Robustness and variability of neuronal coding by amplitude-sensitive afferents in the weakly electric fish eigenmannia

We investigated the variability of P-receptor afferent spike trains in the weakly electric fish, Eigenmannia, to repeated presentations of random elec tric field AMs (RAMs) and quantified its impact on the encoding of time-var ying 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, irr espective of the type of stimuli used (deterministic vs. random) or the rel iability of the recorded spike trains. In our data, the mean spike count an d its variance measured in short time windows were poorly correlated with t he reliability of P-receptor afferent spike trains, implying that such meas ures provide unreliable indices of trial-to-trial variability. P-receptor a fferent 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 manipu lated to increase jitter, information conveyed by P-receptor afferents was degraded only for average jitters considerably larger than those observed e xperimentally. This suggests that the intrinsic variability of single spike trains lies outside of the range where it might degrade the information co nveyed, yet still allows for improvement in coding by averaging across mult iple afferent fibers. Our results were summarized in a phenomenological mod el of P-receptor afferents, incorporating both their linear transfer proper ties and the variability of their spike trains. This model complements an e arlier one proposed by Nelson et al. for P-receptor afferents of Apteronotu s. Because of their relatively high precision with respect to the EOD cycle frequency, P-receptor afferent spike trains possess the temporal resolutio n necessary to support coincidence detection operations at the next stage i n the amplitude-coding pathway.