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The Journal of Neurophysiology Vol. 84 No. 1 July 2000, pp. 189-204
Copyright ©2000 by the American Physiological Society
1Computation and Neural Systems Program, Division of Biology, 139-74 California Institute of Technology, Pasadena 91125; and 2Department of Biology, University of California at Riverside, Riverside, California 92521-0427
Kreiman, Gabriel,
Rüdiger Krahe,
Walter Metzner,
Christof Koch, and
Fabrizio Gabbiani.
Robustness and Variability of Neuronal Coding by
Amplitude-Sensitive Afferents in the Weakly Electric Fish
Eigenmannia. J. Neurophysiol. 84: 189-204, 2000. We investigated the variability of P-receptor afferent spike trains in
the weakly electric fish, Eigenmannia, to repeated presentations of random electric field AMs (RAMs) and quantified its
impact on the encoding of time-varying stimuli. A new measure of spike
timing jitter was developed using the notion of spike train distances
recently introduced by Victor and Purpura. This measure of
variability is widely applicable to neuronal responses, irrespective of
the type of stimuli used (deterministic vs. random) or the reliability
of the recorded spike trains. In our data, the mean spike count and its
variance measured in short time windows were poorly correlated with the
reliability of P-receptor afferent spike trains, implying that such
measures provide unreliable indices of trial-to-trial variability.
P-receptor afferent spike trains were considerably less variable than
those of Poisson model neurons. The average timing jitter of spikes lay
within 1-2 cycles of the electric organ discharge (EOD). At low, but
not at high firing rates, the timing jitter was dependent on the cutoff
frequency of the stimulus and, to a lesser extent, on its contrast.
When spikes were artificially manipulated to increase jitter,
information conveyed by P-receptor afferents was degraded only for
average jitters considerably larger than those observed experimentally. This suggests that the intrinsic variability of single spike trains lies outside of the range where it might degrade the information conveyed, yet still allows for improvement in coding by averaging across multiple afferent fibers. Our results were summarized in a
phenomenological model of P-receptor afferents, incorporating both
their linear transfer properties and the variability of their spike
trains. This model complements an earlier one proposed by Nelson et al.
for P-receptor afferents of Apteronotus. Because of their
relatively high precision with respect to the EOD cycle frequency,
P-receptor afferent spike trains possess the temporal resolution
necessary to support coincidence detection operations at the next stage
in the amplitude-coding pathway.
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