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J Neurophysiol (October 22, 2003). doi:10.1152/jn.00742.2003
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Submitted on August 1, 2003
Accepted on October 6, 2003

Two Distinct Types of Noisy Oscillators in Electroreceptors of Paddlefish

Alexander B. Neiman1 and David F. Russell2*

1 Center for Neurodynamics, University of Missouri at St. Louis, St. Louis, Missouri, USA; Department of Physics and Astronomy, University of Missouri at St. Louis, St. Louis, Missouri, USA
2 Center for Neurodynamics, University of Missouri at St. Louis, St. Louis, Missouri, USA; Department of Biology, University of Missouri at St. Louis, St. Louis, Missouri, USA

* To whom correspondence should be addressed. E-mail: drussell{at}admiral.umsl.edu.

Our computational analyses and experiments demonstrate that the ampullary electroreceptors in paddlefish (Polyodon spathula) contain two 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 ~26 Hz and ±70 µV voltage fluctuations at the canal skin pores, and gives rise to a noisy peak at Fe ~ 26 Hz in power spectra of spontaneous afferent firing. The second type of oscillator resides in afferent terminals, and is seen as a noisy peak at Fa ~ 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 Fa ± Fe are consistent with epithelia-to-afferent unidirectional synaptic coupling, or alternatively, nonlinear mixing of the two oscillatory processes. External stimulation affects the frequency of only the afferent oscillator, not the epithelial oscillators. Application of temperature gradients localized the Fe and Fa oscillators to different depths below the skin. Having two 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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