Spike-Timing Precision Underlies the Coding Efficiency of Auditory Receptor Neurons

Abstract

Sensory systems must translate incoming signals quickly and reliably so that an animal can act successfully in its environment. Even at the level of receptor neurons, however, functional aspects of the sensory encoding process are not yet fully understood. Specifically, this concerns the question how stimulus features and neural response characteristics lead to an efficient transmission of sensory information. To address this issue, we have recorded and analyzed spike trains from grasshopper auditory receptors, while systematically varying the stimulus statistics. The stimulus variations profoundly influenced the efficiency of neural encoding. This influence was largely attributable to the presence of specific stimulus features that triggered remarkably precise spikes whose trial-to-trial timing variability was as low as 0.15 ms--one order of magnitude shorter than typical stimulus time scales. Precise spikes decreased the noise entropy of the spike trains, thereby increasing the rate of information transmission. In contrast, the total spike train entropy, which quantifies the variety of different spike train patterns, hardly changed when stimulus conditions were altered, as long as the neural firing rate remained the same. This finding shows that stimulus distributions that were transmitted with high information rates did not invoke additional response patterns, but instead displayed exceptional temporal precision in their neural representation. The acoustic stimuli that led to the highest information rates and smallest spike-time jitter feature pronounced sound-pressure deflections lasting for 2-3 ms. These upstrokes are reminiscent of salient structures found in natural grasshopper communication signals, suggesting that precise spikes selectively encode particularly important aspects of the natural stimulus environment.