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The Journal of Neuroscience, August 1, 2007, 27(31):8457-8474; doi:10.1523/JNEUROSCI.1512-07.2007

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Behavioral/Systems/Cognitive
Spontaneous Activity of Auditory-Nerve Fibers: Insights into Stochastic Processes at Ribbon Synapses

Peter Heil,¹ Heinrich Neubauer,¹ Dexter R. F. Irvine,² and Mel Brown²

¹Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany, and ²School of Psychology, Psychiatry, and Psychological Medicine, Monash University, Vic 3800, Australia

Correspondence should be addressed to Peter Heil, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany. Email: peter.heil{at}ifn-magdeburg.de

In several sensory systems, the conversion of the representation of stimuli from graded membrane potentials into stochastic spike trains is performed by ribbon synapses. In the mammalian auditory system, the spiking characteristics of the vast majority of primary afferent auditory-nerve (AN) fibers are determined primarily by a single ribbon synapse in a single inner hair cell (IHC), and thus provide a unique window into the operation of the synapse. Here, we examine the distributions of interspike intervals (ISIs) of cat AN fibers under conditions when the IHC membrane potential can be considered constant and the processes generating AN fiber activity can be considered stationary, namely in the absence of auditory stimulation. Such spontaneous activity is commonly thought to result from an excitatory Poisson point process modified by the refractory properties of the fiber, but here we show that this cannot be the case. Rather, the ISI distributions are one to two orders of magnitude better and very accurately described as a result of a homogeneous stochastic process of excitation (transmitter release events) in which the distribution of interevent times is a mixture of an exponential and a gamma distribution with shape factor 2, both with the same scale parameter. Whereas the scale parameter varies across fibers, the proportions of exponentially and gamma distributed intervals in the mixture, and the refractory properties, can be considered constant. This suggests that all of the ribbon synapses operate in a similar manner, possibly just at different rates. Our findings also constitute an essential step toward a better understanding of the spike-train representation of time-varying stimuli initiated at this synapse, and thus of the fundamentals of temporal coding in the auditory pathway.

Key words: auditory nerve; spike timing; ribbon synapse; hair cell; refractoriness; spontaneous activity

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Received April 4, 2007; revised June 15, 2007; accepted June 25, 2007.

Correspondence should be addressed to Peter Heil, Leibniz Institute for Neurobiology, Brenneckestrasse 6, 39118 Magdeburg, Germany. Email: peter.heil{at}ifn-magdeburg.de

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				H. Neubauer, C. Koppl, and P. Heil Spontaneous Activity of Auditory Nerve Fibers in the Barn Owl (Tyto alba): Analyses of Interspike Interval Distributions J Neurophysiol, June 1, 2009; 101(6): 3169 - 3191. [Abstract] [Full Text] [PDF]

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