Electroreceptors with a different kind of buzz

Electric fish in Africa and South America have evolved electroreceptors and electric organs that permit them to detect and produce electric fields. They use these electric fields to communicate, navigate and find prey even as nocturnal animals inhabiting muddy rivers where visual cues are limited. The emittance of these dipole electric fields is sophisticated in nature, with different fish species capable of generating electric organ discharges (EODs) with diverse waveforms at frequencies up to 20 kHz. To detect electric fields, electric fish evolved specialized electroreceptors along their body. Given that dipole electric fields decay sharply with distance (d) as 1/d3, some of these electroreceptors must be highly sensitive, thus requiring them to be well tuned to pick up small signals from noise, as seen in other sensory modalities. However, how these electroreceptors can be tuned to detect weak electric signals oscillating at up to 20 kHz is poorly understood. This is particularly puzzling given that electrical tuning in non-mammalian auditory hair cells is limited to less than 5 kHz (Fettiplace, 2020). Among different types of electroreceptors, Knollenorgans are one type of tuberous electroreceptors that are tuned to higher frequencies (Bell, 1990; Fig. 1A). In an article in this issue of The Journal of Physiology, Raman and Hopkins (2025) stimulated Knollenorgans in mormyrid fish with sinusoidal electric fields of different frequencies and amplitudes, recording in vivo spike-like responses extracellularly. This allowed them to build tuning curves for individual Knollenorgans, in a fashion similar to constructing tuning curves for individual auditory afferent fibres with pure tone stimulation. Although these tuning curves are not very sharp with a typical quality factor QBP < 1 (Frolov & Li, 2017), their best frequencies are found to be as high as 16 kHz. Raman and Hopkins (2025) find that different fish species have different tuning curves matched to the spectrum of EODs that the fish emit, a strong indication that this electrical tuning has evolved to mediate conspecific communication. Moreover, arbitrary electrical noise stimuli applied to Knollenorgan electroreceptors evoked precisely timed spike patterns, which were well replicated by a model of linear filtering, rectification and spike thresholding. These electrically evoked spikes in Knollenorgans are reliable and precise on a time scale of less than 0.1 ms and can thus transmit signals above 10 kHz. Of course, the burning mechanistic question is how this electrical tuning arises given our current understanding of excitable membranes in analogous hair cells. Electrical tuning in non-mammalian auditory hair cells stems from Ca2+ currents closely coupled with Ca2+-dependent K+ currents. This produces membrane voltage oscillations that resonate at a particular frequency (Fig. 1B, grey), which matches the best (or characteristic) frequency in tuning curves. Results from avian, amphibian and reptilian species have suggested that resonant frequencies in hair cells cannot exceed 5 kHz, even in warm-blooded avian species, because this would require not only a very large Ca2+ current to drive steep voltage changes but also a prohibitive amount of ATP to subsequently extrude the Ca2+ ions. Moreover, the membrane time constant (τ = RmCm, where Rm is membrane resistance and Cm is membrane capacitance) would have to be in the submillisecond range, which presumably requires an extremely low Cm and Rm. However, Knollenorgan electroreceptors are densely studded with microvilli (Fig. 1A), which will produce a large surface area and thus a large Cm. Remarkably, Knollenorgans fire spikes whose waveforms are diverse among different species, as discussed by Raman and Hopkins (2025). Notably, these spikes of Knollenorgans are not blocked by tetrodotoxin, so they are presumably Ca2+ action potentials. In Fig. 1B, we propose a putative model using a combination of electrical resonance and spike generation (depicted in grey and black): strongly attenuated subthreshold membrane potential oscillations would resonate at a particular stimulus frequency, and when the threshold is crossed, a single Ca2+ action potential is fired (Rutherford & Roberts, 2009). Thus, a small signal that matches the resonant frequency of a particular electroreceptor would produce a single spike. The spike would be ultranarrow, due perhaps to a large Ca2+ current with unusually fast activation and inactivation kinetics, followed by large K+ currents during the spike downstroke. The height of the depolarizing plateau during the stimulus is Vplateau = RmITransduction, where ITransduction is the stimulus-induced current. If Rm is very small, because τ needs to be small, a large ITransduction is presumably required for Vplateau to be near the threshold. Alternatively, VThreshold may be strategically positioned closely above VRest, although it needs to be safely placed to avoid false-positive spikes generated by random membrane potential fluctuations. A relatively large ITransduction perhaps produced by even a very weak stimulus, may be mediated by a large voltage-gated Ca2+ current in the electroreceptor, which expresses multiple mitochondria just underneath the microvilli. One can also speculate that the volume outside of the cell may have a high external free Ca2+ ion concentration and a high pH (Cho & von Gersdorff, 2014), so the Ca2+ current may indeed be relatively large even for small deviations from VRest. The elegant new work of Raman and Hopkins (2025) reminds us how little we know about the cellular biophysics of the Knollenorgans. It thus challenges us to push the current conceptual boundaries, develop more realistic conductance-based models of these specialized cells, and test them with further inquiries through direct intracellular recording. If subthreshold membrane oscillations exist in Knollenorgan electroreceptors, it would be remarkable if they indeed occur in the range of 5–10 kHz. This does require a bit of ‘suspension of disbelief’, but we should keep an open mind since electrical sensing may provide an immense survival advantage for electric fish. It afforded them extraordinary diversification in species – a beautiful example of convergent evolution from a non-electrogenic common ancestor some 20 million years ago, well after Pangea began splitting Africa from South America more than 200 million years ago. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. The authors declare they have no competing interests. Both authors have read and approved the final version of this manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All persons designated as authors qualify for authorship, and all those who qualify for authorship are listed. No funding was received for this work.