Abstract
Coincidence detection by binaural neurons in the medial superior olive underlies sensitivity to interaural time difference (ITD) and interaural correlation (ρ). It is unclear whether this process is akin to a counting of individual coinciding spikes, or rather to a correlation of membrane potential waveforms resulting from converging inputs from each side. We analyzed spike trains of axons of the cat trapezoid body (TB) and auditory nerve (AN) in a binaural coincidence scheme. ITD was studied by delaying “ipsi-” vs. “contralateral” inputs; ρ was studied by using responses to different noises. We varied the number of inputs; the monaural and binaural threshold and the coincidence window duration. We examined physiological plausibility of output “spike trains” by comparing their rate and tuning to ITD and ρ to those of binaural cells. We found that multiple inputs are required to obtain a plausible output spike rate. In contrast to previous suggestions, monaural threshold almost invariably needed to exceed binaural threshold. Elevation of the binaural threshold to values larger than 2 spikes caused a drastic decrease in rate for a short coincidence window. Longer coincidence windows allowed a lower number of inputs and higher binaural thresholds, but decreased the depth of modulation. Compared to AN fibers, TB fibers allowed higher output spike rates for a low number of inputs, but also generated more monaural coincidences. We conclude that, within the parameter space explored, the temporal patterns of monaural fibers require convergence of multiple inputs to achieve physiological binaural spike rates; that monaural coincidences have to be suppressed relative to binaural ones; and that the neuron has to be sensitive to single binaural coincidences of spikes, for a number of excitatory inputs per side of 10 or less. These findings suggest that the fundamental operation in the mammalian binaural circuit is coincidence counting of single binaural input spikes.
Highlights
The comparison of sound waveforms at the two ears is a prime model for temporal processing in the central nervous system
We studied the output of a binaural coincidence detector to experimentally derived input spike trains
Instead of attempting to make a detailed biophysical model, we used a bare bones approach: the binaural neuron was reduced to the fundamental operation it performs on its excitatory inputs, i.e., an output spike was generated when input events occur close enough in time (Marsalek and Lansky, 2005; Jennings and Colburn, 2010; Sanda and Marsalek, 2012)
Summary
The comparison of sound waveforms at the two ears is a prime model for temporal processing in the central nervous system. The underlying circuit is of wide interest because it implements a neural analog to crosscorrelation, and is well-suited to study coincidence detection. Humans are exquisitely sensitive to two dimensions of binaural temporal differences: interaural time differences (ITDs) and interaural correlation (ρ) (Durlach and Colburn, 1978; Trahiotis et al, 2005). ITD is the dominant cue for horizontal sound localization. Sensitivity to rho is important to hear out signals in noise and for spatial hearing in complex acoustic environments such as concert halls
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