Abstract
Without stimuli, hair cells spontaneously release neurotransmitter leading to spontaneous generation of action potentials (spikes) in innervating afferent neurons. We analyzed spontaneous spike patterns recorded from the lateral line of zebrafish and found that distributions of interspike intervals (ISIs) either have an exponential shape or an “L” shape that is characterized by a sharp decay but wide tail. ISI data were fitted to renewal-process models that accounted for the neuron refractory periods and hair-cell synaptic release. Modeling the timing of synaptic release using a mixture of two exponential distributions yielded the best fit for our ISI data. Additionally, lateral line ISIs displayed positive serial correlation and appeared to exhibit switching between faster and slower modes of spike generation. This pattern contrasts with previous findings from the auditory system where ISIs tended to have negative serial correlation due to synaptic depletion. We propose that afferent neuron innervation with multiple and heterogenous hair-cells synapses, each influenced by changes in calcium domains, can serve as a mechanism for the random switching behavior. Overall, our analyses provide evidence of how physiological similarities and differences between synapses and innervation patterns in the auditory, vestibular, and lateral line systems can lead to variations in spontaneous activity.
Highlights
Pattern of spikes determined by both presynaptic and postsynaptic processes
In order to analyze the temporal patterns of spontaneous spiking in afferent neurons of the lateral line, we began by fitting each interspike intervals (ISIs) distribution to an exponential distribution
By comparing the parameters needed to describe distributions of ISIs recorded from afferent neurons in the lateral line of zebrafish with those previously published for the auditory system, we demonstrated that the auditory depletion model does not account for the spike patterns of the lateral line system
Summary
Pattern of spikes determined by both presynaptic and postsynaptic processes. The postsynaptic mechanisms are especially evident in the vestibular system where regular and irregular classes of afferent neurons display tonic and phasic (respectively) spike patterns based on differences in their synaptic connectivity, ion channel expression, and intrinsic excitability[8,14,15,16,17]. The time required to replenish vesicles at a single ribbon synapse limits the frequency of synaptic release and the timing of spontaneous spikes in the innervating afferent neuron These single synaptic connections result in a temporal pattern of spontaneous spiking that is strongly dependent on the depletion state of an individual hair cell. In contrast to the auditory system, the multiple synaptic contacts of vestibular and lateral line neurons led us to hypothesize that spike patterns would be less constrained by synaptic depletion since other innervating and non-depleted synapses could still drive spiking in the innervating afferent neuron To test this hypothesis, we analyzed patterns of spontaneous spiking recorded from afferent neurons in the zebrafish lateral line by quantifying the underlying characteristics of ISI distributions and the correlation between consecutive ISIs. Using renewal processes, we considered three different distributions for synaptic release time and compared the resulting ISI distributions to our electrophysiological data. Variations in synaptic physiology between the different sensory systems can lead to distinct patterns in spontaneous activity that may serve for unique information transfer dictated by the different systems[18,19]
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