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The Journal of Neuroscience, June 1, 2005, 25(22):5323-5332; doi:10.1523/JNEUROSCI.0359-05.2005

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Behavioral/Systems/Cognitive
Dejittered Spike-Conditioned Stimulus Waveforms Yield Improved Estimates of Neuronal Feature Selectivity and Spike-Timing Precision of Sensory Interneurons

Zane N. Aldworth, John P. Miller, Tomás Gedeon, Graham I. Cummins, and Alexander G. Dimitrov

Center for Computational Biology, Montana State University, Bozeman, Montana 59717

What is the meaning associated with a single action potential in a neural spike train? The answer depends on the way the question is formulated. One general approach toward formulating this question involves estimating the average stimulus waveform preceding spikes in a spike train. Many different algorithms have been used to obtain such estimates, ranging from spike-triggered averaging of stimuli to correlation-based extraction of "stimulus-reconstruction" kernels or spatiotemporal receptive fields. We demonstrate that all of these approaches miscalculate the stimulus feature selectivity of a neuron. Their errors arise from the manner in which the stimulus waveforms are aligned to one another during the calculations. Specifically, the waveform segments are locked to the precise time of spike occurrence, ignoring the intrinsic "jitter" in the stimulus-to-spike latency. We present an algorithm that takes this jitter into account. "Dejittered" estimates of the feature selectivity of a neuron are more accurate (i.e., provide a better estimate of the mean waveform eliciting a spike) and more precise (i.e., have smaller variance around that waveform) than estimates obtained using standard techniques. Moreover, this approach yields an explicit measure of spike-timing precision. We applied this technique to study feature selectivity and spike-timing precision in two types of sensory interneurons in the cricket cercal system. The dejittered estimates of the mean stimulus waveforms preceding spikes were up to three times larger than estimates based on the standard techniques used in previous studies and had power that extended into higher-frequency ranges. Spike timing precision was 5 ms.

Key words: information theory; interneuron; mechanosensory; receptive field; response; temporal coding

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Received Jan 26, 2005; revised April 21, 2005; accepted April 21, 2005.

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