Two distinct types of noisy oscillators in electroreceptors of paddlefish

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 microV voltage fluctuations at the canal skin pores, and gives rise to a noisy peak at f(e) approximately 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) approximately 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.