Ancient cartilaginous vertebrates, such as sharks, skates and rays, possess specialized electrosensory organs that detect weak electric fields and relay this information to the central nervous system1,2,3,4. Sharks exploit this sensory modality for predation, whereas skates may also use it to detect signals from conspecifics5. Here we analyse shark and skate electrosensory cells to determine whether discrete physiological properties could contribute to behaviourally relevant sensory tuning. We show that sharks and skates use a similar low threshold voltage-gated calcium channel to initiate cellular activity but use distinct potassium channels to modulate this activity. Electrosensory cells from sharks express specially adapted voltage-gated potassium channels that support large, repetitive membrane voltage spikes capable of driving near-maximal vesicular release from elaborate ribbon synapses. By contrast, skates use a calcium-activated potassium channel to produce small, tunable membrane voltage oscillations that elicit stimulus-dependent vesicular release. We propose that these sensory adaptations support amplified indiscriminate signal detection in sharks compared with selective frequency detection in skates, potentially reflecting the electroreceptive requirements of these elasmobranch species. Our findings demonstrate how sensory systems adapt to suit the lifestyle or environmental niche of an animal through discrete molecular and biophysical modifications.
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We thank S. Bennett from the Marine Biological Laboratory for supplying animals, J. Wong from the Gladstone/University of California, San Francisco (UCSF) transmission electron microscopy core for performing electron microscopy, A. Zimmerman for help with capacitance measurements, discussion and reading of the manuscript, R. Edwards for discussion, and R. Nicoll for input on the manuscript. This work was supported by a National Institutes of Health (NIH) Institutional Research Service Award to the UCSF CVRI (T32HL007731 to N.W.B.), a Howard Hughes Medical Institute Fellowship of the Life Sciences Research Foundation (N.W.B.), a Simons Foundation Postdoctoral Fellowship to the Jane Coffin Childs Memorial Fund (D.B.L.) and grants from the NIH (1K99DC016658 to D.B.L., K99DK115879 to N.W.B., and NS055299 and NS105038 to D.J.).
Nature thanks B. Carlson, C. Lingle, H. von Gersdorff and the other anonymous reviewer(s) for their contribution to the peer review of this work.