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Molecular tuning of electroreception in sharks and skates

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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 system1–4. Sharks exploit this… Click to show full abstract

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 system1–4. 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.Shark and skate electrosensory cells use specific potassium channels to support either indiscriminate detection of electrical stimuli or selective frequency tuning, respectively, demonstrating adaptation of sensory systems through discrete molecular modifications.

Keywords: voltage; potassium channels; molecular tuning; electrosensory cells; sharks skates

Journal Title: Nature
Year Published: 2018

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