Spontaneous Activity of Auditory Nerve Fibers in the Barn Owl (Tyto alba): Analyses of Interspike Interval Distributions

Abstract

Neubauer H, Köppl C, Heil P. Spontaneous activity of auditorynerve fibers in the barn owl (Tyto alba): analyses of interspike interval distributions. J Neurophysiol 101: 3169 -3191, 2009. First published April 8, 2009 doi:10.1152/jn.90779.2008. 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 action of a brief refractory period (ϳ0.5 ms) on excitatory events generated by a homogeneous stochastic process where the distribution of interevent 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. 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, whereas they covaried 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.

Mechanism of Spontaneous Activity in Afferent Neurons of the Zebrafish Lateral-Line Organ

“…Similar to neurons described in the auditory and vestibular systems of other species, our recordings of spontaneous spiking in zebrafish lateral-line neurons revealed stochastic patterns of activity (Heil et al, 2007; Neubauer et al, 2009). Spontaneous activity has been shown to be dependent on L-type calcium channel activity (Robertson and Paki, 2002).…”

Spike timing in auditory‐nerve fibers during spontaneous activity and phase locking

“…This increase reflects spike‐history effects that can last for tens of milliseconds, as in the example illustrated in Figure C (here, the apparent decrease in the hazard‐rate function with increasing ISI above ∼34 ms is probably due to noise). Similar probability density and hazard‐rate functions can be found in numerous publications (e.g., Gaumond et al, ; Gray, ; Heil et al, ; Köppl and Manley, ; Li and Young, ; Liberman and Kiang, ; Lowen and Teich, ; Lütkenhöner et al, ; Manley and Robertson, ; Neubauer et al, ; Prijs et al, ; Teich and Lowen, ). It is worth noting that although cumulative distribution functions, probability density functions, and hazard‐rate functions can reveal some spike‐history effects, they do not reveal all history effects, such as the presence of correlations in a sequence of ISIs.…”

Birds – same thing, but different? Convergent evolution in the avian and mammalian auditory systems provides informative comparative models

“…Neither birds nor any other non-mammals show similar afferent physiological subclasses, however, their synaptic ultrastructure has not been examined in comparable detail. A recent study of the stochastic properties of spontaneous spike trains of afferent fibres in the barn owl (Neubauer et al, 2009) highlighted the possibility that the association of only one synaptic ribbon with each afferent terminal may be a uniquely mammalian feature. In the owl, but not in the cat, a salient parameter of the inter-spike interval distribution was correlated with mean spontaneous rate.…”

“…In the owl, but not in the cat, a salient parameter of the inter-spike interval distribution was correlated with mean spontaneous rate. Although an indirect indicator, this correlation is plausibly explained by assuming that a varying number of synaptic ribbons feeds into different afferent fibres (Neubauer et al, 2009). This hypothesis is supported by ultrastructural data which suggest that several ribbons per afferent terminal are commonly found across a wide variety of hair-cell end organs, including the avian basilar papilla (e.g., Wegner, 1982;Chandler, 1984;Popper and Saidel, 1990;Martinez-Dunst et al, 1997).…”