High-frequency electrical tuning and linear filter properties of Knollenorgan electroreceptors of mormyrid electric fish.

Abstract

Electrical tuning allows auditory, vestibular, and electrosensory receptor cells to filter sensory signals and selectively transmit specific stimulus frequencies. In auditory hair cells, electrical tuning results from membrane potential resonance produced by voltage-gated Ca and K(Ca) channels, with variable kinetics that generate different tuning properties. Such resonance has been observed only up to ∼1 kHz, however. Additionally, in most species that employ electrical tuning, hearing is constrained to this relatively low-frequency range, raising the question of whether electrical tuning can extend to higher frequencies. Here we investigated this possibility by studying tuning and transduction properties of Knollenorgans, a class of tuberous electroreceptors of mormyrid electric fish. These organs, which generate spike-like receptor potentials, detect species-specific electric organ discharges (EODs). To test whether fish with brief EODs had correspondingly high-frequency electrical tuning, we recorded tuning curves from Knollenorgans of three species, Brevimyrus niger, Gnathonemus petersii, and Pollimyrus adspersus, which have EODs with spectral components exceeding 5 kHz. All species had receptors tuned to a range of frequencies tiling the species-specific EOD spectrum, with best frequencies extending beyond 10 kHz in P. adspersus. We also computed the impulse response of each Knollenorgan by reverse-correlating spikes elicited by white noise stimuli. After incorporation of a spike threshold non-linearity, convolving the impulse response with arbitrary stimulus waveforms successfully predicted spike patterns experimentally evoked by these inputs. These analyses demonstrate that differential electrical tuning properties of Knollenorgans produce distinct, well-timed spike responses that reliably encode time-varying electrical signals at frequencies up to 20 kHz. KEY POINTS: Knollenorgans, among the tuberous electroreceptors of mormyrid electric fish, are modified hair cells that transduce electrical signals into spike-like receptor potentials. Knollenorgans in three species of mormyrids are tuned to frequencies matched to the frequencies present in the species-typical electric organ discharges, suiting them for electric communication. The frequency of highest sensitivity of Knollenorgans can extend well beyond 10 kHz, far exceeding the limit for electrical tuning mechanisms estimated from mechanosensitive hair cells. The timing and probability of spiking by Knollenorgans are accurately predicted by a model composed of linear filtering followed by non-linear rectification and spike thresholding. Differential filtering by different Knollenorgans produces distinct outputs to the same input, with high-tuned receptors effectively transmitting well-timed spikes, on a microsecond time scale, in response to electrical stimuli up to 20 kHz.