can be encoded. Here, we show that adaptation has opposite effects depending on the neural coding strategy and the biophysical mechanism responsible for adaptation. Under noisy conditions, calcium-activated K⁺ current (I_AHP) improved efficient spike-rate coding at the expense of spike-time coding by regularizing the spike train elicited by slow or constant inputs; noise power was increased at high frequencies but reduced at low frequencies, consistent with noise shaping that improves coding of low- frequency signals. In contrast, voltage-activated M-type K⁺ current (I_M) improved spike-time coding at the expense of spike-rate coding by stopping the neuron from spiking repetitively to slow inputs so that it could generate isolated, well timed spikes in response to fast inputs. Using dynamical systems analysis, we demonstrate how I_AHP minimizes perturbation of the interspike interval caused by high- frequency noise, whereas I_M minimizes disruption of spike-timing accuracy caused by repetitive spiking. The dichotomous outcomes are related directly to the distinct activation requirements for I_AHP and I_M, which in turn dictate whether those currents mediate negative feedback onto spiking or membrane potential. Thus, based on their distinct activation properties, I_AHP implements noise shaping that improves spike-rate coding of low-frequency signals, whereas I_M implements high-pass filtering that improves spike-time coding of high- frequency signals.

Key words: interspike interval correlation; noise shaping; ROC analysis; spike-timing reliability; neural code; noise

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Received April 23, 2008; revised Oct. 15, 2008; accepted Oct. 21, 2008.

Correspondence should be addressed to Steven A. Prescott, Department of Neurobiology, University of Pittsburgh, 200 Lothrop Street, Pittsburgh, PA 15213. Email: prescott{at}neurobio.pitt.edu

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