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1 University of Sydney
2 Leibniz Institute for Neurobiology
* To whom correspondence should be addressed. E-mail: peter.heil{at}ifn-magdeburg.de.
In vertebrate auditory systems, the conversion from graded receptor potentials across the hair-cell membrane into stochastic spike trains of the auditory-nerve (AN) fibers is performed by ribbon synapses. The statistics underlying this process constrain auditory coding but are not precisely known. Here, we examine the distributions of interspike intervals (ISIs) from spontaneous activity of AN fibers of the barn owl (Tyto alba), a nocturnal avian predator whose auditory system is specialized for precise temporal coding. The spontaneous activity of AN fibers, with the exception of those showing preferred intervals, is commonly thought to result from excitatory events generated by a homogeneous Poisson point process which lead to spikes unless the fiber is refractory. We show that the ISI distributions in the owl are better explained as resulting from the combination of a brief refractory period (about 0.5 ms) upon excitatory events generated by a homogeneous stochastic process where the distribution of inter-event intervals is a mixture of an exponential and a gamma distribution with shape factor 2, both with the same scaling parameter. The same model was previously shown to apply to AN fibers in the cat (Heil et al. J Neurosci 27:8457-8474, 2007). However, the mean proportions of exponentially versus gamma distributed intervals in the mixture were different for cat and owl. Furthermore, those proportions were constant across fibers in the cat while they co-varied with mean spontaneous rate and with characteristic frequency in the owl. We hypothesize that in birds, unlike in mammals, more than one ribbon may provide excitation to most fibers, accounting for the different proportions, and that variation in the number of ribbons may underlie the variation in the proportions.
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