Stochastic resonance is the phenomenon whereby the addition of an optimal level of noise to a weak information-carrying input to certain nonlinear systems can enhance the information content at their outputs. Computer analysis of spike trains has been needed to reveal stochastic resonance in the responses of sensory receptors except for one study on human psychophysics. But is an animal aware of, and can it make use of, the enhanced sensory information from stochastic resonance? Here, we show that stochastic resonance enhances the normal feeding behaviour of paddlefish (Polyodon spathula), which use passive electroreceptors to detect electrical signals from planktonic prey. We demonstrate significant broadening of the spatial range for the detection of plankton when a noisy electric field of optimal amplitude is applied in the water. We also show that swarms of Daphnia plankton are a natural source of electrical noise. Our demonstration of stochastic resonance at the level of a vital animal behaviour, feeding, which has probably evolved for functional success, provides evidence that stochastic resonance in sensory nervous systems is an evolutionary adaptation.

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We report experimental observation of phase synchronization in an array of nonidentical noncoupled noisy neuronal oscillators, due to stimulation with external noise. The synchronization derives from a noise-induced qualitative change in the firing pattern of single neurons, which changes from a quasiperiodic to a bursting mode. We show that at a certain noise intensity the onsets of bursts in different neurons become synchronized, even though the number of spikes inside the bursts may vary for different neurons. We demonstrate this effect both experimentally for the electroreceptor afferents of paddlefish, and numerically for a canonical phase model, and characterize it in terms of stochastic synchronization.

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.

Synchronization of electrosensitive cells of the paddlefish is studied by means of electrophysiological experiments. Different types of noisy phase locked regimes are observed. The experimental data are compared with computer simulations of a noise-mediated modified Hodgkin-Huxley neuron model and of a stochastic circle map. [S0031-9007(98) Since the historical work of Huygens [1], synchronization has attracted much attention. It occurs when a nonlinear oscillator, showing a stable limit cycle [2], is subjected to an external time-dependent force or is coupled with another oscillator. Synchronization has been observed in a wide variety of natural and man-made systems [3]. It is also important in various biological systems, including, most recently, the human heart-respiratory system, as well as certain brain functions revealed by magnetoencephalography [4].In this Letter we study experimentally the synchronization of electroreceptors of the paddlefish, Polydon spathula, which feeds on zooplankton, e.g., the water flea, Daphnia [5]. While adult fishes filter feed almost entirely on clouds of zooplankton, small paddlefish are particulate feeders, selecting and capturing zooplankton individually [6,7]. The paddlefish is named for its large rostrum, or "paddle," which is covered with an array of thousands of electrosensory organs (see Fig. 1). Recently it has been demonstrated that paddlefish are sensitive to weak electric fields, which they use for sensing prey electrically in the dark [8]. Both natural zooplankton and artificial electric dipoles were used to stimulate feeding [8].Each of the electrosensory organs on the rostrum ( Fig. 1) consists of a patch of ampullary-type cells, which synapse onto primary afferent (sensory) neurons sending long axons to the brain. The latter will be referred to as "electroreceptor cells" because their spike trains can be recorded, and are modulated by weak electric fields near the rostrum. We present here the first direct evidence that each cell contains a noise-mediated oscillator by showing that it can be synchronized with an external signal. In the absence of external stimuli, the cells generate noisy nearly periodic spike sequences. Noise mediated oscillators were previously studied in the electroreceptive cells of the dogfish (a kind of shark) and catfish [9] only indirectly by means of spike interval histograms. They have never been shown to exist in the primitive species of the order acipenseriformes (sturgeons and paddlefish).Extracellular recordings were obtained in vivo from single cells. In our experiments (for details see [8]) a cell was stimulated by a weak electric and/or magnetic field generated by a dipole or a small coil located near the rostrum. The electric field strengths (a few tens of mV ͞cm) were comparable in magnitude to those generated by the zooplankton. Recordings of the spike train from the cell and periodic signal from the dipole were digitized and analyzed by computer. An example recording is shown in Fig. 1. The synchronized 1:5 mode locking (5 s...

Many of the motor neurons in the lobster (Panulirus interruptus) stomatogastric ganglion exhibit plateau potentials; that is, prolonged regenerative depolarizations resulting from active membrane properties, that drive the neurons to fire impulses during bursts. Plateaus are latent in isolated ganglia but are unmasked by central input. These findings emphasize the role of cellular properties as compared to synaptic wiring in the production of cyclic motor patterns by ensembles of neurons.

Recent behavior experiments have demonstrated that paddlefish can make use of stochastic resonance while feeding on Daphnia plankton. Here we calculate the information content of the noisy Daphnia signal at the paddlefish rostrum using an exact statistical treatment of threshold stochastic resonance as a minimal neural model. These calculations compare well with experimentally obtained data on paddlefish strikes at Daphnia prey.

A novel electrosensory function is presented for the large, plankton-feeding, freshwater paddle¢sh, Polyodon spathula, along with a hypothesis which accounts for the distinctive, elongated rostrum of this unusual ¢sh. Behavioural experiments conducted in the`dark' (under infrared illumination), to eliminate vision, show that paddle¢sh e¤ciently capture planktonic prey to distances up to 80^90 mm. They make feeding strikes at dipole electrodes in response to weak low-frequency electrical currents. Fish also avoid metal obstacles placed in the water, again in the dark. Electrophysiological experiments con¢rm that the Lorenzinian ampullae of paddle¢sh are sensitive to weak, low-frequency electrical signals, and demonstrate unequivocally that they respond to the very small electrical signals generated by their natural zooplankton prey (Daphnia sp.). We propose that the rostrum constitutes the biological equivalent of an electrical antenna, enabling the ¢sh to accurately detect and capture its planktonic food in turbid river environments where vision is severely limited. The electrical sensitivity of paddle¢sh to metallic substrates may interfere with their migrations through locks and dams.