Temperature response in electrosensors and thermal voltages in electrolytes.

Temperature sensation is increasingly well understood in several model organisms. One of the most sensitive organs to temperature changes is the functional electrosensor of sharks and their relatives; its extreme thermal responsiveness, in excised preparations, has not been mechanistically described. In recent years, conflicting reports have appeared concerning the properties of a hydrogel that fills the ampullae of Lorenzini. The appearance of a thermoelectric effect in the gel (or, using different methods, a reported lack thereof) suggested a link between the exquisite electrosense and the thermal response of the electroreceptors (or, alternately, denied that link). I review available electrophysiology evidence of the organ's temperature response, calculate a theoretical gel signal prediction using physical chemistry, analyze the strengths and weaknesses of the existing gel measurements, and discuss broader implications for the ampullae and temperature sensation.

From morphology to neural information: the electric sense of the skate.

Morphology typically enhances the fidelity of sensory systems. Sharks, skates, and rays have a well-developed electrosense that presents strikingly unique morphologies. Here, we model the dynamics of the peripheral electrosensory system of the skate, a dorsally flattened batoid, moving near an electric dipole source (e.g., a prey organism). We compute the coincident electric signals that develop across an array of the skate's electrosensors, using electrodynamics married to precise morphological measurements of sensor location, infrastructure, and vector projection. Our results demonstrate that skate morphology enhances electrosensory information. Not only could the skate locate prey using a simple population vector algorithm, but its morphology also specifically leads to quick shifts in firing rates that are well-suited to the demonstrated bandwidth of the electrosensory system. Finally, we propose electrophysiology trials to test the modeling scheme.

Thermoelectricity in natural and synthetic hydrogels.

We describe a technique for measuring a Seebeck effect in gels and present data for three systems. Notably distinct signals are obtained for gel originating in the electrosensitive organs of marine sharks, synthetic collagen-based gel, and as a control, seawater, the gels' solvent. Only the gel of sharks shows a reversible thermoelectric signal. The difference between gel samples and seawater simply confirms that gels suppress mass transport. The difference between synthetic gel and the gel of sharks shows that the charged polymers of the shark gel restrict mass transport much more successfully than the polymers of the collagen gel, and we submit that this sort of ion localization is key to the emergence of thermoelectricity in a gelatinous substance. We compare the properties of the natural gel to those of established thermoelectrics.

Electrical characterization of gel collected from shark electrosensors.

To investigate the physical mechanism of the electric sense, we present an initial electrical characterization of the glycoprotein gel that fills the electrosensitive organs of marine elasmobranchs (sharks, skates, and rays). We have collected samples of this gel, postmortem, from three shark species, and removed the majority of dissolved salts in one sample via dialysis. Here we present the results of dc conductivity measurements, low-frequency impedance spectroscopy, and electrophoresis. Electrophoresis shows a range of large protein-based molecules fitting the expectations of glycoproteins, but the gels of different species exhibit little similarity. The electrophoresis signature is unaffected by thermal cycling and measurement currents. The dc data were collected at various temperatures, and at various electric and magnetic fields, showing consistency with the properties of seawater. The impedance data collected from a dialyzed sample, however, show large values of static permittivity and a loss peak corresponding to an unusually long relaxation time, about 1 ms. The exact role of the gel is still unknown, but our results suggest its bulk properties are well matched to the sensing mechanism, as the minimum response time of an entire electric organ is on the order of 5 ms.

Infrastructure in the electric sense: admittance data from shark hydrogels.

Elasmobranchs (sharks, skates, and rays) possess an electrosensory system with an infrastructure of canals connecting the electrosensors to the environment. The electrosensors and canals are filled with a uniform hydrogel, but the gel's function has not yet been determined. We present electrical admittance spectra collected from the hydrogel from 0.05 to 100 kHz, covering the effective range of the electrosensors. We have taken samples of this gel, postmortem, from Triaenodon obesus and Carcharodon carcharias; for purposes of comparison, we have synthesized a series of collagen-based hydrogel samples. The shark hydrogels demonstrate suppressed admittance when compared to both seawater and collagen gels. In particular, collagen hydrogels with equivalent ion concentrations are roughly 2.5 times more polarizable than the shark samples. We conclude that the shark hydrogels strongly localize ionic species, and we discuss the implications for the related roles of the gel and the canals in the electric sense. The gel-filled canals appear better suited to fostering voltage differences along their length than to providing direct electrical contact to the seawater environment.

Modeling an electrosensory landscape: behavioral and morphological optimization in elasmobranch prey capture.

Most biological sensory systems benefit from multiple sensors. Elasmobranchs (sharks, skates and rays) possess an array of electroreceptive organs that facilitate prey location, mate location and navigation. Here, the perceived electrosensory landscape for an elasmobranch approaching prey is mathematically modeled. The voltages that develop simultaneously in dozens of separate sensing organs are calculated using electrodynamics. These voltages lead directly to firing rate modifications in the primary afferent nerves. The canals connecting the sense organs to an elasmobranch's surface exhibit great variation of location and orientation. Here, the voltages arising in the sense organs are found to depend strongly on the geometrical distribution of the corresponding canals. Two applications for the modeling technique are explored: an analysis of observed elasmobranch prey-capture behavior and an analysis of morphological optimization. For the former, results in specific predator-prey scenarios are compared with behavioral observations, supporting the approach algorithm suggested by A. Kalmijn. For the latter, electrosensory performance is contrasted for two geometrical models of multiple sense organs, a rounded head and a hammer-shaped head.