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Temperature response in electrosensors and thermal voltages in electrolytes

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Abstract

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.

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References

  1. McKemy, D.D.: Temperature sensing across species. Pflugers Arch – Eur. J. Physiol. 454, 777–791 (2007)

    Article  Google Scholar 

  2. Damann, N., Voets, T., Nilius, B.: TRPs in our senses. Curr. Biol. 18, R880–R889 (2008)

    Article  Google Scholar 

  3. Kalmijn, A.: The electric sense of sharks and rays. J. Exp. Biol. 55, 371–383 (1971)

    Google Scholar 

  4. Waltman, B.: Electrical properties and fine structure of the ampullary canals of Lorenzini. Acta Physiol. Scand. Suppl. 264, 1–60 (1966)

    Google Scholar 

  5. Lu, J., Fishman, H.: Interaction of apical and basal membrane ion channels underlies electroreception in ampullary epithelia of skates. Biophys. J. 67, 1525–1533 (1994)

    Article  ADS  Google Scholar 

  6. Murray, R.W., Potts, W.: The composition of the endolymph, perilymph and other body fluids of elasmobranchs. Comp. Biochem. Physiol. 2, 65 (1961)

    Article  Google Scholar 

  7. Brown, B.R., Hutchison, J.C., Hughes, M.E., Kellogg, D.R., Murray, R.W.: Electrical characterization of gel collected from shark electrosensors. Phys. Rev. E 65, 061903 (2002)

    Article  ADS  Google Scholar 

  8. Brown, B.R., Hughes, M.E., Russo, C.: Infrastructure in the electric sense: admittance data from shark hydrogels. J. Comp. Physiol. A 191, 115–123 (2005)

    Article  Google Scholar 

  9. Eley, D.D., Spivey, D.I.: Semiconductivity in proteins and haemoglobin. Nature 188, 724–725 (1981)

    Google Scholar 

  10. Gutman, F., Lyons, L.E.: Organic Semiconductors A&B. Wiley, New York (1967)

    Google Scholar 

  11. Sand, A.: The function of the ampullae of Lorenzini, with some observations on the effect of temperature on sensory rhythms. Proc. R. Soc. Lond. B 125, 524 (1938)

    Article  ADS  Google Scholar 

  12. Murray, R.W.: The response of the ampullae of lorenzini to combined stimulation by temperature change and weak direct currents. J. Physiol. 145, 1–13 (1959)

    Google Scholar 

  13. Murray, R.W.: The response of the ampullae of lorenzini of elasmobranchs to mechanical stimulation. J. Exp. Biol. 37, 417–424 (1960)

    Google Scholar 

  14. Murray, R.W.: The response of the ampullae of lorenzini of elasmobranchs to electrical stimulation. J. Exp. Biol. 39, 119–128 (1962)

    Google Scholar 

  15. Hensel, H.: Effect of temporal and spatial temperature gradients on the ampullae of lorenzini. Pflugers Arch. 347, 89–100 (1974)

    Article  Google Scholar 

  16. Nier, K., Hensel, H., Bromm, B.: Differential thermosensitivity and electric prepolarization of the ampullae of lorenzini. Pflugers Arch. 363, 181–185 (1976)

    Article  Google Scholar 

  17. Broun, G.R., Govardovskii, V.I.: Investigation of the mechanism of temperature sensitivity of the electroreceptors of ampullae of lorenzini. Neurophysiology 12, 54–59 (1980)

    Article  Google Scholar 

  18. Broun, G.R., Govardovskii, V.I.: Changes in transepithelial potential and spike responses of ampullae of lorenzini of the skate to temperature stimulation. Neurophysiology 14, 7–13 (1982)

    Article  Google Scholar 

  19. Akoev, G.N., Volpe, N.O., Zhadan, G.G.: Analysis of effects of chemical and thermal stimuli on the ampullae of Lorenzini of the skates. Comp. Biochem. Physiol. A 65, 193 (1980)

    Article  Google Scholar 

  20. Lowenstein, W.R., Ishiko, N.: Sodium chloride sensitivity and electrochemical effects in a Lorenzinian ampulla. Nature 194, 292–294 (1962)

    Article  ADS  Google Scholar 

  21. Wissing, H., Braun, H.A., Schafer, K.: Dynamic response characteristics of the ampullae of Lorenzini to thermal and electrical stimuli. Progr. Brain Res. 74, 99–110 (1988)

    Article  Google Scholar 

  22. Braun, H.A., Wissing, H., Schafer, K., Hirsch, M.C.: Oscillation and noise determine signal transduction in shark multimodal sensory cells. Nature 367, 270–273 (1994)

    Article  ADS  Google Scholar 

  23. Brown, B.R.: Sensing temperature without ion channels. Nature 421, 495 (2003)

    Article  ADS  Google Scholar 

  24. Nolas, G.S., Sharp, J., Goldsmid, H.J.: Thermoelectrics. Springer, New York (2001)

    MATH  Google Scholar 

  25. Brown, B.R., Hughes, M.E., Russo, C.: Thermoelectricity in natural and synthetic hydrogels. Phys. Rev. E 70, 031917 (2004)

    Article  ADS  Google Scholar 

  26. Agar, J.N., Turner, J.C.R.: Thermal diffusion in solutions of electrolytes. Proc. R. Soc. Lond. A Math. Phys. Sci. 255, 307–330 (1960)

    Article  ADS  Google Scholar 

  27. Leaist, D.G.: Soret coefficients of mixed electrolytes. J. Sol. Chem. 19, 1–10 (1990)

    Article  Google Scholar 

  28. Wiegand, S.: Thermal diffusion in liquid mixtures and polymer solutions. J. Phys: Condens. Matter 16, R357–R379 (2004)

    Article  ADS  Google Scholar 

  29. Artola, P., Rousseau, B.: Microscopic interpretation of a pure chemical contribution to the Soret effect. Phys. Rev. Lett. 98, 125901 (2007)

    Article  ADS  Google Scholar 

  30. Leaist, D.G., Hui, L.: Conductometric determination of Soret coefficients of a ternary mixed electrolyte. J. Phys. Chem. 94, 447–451 (1990)

    Article  Google Scholar 

  31. Piazza, R., Guarino, A.: Soret effect in interacting micellar solutions. Phys. Rev. Lett. 88, 208302 (2002)

    Article  ADS  Google Scholar 

  32. Hyk, W., Ciszkowska, M.: Studies of transport phenomena and electrostatic interactions in polyacrylate gels. J. Phys. Chem. B 103, 6466–6474 (1999)

    Article  Google Scholar 

  33. Grosso, G., Parravicini, G.P.: Solid State Physics, pp. 414–424. Academic Press, London (2000)

    Google Scholar 

  34. Kasap, S.O.: Principles of Electronic Materials and Devices, pp. 278-284. McGraw Hill, San Francisco (2000)

    Google Scholar 

  35. Brown, B.R.: Sensing temperature without ion channels: corrigendum. Nature 454, 246 (2008)

    Article  ADS  Google Scholar 

  36. Fields, R.D., Fields, K.D., Fields, M.C.: Semiconductor gel in shark sense organs? Neurosci. Lett. 426, 166–170 (2007)

    Article  Google Scholar 

  37. Milazzo, G., Caroli, S.: Tables of Standard Electrochemical Potentials. John Wiley and Sons, New York (1978)

    Google Scholar 

  38. Sanford, T.B., Carlson, J.A., Dunlap, J.H., Prater, M.D., Lien, R.-C.: An electromagnetic vorticity and velocity sensor for observing finescale kinetic fluctuations in the ocean. J. Atmos. Ocean. Technol. 16, 1647–1667 (1999)

    Article  ADS  Google Scholar 

  39. Sanford, T.B.: Doctoral Thesis, Massachusetts Institute of Technology, Boston (1967)

  40. Braun, H.A., Schafer, K., Wissing, H.: Theories and models of temperature transduction. In: Bligh, J., Voigt, K. (eds.) Thermoreception and Temperature Regulation, pp. 19–29. Springer-Verlag, Berlin (1990)

    Google Scholar 

  41. Akoev, G.N.: Temperature sensitivity of the ampullea of lorenzini of elasmobranchs. In: Bligh, J., Voigt, K. (eds.) Thermoreception and Temperature Regulation, pp. 44–52. Springer-Verlag, Berlin (1990)

    Google Scholar 

  42. Clapham, D.E.: TRP Channels as cellular sensors. Nature 426, 517–524 (2003)

    Article  ADS  Google Scholar 

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Acknowledgements

The author thanks: T.B. Sanford for detailed discussions of the Soret effect and metal electrodes in seawater; T. Tricas, F. Moss, and L.A. Wilkens, for conversations relating to the ampullae of Lorenzini; J. Curtis, C. Hutchison, and L. Margerum for discussions of electrode chemistry; and M. Hughes, C. Russo, A. Abramson and J. Dyck for discussion of experimental techniques. The author declares no conflict of interest.

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Brown, B.R. Temperature response in electrosensors and thermal voltages in electrolytes. J Biol Phys 36, 121–134 (2010). https://doi.org/10.1007/s10867-009-9174-8

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