Sensory receptor diversity establishes a peripheral population code for stimulus duration at low intensities

Journal of Experimental Biology

Volumn 215, Issue 15, 2012, Pages 2586-2600

  Lyons Warren, Ariel M ^a   Hollmann, Michael ^a   Carlson, Bruce A ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

Duration tuning; Electroreception; Mormyrid; Peripheral filtering; Sensory processing; Temporal coding; Weakly electric fish

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; ELECTRIC FISH; ELECTRIC ORGAN; EVOKED RESPONSE; FEMALE; MALE; MESENCEPHALON; PHYSIOLOGY; REACTION TIME; SENSORY RECEPTOR; STIMULATION; TIME;

ANIMALS; BEHAVIOR, ANIMAL; ELECTRIC FISH; ELECTRIC ORGAN; EVOKED POTENTIALS; FEMALE; MALE; MESENCEPHALON; MODELS, BIOLOGICAL; PHYSICAL STIMULATION; REACTION TIME; SENSORY RECEPTOR CELLS; TIME FACTORS;

MORMYRIDAE; PISCES;

EID: 84863966989     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.064733     Document Type: Article

References (75)

1. Amagai, S. (1998). Time coding in the midbrain of mormyrid electric fish. II. Stimulus selectivity in the nucleus exterolateralis pars posterior. J. Comp. Physiol. A 182, 131-143.
2. Amagai, S., Friedman, M. A. and Hopkins, C. D. (1998). Time coding in the midbrain of mormyrid electric fish. I. Physiology and anatomy of cells in the nucleus exterolateralis pars anterior. J. Comp. Physiol. A 182, 115-130.
3. Arnegard, M. E. and Hopkins, C. D. (2003). Electric signal variation among seven blunt-snouted Brienomyrus species (Teleostei: Mormyridae) from a riverine species flock in Gabon, Central Africa. Environ. Biol. Fishes 67, 321-339.
4. Arnegard, M. E., Bogdanowicz, S. M. and Hopkins, C. D. (2005). Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatry. Evolution 59, 324-343.
5. Arnegard, M. E., Jackson, B. S. and Hopkins, C. D. (2006). Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes. J. Exp. Biol. 209, 2182-2198.
6. Arnegard, M. E., McIntyre, P. B., Harmon, L. J., Zelditch, M. L., Crampton, W. G., Davis, J. K., Sullivan, J. P., Lavoue, S. and Hopkins, C. D. (2010). Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am. Nat. 176, 335-356.
7. Aubie, B., Becker, S. and Faure, P. A. (2009). Computational models of millisecond level duration tuning in neural circuits. J. Neurosci. 29, 9255-9270.
8. Barlow, H. B. (1972). Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1, 371-394.
9. Barlow, H. B. (2001). Redundancy reduction revisited. Network 12, 241-253.
10. Bass, A. H. and Hopkins, C. D. (1984). Shifts in frequency tuning of electroreceptors in androgen-treated mormyrid fish. J. Comp. Physiol. A 155, 713-724.
11. Bell, C. C. (1990). Mormyromast electroreceptor organs and their afferent fibers in mormyrid fish. III. Physiological differences between two morphological types of fibers. J. Neurophysiol. 63, 319-332.
12. Bell, C. C. and Grant, K. (1989). Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J. Neurosci. 9, 1029-1044.
13. Bell, C. C. and Szabo, T. (1986). Electroreception in mormyrid fish: central anatomy. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 375-421. New York: John Wiley and Sons.
14. Bennett, M. V. L. (1965). Electroreceptors in mormyrids. Cold Spring Harb. Symp. Quant. Biol. 30, 245-262.
15. Bennett, M. V. L. (1971). Electroreception. In Fish Physiology, Vol. 5 (ed. W. S. Hoar and D. J. Randall), pp. 493-568. New York: Academic Press.
16. Brand, A., Urban, R. and Grothe, B. (2000). Duration tuning in the mouse auditory midbrain. J. Neurophysiol. 84, 1790-1799.
17. Carlson, B. A. (2002). Electric signaling behavior and the mechanisms of electric organ discharge production in mormyrid fish. J. Physiol. Paris 96, 405-419.
18. Carlson, B. A. (2006). A neuroethology of electrocommunication: senders, receivers, and everything in between. In Communication in Fishes, Vol. 2 (ed. F. Ladich, S. P. Collin, P. Moller and B. G. Kapoor), pp. 805-848. Enfield, NH: Science Publishers.
19. Carlson, B. A. (2009). Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. J. Neurosci. 29, 9417-9428.
20. Carlson, B. A. and Hopkins, C. D. (2004). Stereotyped temporal patterns in electrical communication. Anim. Behav. 68, 867-878.
21. Carlson, B. A. and Kawasaki, M. (2006). Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes. J. Neurosci. 26, 9173-9183.
22. Carlson, B. A. and Kawasaki, M. (2007). Behavioral responses to jamming and 'phantom' jamming stimuli in the weakly electric fish Eigenmannia. J. Comp. Physiol. A 193, 927-941.
23. Carlson, B. A., Hopkins, C. D. and Thomas, P. (2000). Androgen correlates of socially induced changes in the electric organ discharge waveform of a mormyrid fish. Horm. Behav. 38, 177-186.
24. Carlson, B. A., Hasan, S. M., Hollmann, M., Miller, D. B., Harmon, L. J. and Arnegard, M. E. (2011). Brain evolution triggers increased diversification of electric fishes. Science 332, 583-586.
25. Carr, C. E. and Friedman, M. A. (1999). Evolution of time coding systems. Neural Comput. 11, 1-20.
26. Chelaru, M. I. and Dragoi, V. (2008). Efficient coding in heterogeneous neuronal populations. Proc. Natl. Acad. Sci. USA 105, 16344-16349.
27. Clark, B. D., Goldberg, E. M. and Rudy, B. (2009). Electrogenic tuning of the axon initial segment. Neuroscientist 15, 651-668.
28. Covey, E. and Casseday, J. H. (1999). Timing in the auditory system of the bat. Annu. Rev. Physiol. 61, 457-476.
29. Derbin, C. and Szabo, T. (1968). Ultrastructure of an electroreceptor (knollenorgan) in the mormyrid fish Gnathonemus petersii. I. J. Ultrastruct. Res. 22, 469-484.
30. Edwards, C. J., Leary, C. J. and Rose, G. J. (2007). Counting on inhibition and rate-dependent excitation in the auditory system. J. Neurosci. 27, 13384-13392.
31. Edwards, C. J., Leary, C. J. and Rose, G. J. (2008). Mechanisms of long-interval selectivity in midbrain auditory neurons: roles of excitation, inhibition, and plasticity. J. Neurophysiol. 100, 3407-3416.
32. Feulner, P. G., Plath, M., Engelmann, J., Kirschbaum, F. and Tiedemann, R. (2009). Electrifying love: electric fish use species-specific discharge for mate recognition. Biol. Lett. 5, 225-228.
33. Fischer, B. J., Steinberg, L. J., Fontaine, B., Brette, R. and Pena, J. L. (2011). Effect of instantaneous frequency glides on interaural time difference processing by auditory coincidence detectors. Proc. Natl. Acad. Sci. USA 108, 18138-18143.
34. Fortune, E. S., Rose, G. J. and Kawasaki, M. (2006). Encoding and processing biologically relevant temporal information in electrosensory systems. J. Comp. Physiol. A 192, 625-635.
35. Friedman, M. A. and Hopkins, C. D. (1996). Tracking individual mormyrid electric fish in the field using electric organ discharge waveforms. Anim. Behav. 51, 391-407.
36. Friedman, M. A. and Hopkins, C. D. (1998). Neural substrates for species recognition in the time-coding electrosensory pathway of mormyrid electric fish. J. Neurosci. 18, 1171-1185.
37. Gabbiani, F. and Koch, C. (1998). Principles of spike train analysis. In Methods in Neuronal Modeling: From Ions to Networks (ed. C. Koch and I. Segev), pp. 313-360. Cambridge, MA: MIT Press.
38. George, A. A., Lyons-Warren, A. M., Ma, X. and Carlson, B. A. (2011). A diversity of synaptic filters are created by temporal summation of excitation and inhibition. J. Neurosci. 31, 14721-14734.
39. Graff, C. and Kramer, B. (1992). Trained weakly-electric fishes, Pollimyrus isidori and Gnathonemus petersii (Mormyridae, Teleostei) discriminate between waveforms of electric pulse discharges. Ethology 90, 279-292.
40. Harder, W. (1968a). Die beziehungen zwischen elektrorezeptoren, elektrischem organ, seitenlinienorganen und nervensystem bei den Mormyridae (Teleostei, Pisces). Z. Vgl. Physiol. 59, 272-318.
41. Harder, W. (1968b). Zum aufbau der epidermalen sinnesorgane der Mormyridae (Mormyriformes, Teleostei). Z. Zellforsch. Mikrosk. Anat. 89, 212-224.
42. Hopkins, C. D. (1976). Stimulus filtering and electroreception: tuberous electroreceptors in three species of gymnotoid fish. J. Comp. Physiol. A 111, 171-207.
43. Hopkins, C. D. (1981). On the diversity of electric signals in a community of mormyrid electric fish in West Africa. Am. Zool. 21, 211-222.
44. Hopkins, C. D. and Bass, A. H. (1981). Temporal coding of species recognition signals in an electric fish. Science 212, 85-87.
45. Koppl, C. (2009). Evolution of sound localisation in land vertebrates. Curr. Biol. 19, R635-R639.
46. Lawhern, V., Nikonov, A. A., Wu, W. and Contreras, R. J. (2011). Spike rate and spike timing contributions to coding taste quality information in rat periphery. Front. Integr. Neurosci. 5, 18.
47. Lissmann, H. W. and Mullinger, A. M. (1968). Organization of ampullary electric receptors in Gymnotidae (Pisces). Proc. R. Soc. Lond. B169, 345-378.
48. Livingstone, M. and Hubel, D. (1988). Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740-749.
49. Machnik, P. and Kramer, B. (2008). Female choice by electric pulse duration: attractiveness of the males' communication signal assessed by female bulldog fish, Marcusenius pongolensis (Mormyridae, Teleostei). J. Exp. Biol. 211, 1969-1977.
50. Marsat, G. and Maler, L. (2010). Neural heterogeneity and efficient population codes for communication signals. J. Neurophysiol. 104, 2543-2555.
51. Moller, P. and Bauer, R. (1973). 'Communication' in weakly electric fish, Gnathonemus petersii (Mormyridae) II. Interaction of electric organ discharge activities of two fish. Anim. Behav. 21, 501-512.
52. Moller, P., Serrier, J. and Bowling, D. (1989). Electric organ discharge displays during social encounter in the weakly electric fish Brienomyrus niger L. (Mormyridae). Ethology 82, 177-191.
53. Mugnaini, E. and Maler, L. (1987). Cytology and immunocytochemistry of the nucleus extrolateralis anterior of the mormyrid brain: possible role of GABAergic synapses in temporal analysis. Anat. Embryol. 176, 313-336.
54. Neumann, E. and Nachmansohn, D. (1975). Nerve excitability - toward an integrating concept. In Biomembranes, Vol. 7 (ed. H. Eisenberg, E. Katchalski-Katzir and L. A. Manson), pp. 99-166. New York: Plenum Press.
55. Nishino, E. and Ohmori, H. (2009). The modulation by intensity of the processing of interaural timing cues for localizing sounds. Mol. Neurobiol. 40, 157-165.
56. Nishino, E., Yamada, R., Kuba, H., Hioki, H., Furuta, T., Kaneko, T. and Ohmori, H. (2008). Sound-intensity-dependent compensation for the small interaural time difference cue for sound source localization. J. Neurosci. 28, 7153-7164.
57. Paintner, S. and Kramer, B. (2003). Electrosensory basis for individual recognition in a weakly electric, mormyrid fish, Pollimyrus adspersus (Gunther, 1866). Behav. Ecol. Sociobiol. 55, 197-208.
58. Pena, J. L. and Konishi, M. (2000). Cellular mechanisms for resolving phase ambiguity in the owl's inferior colliculus. Proc. Natl. Acad. Sci. USA 97, 11787-11792.
59. Post, N. and von der Emde, G. (1999). The "novelty response" in an electric fish: response properties and habituation. Physiol. Behav. 68, 115-128.
60. Ricci, A. J., Crawford, A. C. and Fettiplace, R. (2003). Tonotopic variation in the conductance of the hair cell mechanotransducer channel. Neuron 40, 983-990.
61. Rose, G. J. (2004). Insights into neural mechanisms and evolution of behaviour from electric fish. Nat. Rev. Neurosci. 5, 943-951.
62. Sawtell, N. B., Williams, A. and Bell, C. C. (2005). From sparks to spikes: information processing in the electrosensory systems of fish. Curr. Opin. Neurobiol. 15, 437-443.
63. Sayegh, R., Aubie, B. and Faure, P. A. (2011). Duration tuning in the auditory midbrain of echolocating and non-echolocating vertebrates. J. Comp. Physiol. A 197, 571-583.
64. Sullivan, J. P., Lavoue, S. and Hopkins, C. D. (2002). Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei). Evolution 56, 597-616.
65. Sullivan, W. E. and Konishi, M. (1984). Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl. J. Neurosci. 4, 1787-1799.
66. Szabo, T. (1965). Sense organs of the lateral line system in some electric fish of the Gymnotidae, Mormyridae and Gymnarchidae. J. Morphol. 117, 229-249.
67. Szabo, T., Enger, P. S. and Libouban, S. (1979). Electrosensory systems in the mormyrid fish, Gnathonemus petersii: special emphasis on the fast conducting pathway. J. Physiol. Paris 75, 409-420.
68. Szamier, R. B. and Wachtel, A. W. (1970). Special cutaneous receptor organs of fish. VI. Ampullary and tuberour organs of Hypopomus. J. Ultrastruct. Res. 30, 450-471.
69. Szabo, T., Ravaille, M., Libouban, S. and Enger, P. S. (1983). The mormyrid rhombencephalon: I. Light and EM investigations on the structure and connections of the lateral line lobe nucleus with HRP labelling. Brain Res. 266, 1-19.
70. Szucs, A. (1998). Applications of the spike density function in analysis of neuronal firing patterns. J. Neurosci. Methods 81, 159-167.
71. von der Emde, G. (1999). Active electrolocation of objects in weakly electric fish. J. Exp. Biol. 202, 1205-1215.
72. Xu-Friedman, M. A. and Hopkins, C. D. (1999). Central mechanisms of temporal analysis in the knollenorgan pathway of mormyrid electric fish. J. Exp. Biol. 202, 1311-1318.
73. Young, E. D. (1998). Parallel processing in the nervous system: evidence from sensory maps. Proc. Natl. Acad. Sci. USA 95, 933-934.
74. Zakon, H. H. (1986). The electroreceptive periphery. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 103-156. New York: John Wiley and Sons.
75. Zakon, H. H. (2003). Insight into the mechanisms of neuronal processing from electric fish. Curr. Opin. Neurobiol. 13, 744-750.