Statistics of the electrosensory input in the freely swimming weakly electric fish Apteronotus leptorhynchus

Journal of Neuroscience

Volumn 33, Issue 34, 2013, Pages 13758-13772

  Fotowat, Haleh ^a   Harrison, Reid R ^b   Krahe, Rüdiger ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Intan Technologies   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; APTERONOTUS LEPTORHYNCHUS; ARTICLE; CONTROLLED STUDY; DYNAMICS; ELECTRIC FISH; ELECTRIC POTENTIAL; ELECTRODE; ELECTROSTIMULATION; MOVEMENT (PHYSIOLOGY); NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RECORDING; SENSORY STIMULATION; SIGNAL NOISE RATIO; SPATIOTEMPORAL ANALYSIS; SWIMMING; TRUNK; WIRELESS COMMUNICATION;

ANALYSIS OF VARIANCE; ANIMALS; COMPUTER SIMULATION; ELECTRIC FISH; ELECTRIC ORGAN; ELECTRICITY; EVOKED POTENTIALS; MODELS, BIOLOGICAL; SENSORY RECEPTOR CELLS; SKIN; SOCIAL BEHAVIOR; SWIMMING; TELEMETRY; VIDEO RECORDING;

EID: 84882713440     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0998-13.2013     Document Type: Article

References (67)

1. Assad C, Rasnow B, Stoddard PK (1999) Electric organ discharges and electric images during electrolocation. J Exp Biol 202:1185-1193.
2. Attias H, Schreiner CE (1997) Temporal low-order statistics of natural sounds. Advances in Neural Information Processing Systems 9:27-33.
3. Babineau D, Longtin A, Lewis JE (2006) Modeling the electric fieldofweakly electric fish. J Exp Biol 209:3636-3651.
4. Barlow HB (1961) Possible principles underlying the transformationof sensory messages. In: Sensory communication (Rosenblith WA, ed.), pp 217-234. Cambridge: MIT.
5. Bastian J (1981) Electrolocation. 1. How the electroreceptors of Apteronotus albifrons code for moving objects and other electrical stimuli. J Comp Physiol A 144:465-479.
6. Bastian J (1995) Pyramidal-cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs. J Comp Physiol A 176:63-78.
7. Bastian J (1999) Plasticity of feedback inputs in the apteronotid electrosen-sory system. J Exp Biol 202:1327-1337.
8. Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85:10-22.
9. Bastian J, Chacron MJ, Maler L (2004) Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41:767-779.
10. Billock VA, de Guzman GC, Scott Kelso JA (2001) Fractal time and 1/f spectra in dynamic images and human vision. Physica D: Nonlinear Phenomena 148:136-146.
11. Bullock TH, Hopkins CD, Fay RR, editors (2005) Electroreception. New York: Springer.
12. Carr CE, Maler L, Sas E (1982) Peripheral organization and central projections of the electrosensory nerves in gymnotiform fish. J Comp Neurol 211:139-153.
13. Chacron MJ (2006) Nonlinear information processing in a model sensory system. J Neurophysiol 95:2933-2946.
14. Chacron MJ, Maler L, Bastian J (2005) Electroreceptor neuron dynamics shape information transmission. Nat Neurosci 8:673-678.
15. Chen L, House JL, Krahe R, Nelson ME (2005) Modeling signal and background components of electrosensory scenes. J Comp Physiol A Neuro-ethol Sens Neural Behav Physiol 191:331-345.
16. Dong DW, Atick JJ (1995) Statistics of natural time-varying images. Network: Computation in Neural Systems 6:345-358.
17. Egelhaaf M, Boeddeker N, Kern R, Kurtz R, Lindemann JP (2012) Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action. Front Neural Circuits 6:108.
18. Eke A, Herman P, Kocsis L, Kozak LR (2002) Fractal characterization of complexity in temporal physiological signals. Physiol Meas 23:R1-38.
19. Fairhall AL, Lewen GD, Bialek W, de Ruyter van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792.
20. Fortune ES (2006) The decoding ofelectrosensory systems. Curr Opin Neu-robiol 16:474-480.
21. Geisler WS (2008) Visual perception and the statistical properties of natural scenes. Annu Rev Psychol 59:167-192.
22. Gisiger T (2001) Scale invariance in biology: coincidence or footprint of a universal mechanism? Biol Rev Camb Philos Soc 76:161-209.
23. Gussin D, Benda J, Maler L (2007) Limits of linear rate coding of dynamic stimuli by electroreceptor afferents. J Neurophysiol 97:2917-2929.
24. Hagiwara S, Morita H (1963) Coding mechanisms of electroreceptor fibers in some electric fish. J Neurophysiol 26:551-567.
25. Hardstone R, Poil SS, Schiavone G, Jansen R, Nikulin VV, Mansvelder HD, Linkenkaer-Hansen K (2012) Detrended fluctuation analysis: a scale-free view on neuronal oscillations. Front Physiol 3:450.
26. Harrison RR, Fotowat H, Chan R, Kier RJ, Olberg R, Leonardo A, Gabbiani F (2011) Wireless neural/EMG telemetry systems for small freely moving animals. IEEE Trans Biomed Circuits Syst 5:103-111.
27. Hedrick TL (2008) Software techniques for two- and three-dimensional kinematic mea surements of biological and biomimetic systems. Bioinspir Biomim 3:034001.
28. Heiligenberg W (1991) Neural nets in electric fish. Cambridge, MA: MIT.
29. Heneghan C, McDarby G (2000) Establishing the relation between de-trended fluctuation analysis and power spectral density analysis for stochastic processes. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 62:6103-6110.
30. Hofmann V, Sanguinetti-Scheck JI, Künzel S, Geurten B, Gómez-Sena L, Engelmann J (2013) Sensory flow shaped by active sensing: sensorimo-tor strategies in electric fish. J Exp Biol 216:2487-2500.
31. Jackson JD (1975) Classical electrodynamics. New York: Wiley.
32. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541-577.
33. Kayser C, Einhäuser W, König P (2003) Temporal correlations of orientations in natural scenes. Neurocomputing 52-54:117-123.
34. Kelly M, Babineau D, Longtin A, Lewis JE (2008) Electric field interactions in pairs of electric fish: modeling and mimicking naturalistic inputs. Biol Cybern 98:479-490.
35. Krahe R, Budinger E, Ronacher B (2002) Coding of a sexually dimorphic song feature by auditory interneurons of grasshoppers: the role of leading inhibition. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 187: 977-985.
36. Krahe R, Bastian J, Chacron MJ (2008) Temporal processing across multiple topographic maps in the electrosensory system. J Neurophysiol 100:852-867.
37. Kurtz R, Egelhaaf M (2003) Natural patterns of neural activity: how physiological mechanisms are orchestrated to cope with real life. Mol Neuro-biol 27:13-32.
38. Lundstrom BN, Higgs MH, Spain WJ, Fairhall AL (2008) Fractional differentiation by neocortical pyramidal neurons. Nat Neurosci 11:1335-1342.
39. Lundstrom BN, Fairhall AL, Maravall M (2010) Multiple timescale encoding of slowly varying whisker stimulus envelope in cortical and thalamic neurons in vivo. J Neurosci 30:5071-5077.
40. MacIver MA, Patankar NA, Shirgaonkar AA (2010) Energy-information trade-offs between movement and sensing. PLoS Comput Biol 6:e1000769.
41. MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: Motion analysis and effects of water conductivity. J Exp Biol 204:543-547.
42. Maler L (2009) Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size. J Comp Neurol 516:376-393.
43. Mandelbrot BB, Van Ness JW (1968) Fractional Brownian motions, fractional noises and applications. Society for Industrial and Applied Mathematics Reviews 10:422-437.
44. Mareschal I, Baker CL Jr (1998) A cortical locus for the processing of contrast-defined contours. Nat Neurosci 1:150-154.
45. Marsat G, Maler L (2012) Preparing for the unpredictable: adaptive feedback enhances the response to unexpected communication signals. JNeu-rophysiol 107:1241-1246.
46. McGillivray P, Vonderschen K, Fortune ES, Chacron MJ (2012) Parallel coding offirst- and second-order stimulus attributes bymidbrain electro-sensory neurons. J Neurosci 32:5510-5524.
47. Middleton JW, Longtin A, Benda J, Maler L (2006) The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proc Natl Acad Sci U S A 103:14596-14601.
48. Moore DS, McCabe GP (2006) Introduction to the practice of statistics, pp 637-667. New York: Freeman.
49. Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202:1195-1203.
50. Nelson ME, Xu Z, Payne JR (1997) Characterization and modeling of P-type electrosen sory afferent responses to amplitude modulations in a wave-type electric fish. J Comp Physiol A 181:532-544.
51. Pollak GD (2012) Circuits for processing dynamic interaural intensity disparities in the inferior colliculus. Hear Res 288:47-57.
52. Rasnow B, Bower J (1996) The electric organ discharges ofthe gymnotiform fishes. 1. Apteronotus leptorhynchus. J Comp Physiol A 178:383-396.
53. Rasnow B, Assad C, Bower J (1993) Phase and amplitude maps of the electric organ discharge of the weakly electric fish,Apteronotus leptorhynchus. J Comp Physiol A 172:481-491.
54. Rodriguez FA, Chen C, Read HL, Escabí MA (2010) Neural modulation tuning characteristics scale to efficiently encode natural sound statistics. J Neurosci 30:15969-15980.
55. Ruderman DL, Bialek W (1994) Statistics of natural images: scaling in the woods. Phys Rev Lett 73:814-817.
56. Sas E, Maler L (1987) The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anat Em-bryol 177:55-79.
57. Savard M, Krahe R, Chacron MJ (2011) Neural heterogeneities influence envelope and temporal coding at the sensory periphery. Neuroscience 172:270-284.
58. Schroeder CE, Wilson DA, Radman T, Scharfman H, Lakatos P (2010) Dynamics of active sensing and perceptual selection. Curr Opin Neurobiol 20:172-176.
59. Shumway CA (1989) Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. 1. Physiological differences. J Neurosci 9:4388-4399.
60. Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193-1216.
61. Stamper SA, Roth E, Cowan NJ, Fortune ES (2012) Active sensing via movement shapes spatiotemporal patterns of sensory feedback. J Exp Biol 215: 1567-1574.
62. Van Hateren JH (1993) Spatiotemporal contrast sensitivity of early vision. Vision Res 33:257-267.
63. Voss RF, Clarke J (1975) 1/f noiseinspeech and music. Nature 258:317-318.
64. Xu Z, Payne JR, Nelson ME (1996) Logarithmic time course of sensory adaptation in electrosensory afferent nerve fibers in a weakly electric fish. J Neurophysiol 76:2020-2032.
65. Yu N, Hupé G, Garfinkle C, Lewis JE, Longtin A (2012) Coding conspe-cific identity and motion in the electric sense. PLoS Comput Biol 8:e1002564.
66. Zeimer RE, Tranter WH, Fannin DR (1990) Signals and systems: continuous and discrete. New Jersey: Prentice Hall.
67. Zhou YX, Baker CL Jr (1994) Envelope-responsive neurons in areas 17 and 18 of cat. J Neurophysiol 72:2134-2150.