Molecular tuning of electroreception in sharks and skates

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 analyze shark and skate electrosensory cells to ask if discrete physiological properties could contribute to behaviorally-relevant sensory tuning. We show that sharks and skates use a similar low threshold voltage-gated calcium channel to initiate cellular activity but employ 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. In 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 versus selective frequency detection in skates, potentially reflecting the electroreceptive requirements of these elasmobranch species. Our findings demonstrate how sensory systems adapt to suit an animal’s lifestyle or environmental niche through discrete molecular and biophysical modifications.

Cellular and molecular mechanisms of photoreceptor tuning for prey capture in larval zebrafish

“…7a,b). Different ribbon designs are used extensively in sensory systems to support both transient and continuous high-throughput vesicle release with a broad spectrum of properties (Baden et al, 2013a;Bellono et al, 2018;Heidelberger et al, 2005;Lagnado and Schmitz, 2015;Wichmann and Moser, 2015). Accordingly, we wondered if UVcones may also differentially tune their synaptic release machinery to further enhance the differences already present at the level of calcium and thus amplify eye-position specific signalling.…”

“…In vision, photoreceptors drive the retinal network through continuous modulations in synaptic release (Baden et al, 2013a;Heidelberger et al, 2005;Lagnado and Schmitz, 2015;Moser et al, 2019;Regus-Leidig and Brandstätter, 2012;Thoreson, 2007). However, how changes in incoming photon flux lead to changes in the rate of vesicle fusion at the synapse varies dramatically between photoreceptor designs (Bellono et al, 2018;Sterling and Matthews, 2005;Thoreson, 2007). For example, in the vertebrate retina, the slow rod-photoreceptors typically have large outer segments and high-gain intracellular signalling cascades to deliver singlephoton sensitivity critical for vision at low light (Field et al, 2005;Lamb, 2016;Yau and Hardie, 2009).…”

Electroreception in marine fishes: chondrichthyans

“…Considering the research of Bellono et al . (, ), it is likely that these hormone‐induced seasonal changes in electroreceptor sensitivity are due, in part, to altered gene expression patterns and molecular modifications to the ion channels within the receptor cells.…”

“…If so, then species‐specific tuning could be achieved, in part, by molecular adaptations to the ion channels within the membranes of the electroreceptor cells similar to those described in the L. erinacea by Bellono et al . (, ). The basal position of skates within Chondrichthyan phylogeny would enable researchers to study the evolution and molecular basis, of electrosensory mediated communication and behaviour in vertebrates.…”

“…Males would probably incur substantial metabolic costs during the mating season as their electrosensory system is presumably less adept at finding prey items. Considering the research of Bellono et al (2017Bellono et al ( , 2018, it is likely that these hormone-induced seasonal changes in electroreceptor sensitivity are due, in part, to altered gene expression patterns and molecular modifications to the ion channels within the receptor cells.…”