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Two Distinct Types of Noisy Oscillators in Electroreceptors of Paddlefish

Center for Neurodynamics, ¹Department of Physics and Astronomy, and ²Department of Biology, University of Missouri at St. Louis, St. Louis, Missouri 63121-4499

Submitted 31 July 2003; accepted in final form 10 October 2003

Our computational analyses and experiments demonstrate that ampullary electroreceptors in paddlefish (Polyodon spathula) contain 2 distinct types of continuously active noisy oscillators. The spontaneous firing of afferents reflects both rhythms, and as a result is stochastically biperiodic (quasiperiodic). The first type of oscillator resides in the sensory epithelia, is recorded as approximately 26 Hz and ±70 µV voltage fluctuations at the canal skin pores, and gives rise to a noisy peak at f_e 26 Hz in power spectra of spontaneous afferent firing. The second type of oscillator resides in afferent terminals, is seen as a noisy peak at f_a 30–70 Hz that dominates the power spectra of spontaneous afferent firing, and corresponds to the mean spontaneous firing rate. Sideband peaks at frequencies of f_a ± f_e are consistent with epithelia-to-afferent unidirectional synaptic coupling or, alternatively, nonlinear mixing of the 2 oscillatory processes. External stimulation affects the frequency of only the afferent oscillator, not the epithelial oscillators. Application of temperature gradients localized the f_e and f_a oscillators to different depths below the skin. Having 2 distinct types of internal oscillators is a novel form of organization for peripheral sensory receptors, of relevance for other hair cell sensory receptors.

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