The response properties of ampullary electroreceptors of paddlefish, Polyodon spathula, were studied in vivo, as single-unit afferent responses to external electrical stimulation with varied intensities of several types of noise waveforms, all Gaussian and zero-mean. They included broadband white noise, Ornstein-Uhlenbeck noise, low- or high-frequency band-limited noise, or natural noise recorded from swarms of Daphnia zooplankton prey, or from individual prey. Normally the afferents fire spontaneously in a tonic manner, which is actually quasiperiodic due to embedded oscillators. 1) Weak noise stimuli increased the variability of afferent firing, but it remained tonic. 2) In contrast, stimulation with less-weak broadband noise led to a qualitative change of the firing patterns, to parabolic bursting, even though the mean firing rate was scarcely affected. 3) The transition to afferent bursting was marked by the development of two well-separated timescales: the fast frequency of spiking inside bursts at ≤250 spikes/s and the slow frequency of burst occurrences at about 9 (range 5-13) bursts/s. These two time-scales were manifested as two regimes in afferent power spectra, bimodal interspike interval histograms, return maps, and autocorrelation functions of afferent spike trains. 4) The stochastic approximately 9-Hz bursts were not simply driven by similar-frequency components of noise stimuli because bursts could be dissociated from stimulus waveforms using high-pass filtered noise, or a 0.1-Hz sine-wave stimulus. 5) Arrhenius plots showed that the threshold noise intensity required to elicit bursting depended on the frequency content of a noise stimulus, being lowest, about 1.2 μV/cm, for stimuli matching the 1- to 20-Hz best response band of these cathodally excited ampullary electroreceptors. This is only slightly higher than previous behavioral estimates of the electrosensory threshold as 0.5 μV/cm. 6) Comparable threshold values for bursting came from an alternate analytical approach, based on correlation times of spike trains. 7) Simultaneous recordings from pairs of afferents showed that their bursting frequencies (bursts/s) always converged as the amplitude of a noise stimulus was raised. Thus the slow timescale of bursting is similar for different electroreceptors, even though their mean spiking rates can differ. In conclusion, the ampullary electroreceptors of paddlefish have two distinct modes of operation: their spontaneous tonic firing is modulated by the weakest stimuli, but they switch to bursting output for less-weak stimuli. We propose that afferent bursting may mediate close-range tracking of planktonic prey.