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Sensory coding in oscillatory electroreceptors of paddlefish

Source: Chaos 21, 047505 (2012); http://dx.doi.org/10.1063/1.3669494

Published 29 December 2011

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ISSN:
1553-9628 (online)
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AIP is a member of CrossRef AIP
Alexander B. Neiman1 and David F. Russell2
1Neuroscience Program, Department of Physics and Astronomy, Ohio University, Athens, Ohio 45701, USA
2Neuroscience Program, Department of Biological Sciences, Ohio University, Athens, Ohio 45701, USA
Coherence and information theoretic analyses were applied to quantitate the response properties and the encoding of time-varying stimuli in paddlefish electroreceptors (ERs), studied in vivo. External electrical stimuli were Gaussian noise waveforms of varied frequency band and strength, including naturalistic waveforms derived from zooplankton prey. Our coherence analyses elucidated the role of internal oscillations and transduction processes in shaping the 0.5–20 Hz best frequency tuning of these electroreceptors, to match the electrical signals emitted by zooplankton prey. Stimulus-response coherence fell off above approximately 20 Hz, apparently due to intrinsic limits of transduction, but was detectable up to 40–50 Hz. Aligned with this upper fall off was a narrow band of intense internal noise at ~25 Hz, due to prominent membrane potential oscillations in cells of sensory epithelia, which caused a narrow deadband of external insensitivity. Using coherence analysis, we showed that more than 76% of naturalistic stimuli of weak strength, ~1 µV/cm, was linearly encoded into an afferent spike train, which transmitted information at a rate of ~30 bits/s. Stimulus transfer to afferent spike timing became essentially nonlinear as the stimulus strength was increased to induce bursting firing. Strong stimuli, as from nearby zooplankton prey, acted to synchronize the bursting responses of afferents, including across populations of electroreceptors, providing a plausible mechanism for reliable information transfer to higher-order neurons through noisy synapses. ©2011 American Institute of Physics
History: Received 12 September 2011; accepted 22 November 2011; published 29 December 2011
Digital Object Identifier: http://dx.doi.org/10.1063/1.3669494

REFERENCES (78)

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  1. Bahar, S., Kantelhardt, J. W., Neiman, A., Rego, A. H. H., , Russell, D. F., Wilkens, L., Bunde, A., and Moss, F., “Long-range temporal anti-correlations in paddlefish electroreceptors,” Europhys. Lett. 56(3), 454–460 (2001).
  2. Barnett, T. P., Johnson, L. C., Naitoh, P., Hicks, N., and Nute, C., “Bispectrum analysis of electroencephalogram signals during waking and sleeping,” Science 172, 401–402 (1971).
  3. Benda, J., Longtin, A., and Maler, L., “Spike-frequency adaptation separates transient communication signals from background oscillations,” J. Neurosci. 25(9), 2312–2321 (2005).
  4. Bendat, J. S. and Piersol, A. G., Random Data Analysis and Measurement Procedures (Wiley, New York, 2000).
  5. Bennett, M. V. and Obara, S., “Ionic mechanisms and pharmacology of electroreceptors,” in Electroreception, edited by T. H. Bullock and W. Heiligenberg (Wiley, New York, 1986), pp. 157–181.
  6. Bialek, W., Rieke, F., de Ruyter van Steveninck, R. R., and Warland, D., “Reading a neural code,” Science 252(5014), 1854–1857 (1991).
  7. Braun, H. A., Schafer, K., Voigt, K., Peters, R., Bretschneider, F., Pei, X., Wilkens, L., and Moss, F., “Low-dimensional dynamics in sensory biology. 1: Thermally sensitive electroreceptors of the catfish,” J. Comput. Neurosci. 4(4), 335–347 (1997).
  8. Braun, H. A., Wissing, H., Schafer, K., and Hirsch, M. C., “Oscillation and noise determine signal transduction in shark multimodal sensory cells,” Nature 367(6460), 270–273 (1994).
  9. Bryant, H. L. and Segundo, J. P., “Spike initiation by transmembrane current: A white-noise analysis,” J. Physiol. 260(2), 279–314 (1976).
  10. Bullock, T. H., “Electroreception,” Ann. Rev. Neurosci. 5, 121–170 (1982).
  11. Bullock, T. H., Achimowicz, J. Z., Duckrow, R. B., Spencer, S. S., and Iragui-Madoz, V. J., “Bicoherence of intracranial EEG in sleep, wakefulness and seizures,” Electroencephalogr. Clin. Neurophysiol. 103(6), 661–678 (1997).
  12. Bullock, T. H., Bodznick, D. A., and Northcutt, R. G., “The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sense modality,” Brain Res. 287, 25–46 (1983).
  13. Catacuzzeno, L., Fioretti, B., Perin, P., and Franciolini, F., “Spontaneous low-frequency voltage oscillations in frog saccular hair cells,” J. Physiol. 561, 685–701 (2004).
  14. Chacron, M. J., “Nonlinear information processing in a model sensory system,” J. Neurophysiol. 95(5), 2933–2946 (2006).
  15. Chacron, M. J., Longtin, A., and Maler, L., “Negative interspike interval correlations increase the neuronal capacity for encoding time-dependent stimuli,” J. Neurosci. 21(14), 5328–5343 (2001).
  16. Chacron, M. J., Longtin, A., and Maler, L., “To burst or not to burst?,” J. Comput. Neurosci. 17(2), 127–136 (2004).
  17. Chacron, M. J., Maler, L., and Bastian, J., “Electroreceptor neuron dynamics shape information transmission,” Nature Neurosci. 8(5), 673–678 (2005).
  18. Chagnaud, B. P., Wilkens, L. A., and Hofmann, M. H., “Receptive field organization of electrosensory neurons in the paddlefish (Polyodon spathula),” J. Physiol. Paris 102(4–6), 246–255 (2008).
  19. Chagnaud, B. P., Wilkens, L. A., and Hofmann, M. H., “Response properties of electrosensory neurons in the lateral mesencephalic nucleus of the paddlefish,” J. Comput. Physiol. A 194(3), 209–220 (2008).
  20. Clusin, W. T. and Bennett, M. V. L., “The ionic basis of oscillatory responses of skate electroreceptors,” J. Gen. Physiol. 73(6), 703–723 (1979).
  21. Clusin, W. T. and Bennett, M. V. L., “The oscillatory responses of skate electroreceptors to small voltage stimuli,” J. Gen. Physiol. 73, 685–702 (1979).
  22. Eguiluz, V. M., Ospeck, M., Choe, Y., Hudspeth, A. J., and Magnasco, M. O., “Essential nonlinearities in hearing,” Phys. Rev. Lett. 84(22), 5232–5235 (2000).
  23. Engel, T. A., Helbig, B., Russell, D. F., Schimansky-Geier, L., and Neiman, A. B., “Coherent stochastic oscillations enhance signal detection in spiking neurons,” Phys. Rev. E 80, 021919 (2009).
  24. Engelmann, J., Gertz, S., Goulet, J., Schuh, A., and von der Emde, G., “Coding of stimuli by ampullary afferents in Gnathonemus petersii,” J. Neurophysiol. 104(4), 1955–1968 (2010).
  25. Ermentrout, G. B., Galan, R. F., and Urban, N. N., “Relating neural dynamics to neural coding,” Phys. Rev. Lett. 99(24), 248103 (2007).
  26. Freund, J. A., Schimansky-Geier, L., Beisner, B., Neiman, A., and Russell, D. F., Yakusheva, T., and Moss, F., “Behavioral stochastic resonance: how the noise from a Daphnia swarm enhances individual prey capture by juvenile paddlefish,” J. Theor. Biol. 214(1), 71–83 (2002).
  27. Fuwape, I. and Neiman, A. B., “Spontaneous firing statistics and information transfer in electroreceptors of paddlefish,” Phys. Rev. E 78, 051922 (2008).
  28. Gabbiani, F., “Coding of time-varying signals in spike trains of linear and half-wave rectifying neurons,” Network Comput. Neural Syst. 7(1), 61–85 (1996).
  29. Gabbiani, F. and Koch, C., “Principles of spike train analysis,” in Methods in Neuronal Modeling. From Ions to Networks, edited by C. Koch, and I. Segev (MIT Press, Cambridge, Mass, 1998), pp. 313–360.
  30. Gabbiani, F. and Metzner, W., “Encoding and processing of sensory information in neuronal spike trains,” J. Exp. Biol. 202, 1267–1279 (1999).
  31. Goldberg, J. M., “Afferent diversity and the organization of central vestibular pathways,” Exp. Brain Res. 130(3), 277–297 (2000).
  32. Goldobin, D. S. and Pikovsky, A., “Synchronization and desynchronization of self-sustained oscillators by common noise,” Phys. Rev. E 71, 045201 (2005).
  33. Hanggi, P. and Thomas, H., “Stochastic-Processes - Time Evolution, Symmetries and Linear Response,” Phys. Rep.-Rev. Sec. Phys. Lett. 88(4), 207–319 (1982).
  34. Hofmann, M. H., Chagnaud, B., and Wilkens, L. A., “Response properties of electrosensory afferent fibers and secondary brain stem neurons in the paddlefish,” J. Exp. Biol. 208, 4213–4222 (2005).
  35. Hofmann, M. H., Jung, S. N., Siebenaller, U., Preissner, M., Chagnaud, B. P., and Wilkens, L. A., “Response properties of electrosensory units in the midbrain tectum of the paddlefish (Polyodon spathula Walbaum),” J. Exp. Biol. 211, 773–779 (2008).
  36. Hofmann, M. H. and Wilkens, L. A., “Temporal analysis of moving DC electric fields in aquatic media,” Phys. Biol. 2(1–2), 23–28 (2005).
  37. Horsthemke, W. and Lefever, R., Noise-Induced Transitions. Theory and Applications in Physics, Chemistry, and Biology (Springer, Berlin, 1984).
  38. Hudspeth, A. J., Julicher, F., and Martin, P., “A critique of the critical cochlea: Hopf–a bifurcation–is better than none,” J. Neurophysiol. 104(3), 1219–1229 (2010).
  39. Johnson, L. C., Nute, C., Austin, M. T., and Lubin, A., “Spectral analysis of the EEG during waking and sleeping,” Electroencephalogr. Clin. Neurophysiol. 23(1), 80 (1967).
  40. Lesica, N. A. and Stanley, G. B., “Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus,” J. Neurosci. 24(47), 10731–10740 (2004).
  41. Lu, J. and Fishman, H. M., “Localization and function of the electrical oscillation in electroreceptive ampullary epithelium from skates,” Biophys. J. 69(6), 2458–2466 (1995).
  42. Mainen, Z. F. and Sejnowski, T. J., “Reliability of spike timing in neocortical neurons,” Science 268(5216), 1503–1506 (1995).
  43. Manley, G. A., “Preferred intervals in the spontaneous activity of primary auditory neurons,” Naturwiss. 66(11), 582–584 (1979).
  44. Martin, P., Bozovic, D., Choe, Y., and Hudspeth, A. J., “Spontaneous oscillation by hair bundles of the bullfrog's sacculus,” J. Neurosci. 23(11), 4533–4548 (2003).
  45. Massot, C., Chacron, M. J., and Cullen, K. E., “Information transmission and detection thresholds in the vestibular nuclei: single neurons vs. population encoding,” J. Neurophysiol. 105(4), 1798–1814 (2011).
  46. Metzner, W., Koch, C., Wessel, R., and Gabbiani, F., “Feature extraction by burst-like spike patterns in multiple sensory maps,” J. Neurosci. 18(6), 2283–2300 (1998).
  47. Neiman, A. and Russell, D. F., “Stochastic biperiodic oscillations in the electroreceptors of paddlefish,” Phys. Rev. Lett. 86(15), 3443–3446 (2001).
  48. Neiman, A. B. and Russell, D. F., “Synchronization of noise-induced bursts in noncoupled sensory neurons,” Phys. Rev. Lett. 88(13), 138103 (2002).
  49. Neiman, A. B. and Russell, D. F., “Two distinct types of noisy oscillators in electroreceptors of paddlefish,” J. Neurophysiol. 92(1), 492–509 (2004).
  50. Neiman, A. B. and Russell, D. F., “Models of stochastic biperiodic oscillations and extended serial correlations in electroreceptors of paddlefish,” Phys. Rev. E 71, 061915 (2005).
  51. Neiman, A. B., Yakusheva, T. A., and Russell, D. F., “Noise-induced transition to bursting in responses of paddlefish electroreceptor afferents,” J. Neurophysiol. 98(5), 2795–2806 (2007).
  52. Neiman, A., Schimansky-Geier, L., and Moss, F., “Linear response theory applied to stochastic resonance in models of ensembles of oscillators,” Phys. Rev. E 56(1), R9 (1997).
  53. Nguyen, H. and Neiman, A. B., “Spontaneous dynamics and response properties of a Hodgkin-Huxley-type neuron model driven by harmonic synaptic noise,” Eur. Phys. J. Spec. Top. 187(1), 179–187 (2010).
  54. Nikias, C. L. and Petropulu, A. P., Higher-Order Spectral Analysis. A Nonlinear Signal Processing Framework (Prentice Hall, Englewood Cliffs, NJ, 1993).
  55. Pakdaman, K. and Mestivier, D., “External noise synchronizes forced oscillators,” Phys. Rev. E 64, 030901 (2001).
  56. Passaglia, C. L. and Troy, J. B., “Information transmission rates of cat retinal ganglion cells,” J Neurophysiol. 91(3), 1217–1229 (2004).
  57. Pei, X., Russell, D. F., Wilkens, L. A., and Moss, F., “Dynamics of the electroreceptors in the paddlefish, Polyodon spathula,” in Computational Neuroscience: Trends in Research 1998, edited by J. Bower (Plenum, New York, 1998), pp. 245–249.
  58. Ratnam, R. and Nelson, M. E., “Nonrenewal statistics of electrosensory afferent spike trains: implications for the detection of weak sensory signals,” J. Neurosci. 20(17), 6672–6683 (2000).
  59. Reinagel, P., Godwin, D., Sherman, S. M., and Koch, C., “Encoding of visual information by LGN bursts,” J. Neurophysiol. 81(5), 2558–2569 (1999).
  60. Rieke, F., Bodnar, D. A., and Bialek, W., “Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents,” Proc. Biol. Sci. 262(1365), 259–265 (1995).
  61. Roddey, J. C., Girish, B., and Miller, J. P., “Assessing the performance of neural encoding models in the presence of noise,” J. Comput. Neurosci. 8(2), 95–112 (2000).
  62. Russell, D. F., Tucker, A., Wettering, B. A., Neiman, A. B., Wilkens, L. A., and Moss, F., “Noise effects on the electrosense-mediated feeding behavior of small paddlefish,” Fluctuation Noise Lett. 1, L71–L86 (2001).
  63. Russell, D. F., Wilkens, L. A., and Moss, F., “Use of behavioural stochastic resonance by paddle fish for feeding,” Nature 402(6759), 291–294 (1999).
  64. Russell, D. F., Yakusheva, T., Neiman, A. B., and Moss, F., “The receptive field of an electroreceptor afferent in paddlefish corresponds to a single cluster of canals,” (unpublished).
  65. Rutherford, M. A. and Roberts, W. M., “Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus,” J. Neurosci. 29(32), 10025–10037 (2009).
  66. Sadeghi, S. G., Chacron, M. J., Taylor, M. C., and Cullen, K. E., “Neural variability, detection thresholds, and information transmission in the vestibular system,” J. Neurosci. 27(4), 771–781 (2007).
  67. Schafer, K., Braun, H. A., Peters, R. C., and Bretschneider F., “Periodic firing pattern in afferent discharges from electroreceptor organs of catfish,” Pfluegers Arch. 429(3), 378–385 (1995).
  68. Schanze, T. and Eckhorn, R., “Phase correlation among rhythms present at different frequencies: spectral methods, application to microelectrode recordings from visual cortex and functional implications,” Int. J. Psychophysiol. 26(1–3), 171–189 (1997).
  69. Schleimer, J. H. and Stemmler, M., “Coding of information in limit cycle oscillators,” Phys. Rev. Lett. 103(24), 248105 (2009).
  70. Strong, S. P., Koberle, R., de Ruyter van Steveninck, R., and Bialek, W., “Entropy and information in neural spike trains,” Phys. Rev. Lett. 80(1), 197 (1998).
  71. Struik, M., Bretschneider, F., and Peters, R., “Spontaneous nerve a ctivity and sensitivity in catfish ampullary electroreceptor organs after tetanus toxin application,” Pflüegers Arch. 443(5–6), 903–907 (2006).
  72. Swami A, Mendel, J. M., and Nikias, C. L., HOSAHigher Order Spectral Analysis Toolbox, http://www.mathworks.com/matlabcentral/fileexchange/loadFile.do?objectId=3013&objectType=FILE (2003).
  73. Tass, P., “Stimulus-locked transient phase dynamics, synchronization and desynchronization of two oscillators,” Europhys. Lett. 59(2), 199–205 (2002).
  74. Tricas, T. C. and New, J. G., “Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields,” J. Comput. Physiol. A 182(1), 89 (1998).
  75. Wessel, R., Koch, C., and Gabbiani, F., “Coding of time-varying electric field amplitude modulations in a wave-type electric fish,” J. Neurophysiol. 75(6), 2280–2293 (1996).
  76. Wilkens, L. A., Russell, D. F., Pei, X., and Gurgens, C., “The paddlefish rostrum functions as an electrosensory antenna in plankton feeding,” Proc. R. Soc., London, Ser B 264(1389), 1723–1729 (1997).
  77. Wilkens, L. A., Wettering, B. A., Wagner, E., Wojtenek, W., and Russell, D. F., “Prey detection in selective plankton feeding by the paddlefish: is the electric sense sufficient?,” J. Exp. Biol. 204, 1381–1389 (2001).
  78. Wojtenek, W., Pei, X., and Wilkens, L. A., “Paddlefish strike at artificial dipoles simulating the weak electric fields of planktonic prey,” J. Exp. Biol. 204, 1391–1399 (2001).

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