On the Origin of the Extracellular Field Potential in the Nucleus Laminaris of the Barn Owl (Tyto alba)

The neurophonic is a sound-evoked, frequency-following potential that can be recorded extracellularly in nucleus laminaris of the barn owl. The origin of the neurophonic, and thus the mechanisms that give rise to its exceptional temporal precision, has not yet been identified. Putative generators of the neurophonic are the activity of afferent axons, synaptic activation of laminaris neurons, or action potentials in laminaris neurons. To identify the generators, we analyzed the neurophonic in the high-frequency (>2.5 kHz) region of nucleus laminaris in response to monaural pure-tone stimulation. The amplitude of the neurophonic is typically in the millivolt range. The signal-to-noise ratio reaches values beyond 30 dB. To assess which generators could give rise to these large, synchronous extracellular potentials, we developed a computational model. Spike trains were produced by an inhomogeneous Poisson process and convolved with a spike waveform. The model explained the dependence of the simulated neurophonic on parameters such as the mean rate, the vector strength of phase locking, the number of statistically independent sources, and why the signal-to-noise ratio is independent of the spike waveform and subsequent filtering of the signal. We found that several hundred sources are needed to reach the observed signal-to-noise ratio. The summed coherent signal from the densely packed afferent axons and activation of their synapses on laminaris neurons are alone sufficient to explain the measured properties of the neurophonic.