Extracellular signal fluctuations in shark electrosensors

We examine the roll of an extracellular gel in the functioning of the electrosensors of elasmobranchs (sharks, skates, and rays). Here we focus on physical characteristics of the gel and their mechanistic relevance to the observed functioning of the electrosensors. The electrosensitive organs show sharp transient responses to both tiny electrical fluctuations and temperature fluctuations. We present a thermoelectric characterization of the gel. The data suggest a gel-mediated mechanism of transducing thermal fluctuations to electrical fluctuations in the electrosensor, independent of the sensing cells. We also present frequency-dependent electrical properties of the gel collected using electrical impedance spectroscopy. From these measurements we try to extract characteristic relaxation times. We analyze these results within the context of the electrosensors’ bandwidth, as demonstrated in previous behavioral experiments.

[1]  J. Sisneros,et al.  Electrosensory optimization to conspecific phasic signals for mating , 1995, Neuroscience Letters.

[2]  A. Oberst.  Cells, Gels, and the Engines of Life , 2003, Cell Death and Differentiation.

[3]  H. M. Fishman,et al.  Interaction of apical and basal membrane ion channels underlies electroreception in ampullary epithelia of skates. , 1994, Biophysical journal.

[4]  Ad. J. Kalmijn,et al.  Electro-Orientation in Sharks and Rays: Theory and Experimental Evidence , 1973 .

[5]  J Doyle,et al.  The 'Lorenzan sulphates'. A new group of vertebrate mucopolysaccharides. , 1967, The Biochemical journal.

[6]  K. Schäfer,et al.  Oscillation and noise determine signal transduction in shark multimodal sensory cells , 1994, Nature.

[7]  G. Zhadan,et al.  Analysis of effects of chemical and thermal stimuli on the ampullae of Lorenzini of the skates , 1980 .

[8]  C. Mccombie,et al.  Solid-State Physics , 1965, Nature.

[9]  P. Kounavis,et al.  Thermopower, conductivity and the Hall effect in V2O5 gels , 1988 .

[10]  Brandon R Brown,et al.  Modeling an electrosensory landscape: behavioral and morphological optimization in elasmobranch prey capture. , 2002, The Journal of experimental biology.

[11]  A. Jonscher.  Dielectric relaxation in solids , 1983 .

[12]  Arthur J. Epstein,et al.  Charge transport of the mesoscopic metallic state in partially crystalline polyanilines , 1998 .

[13]  R. W. Murray,et al.  The composition of the endolymph, perilymph , 1961 .

[14]  John C. Montgomery.  Frequency response characteristics of primary and secondary neurons in the electrosensory system of the thornback ray , 1984 .

[15]  A. Klimley,et al.  Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field , 1993 .

[16]  D. Clapham.  Hot and Cold TRP Ion Channels , 2002, Science.

[17]  A. Shakouri,et al.  Thermoelectric power factor for electrically conductive polymers , 1999, Eighteenth International Conference on Thermoelectrics. Proceedings, ICT'99 (Cat. No.99TH8407).

[18]  A. Kalmijn,et al.  Electric and magnetic field detection in elasmobranch fishes. , 1982, Science.

[19]  B. Scaife,et al.  Principles of dielectrics , 1989 .

[20]  George S. Nolas,et al.  Thermoelectrics: Basic Principles and New Materials Developments , 2001 .

[21]  A. Sand,et al.  The function of the ampullae of Lorenzini, with some observations on the effect of temperature on sensory rhythms , 1938 .

[22]  Mary E. Hughes,et al.  Electrical characterization of gel collected from shark electrosensors. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[23]  D. Kell,et al.  The passive electrical properties of biological systems: their significance in physiology, biophysics and biotechnology. , 1987, Physics in medicine and biology.

[24]  Dynamic response characteristics of the ampullae of Lorenzini to thermal and electrical stimuli. , 1988, Progress in brain research.

[25]  B Waltman,et al.  Electrical properties and fine structure of the ampullary canals of Lorenzini. , 1966, Acta physiologica Scandinavica. Supplementum.

[26]  R. Pethig,et al.  Water structure-dependent charge transport in proteins. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[27]  H. A. Braun,et al.  Theories and Models of Temperature Transduction , 1990 .

[28]  H. L. Pratt,et al.  Temperature and Activities of a White Shark, Carcharodon carcharias , 1982 .

[29]  D. Sims,et al.  Selective foraging behaviour of basking sharks on zooplankton in a small-scale front , 1998, Nature.

[30]  William M. Balch,et al.  A line in the sea , 1994, Nature.

[31]  D. Beebe,et al.  Lentropin: a factor in vitreous humor which promotes lens fiber cell differentiation. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[32]  R J Sheppard,et al.  Dielectric behaviour of biological molecules in solution , 1978 .