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.

Efficient Encoding of Vocalizations in the Auditory Midbrain

“…This hypothesis is grounded in observations of phase-locked responses throughout the auditory system, originating in the auditory nerve (Galambos and Davis, 1943) and extending to auditory cortex (Steinschneider et al, 1999). Information theoretic analyses of real and simulated sensory neurons have quantified how variability in spike timing reduces the information content of the neural code (Bialek et al, 1991;Rieke et al, 1993Rieke et al, , 1995Rokem et al, 2006;Shamir et al, 2007). We assumed that a neuron that was selective to a particular vocalization would generate responses with the least amount of spike time variability (jitter) across repeated presentations.…”

Adaptation Reduces Spike-Count Reliability, But Not Spike-Timing Precision, of Auditory Nerve Responses

“…For example, if all spikes occur in one bin, would be zero, when in fact some of those spikes may have occurred at different times within the bin. A conservative estimate then is to add a correction factor equal to half of the sampling bin size, which represents the case where half the observations occur on one side of the bin whereas the rest occur on the other (Rokem et al, 2006). Because the sampling bin was 10 s, the correction factor was only 5 s and was added to all estimates of .…”

GABAergic Excitation of Spider Mechanoreceptors Increases Information Capacity by Increasing Entropy Rather than Decreasing Jitter

“…Action potential timing jitter is a well known neuronal phenomenon with several possible sources (Rieke et al, 1997;Billimoria et al, 2006;Rokem et al, 2006;Kreuz et al, 2007). Reducing jitter can increase the fidelity of information transmission (Aldworth et al, 2005).…”