Temporal precision of speech coded into nerve-action potentials

Abstract

The auditory pathway is an excellent system to study temporal aspects of neuronal processing. Unlike other sensory systems, temporal cues cover an extremely wide range of information: for sound localization, interaural time differences with a precision of tens of microseconds are extracted. Phase-locking of auditory nerve responses, which is related to the coding of the temporal fine structure, occurs from the lowest audible frequencies probably up to 3 kHz in humans. Amplitude modulations in speech signals are processed in the ms to tens of ms range. And finally, the energy of spoken speech itself is modulated with a frequency of about 4 Hz, corresponding to a syllable frequency in the order of few hundreds of ms. To extract temporal cues at all timescales, it is important to understand how temporal information is coded. We investigate temporal coding of speech signals using the methods of information theory and a model of the human inner ear. The model is based on a traveling-wave model, a nonlinear compression stage which mimics the function of the amplifier, a model of the sensory cells, the afferent synapse and spike generation (Sumner ) which we extended to replicate offset adaptation (Zhang). We used the action potentials of the auditory nerve to drive Hodgkin-Huxley-type point models of various neurons in the cochlear nucleus. In this investigation we only report data from onset neurons, which exhibit extraordinary fast membrane time-constants below 1 ms. Onset neurons are known for their precise temporal processing. They achieve precisely timed action potentials by coincidence detection: they fire only if at least 10% of the auditory nerve fibers which innervate them fire synchronously. With information theory, we analyzed the transmitted information rate coded in neural spike trains of modeled neurons in the cochlear nucleus for vowels. We found that onset neurons are able to code temporal information with sub-millisecond precision (<0.02 ms) across a wide range of characteristic frequencies. Temporal information is coded by precisely timed spikes per se, not only temporal fine structure. Moreover, the major portion of information (60%) is coded with a temporal precision from 0.2 to 4 ms. Enhancing the temporal resolution from 10 ms to 3 ms and from 3 ms to 0.3 ms is expected to increase the transmitted information by approximately twofold and 2.5 fold, respectively. In summary, our results provide quantitative insight into temporal processing strategies of neuronal speech processing. We conclude that coding of information in the time domain might be essential to complement the rate-place code, especially in adverse acoustical environments. Acknowledgments:Supported by within the Munich Bernstein Center for Computational Neuroscience by the German Federal Ministry of Education and Research (reference numbers 01GQ0441 and 01GQ0443).