Bursts and isolated spikes code for opposite movement directions in midbrain electrosensory neurons

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Khosravi Hashemi, Navid ^a   Chacron, Maurice J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL T TYPE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; BURSTS AND ISOLATED SPIKE; CONTROLLED STUDY; ELECTRIC FISH; MATHEMATICAL MODEL; MIDBRAIN ELECTROSENSORY NEURON; MOVEMENT PERCEPTION; NONHUMAN; OPPOSITE MOVEMENT DIRECTION; PREDICTION; SENSORY NERVE CELL; STIMULATION; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BIOPHYSICAL PHENOMENA; CALCIUM CHANNELS, T-TYPE; ELECTRIC FISH; MESENCEPHALON; MODELS, NEUROLOGICAL; MOVEMENT; NEURAL INHIBITION; SENSORY RECEPTOR CELLS; SYNAPSES; TIME FACTORS;

EID: 84863107760     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040339     Document Type: Article

References (104)

1. Tammero LF, Frye MA, Dickinson MH, (2004) Spatial organization of visuomotor reflexes in Drosophila. J Exp Biol 207: 113-122.
2. Frye MA, (2001) Effects of stretch receptor ablation on the optomotor control of lift in the hawkmoth Manduca sexta. J Exp Biol 204: 3683-3691.
3. Srinivasan MV, Poteser M, Kral K, (1999) Motion detection in insect orientation and navigation. Vision Res 39: 2749-2766.
4. Rose GJ, Call SJ, (1993) Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines. Journal of Neuroscience 13: 1178-1189.
5. Cowan NJ, Fortune ES, (2007) The critical role of locomotion mechanics in decoding sensory systems. Journal of Neuroscience 27: 1123-1128.
6. Horak FB, Macpherson JM, (1996) Postural orientation and equilibrium. In: Rowell LB, Shepherd JT, editors. pp. 255-292 editors. Handbook of physiology section 12: Exercise regulation and integration of multiple systems. New York (New York): Oxford University Press.
7. Kuo AD, (2005) An optimal state estimation model of sensory integration in human postural balance. J Neural Eng 2: S235-249.
8. Kiemel T, Oie KS, Jeka JJ, (2002) Multisensory fusion and the stochastic structure of postural sway. Biol Cybern 87: 262-277.
9. Carver S, Kiemel T, van der Kooij H, Jeka JJ, (2005) Comparing internal models of the dynamics of the visual environment. Biol Cybern 92: 147-163.
10. Nelson ME, MacIver MA, (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. Journal of Experimental Biology 202: 1195-1203.
11. 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: 543-557.
12. Hubel DH, Wiesel TN, (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160: 106-154.
13. Euler T, Detwiler PB, Denk W, (2002) Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418: 845-852.
14. Haag J, Denk W, Borst A, (2004) Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. PNAS 101: 16333-16338.
15. Heiligenberg W, Rose GJ, (1987) The Optic Tectum of the Gymnotiform Electric Fish, Eigenmannia - Labeling of Physiologically Identified Cells. Neuroscience 22: 331-340.
16. Bastian J, (1982) Vision and Electroreception - Integration of Sensory Information in the Optic Tectum of the Weakly Electric Fish Apteronotus-Albifrons. Journal of Comparative Physiology 147: 287-297.
17. Ramcharitar JU, Tan EW, Fortune ES, (2006) Global Electrosensory Oscillations Enhance Directional Responses of Midbrain Neurons in Eigenmannia. Journal of Neurophysiology 96: 2319-2326.
18. Chacron MJ, Toporikova N, Fortune ES, (2009) Differences in the Time Course of Short-Term Depression Across Receptive Fields Are Correlated With Directional Selectivity in Electrosensory Neurons. Journal of Neurophysiology 102: 3270-3279.
19. Borst A, (2007) Correlation versus gradient type motion detectors: the pros and cons. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences 362: 369-374.
20. Derrington AM, Allen HA, Delicato LS, (2004) Visual mechanisms of motion analysis and motion perception. Annu Rev Psychol 55: 181-205.
21. Hock HS, Schoner G, Gilroy L, (2009) A counterchange mechanism for the perception of motion. Acta Psychol (Amst) 132: 1-21.
22. Maex R, Orban GA, (1991) Subtraction inhibition combined with a spiking threshold accounts for cortical direction selectivity. Proc Natl Acad Sci U S A 88: 3549-3553.
23. Borst A, Egelhaaf M, (1989) Principles of visual motion detection. Trends Neurosci 12: 297-306.
24. Borst A, Egelhaaf M, (1990) Direction selectivity of blowfly motion-sensitive neurons is computed in a two-stage process. PNAS 87: 9363-9367.
25. Avila Akerberg O, Krahe R, Chacron MJ, (2010) Neural heterogeneities and stimulus properties affect burst coding in vivo. Neuroscience 168: 300-313.
26. Khosravi-Hashemi N, Fortune ES, Chacron MJ, (2011) Coding Movement Direction by Burst Firing in Electrosensory Neurons. Journal of Neurophysiology 106: 1954-1968.
27. Jagadeesh B, Wheat HS, Kontsevich LL, Tyler CW, Ferster D, (1997) Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. Journal of Neurophysiology 78: 2772-2789.
28. Priebe NJ, Ferster D, (2008) Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57: 482-497.
29. Priebe NJ, Mechler F, Carandini M, Ferster D, (2004) The contribution of spike threshold to the dichotomy of cortical simple and complex cells. Nature Neuroscience 7: 1113-1122.
30. Reichardt W, Wenking H, (1969) Optical detection and fixation of objects by fixed flying flies. Naturwissenschaften 56: 424-425.
31. Reichardt W, (1987) Evaluation of optical motion information by movement detectors. Journal of Comparative Physiology A 161: 533-547.
32. Carver S, Roth E, Cowan NJ, Fortune ES, (2008) Synaptic plasticity can produce and enhance direction selectivity. PLoS Computational Biology 4: e32.
33. Chance FS, Nelson SB, Abbott LF, (1998) Synaptic depression and the temporal response characteristics of V1 cells. Journal of Neuroscience 18: 4785-4799.
34. Adelson EH, Bergen JR, (1985) Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A-Optics & Image Science 2: 284-299.
35. Chacron MJ, Fortune ES, (2010) Subthreshold membrane conductances enhance directional selectivity in vertebrate sensory neurons. Journal of Neurophysiology 104: 449-462.
36. Chacron MJ, Bastian J, (2008) Population coding by electrosensory neurons. Journal of Neurophysiology 99: 1825-1835.
37. Chacron MJ, Longtin A, Maler L, (2001) Simple models of bursting and non-bursting electroreceptors. Neurocomputing 38: 129-139.
38. Chacron MJ, Longtin A, Maler L, (2004) To Burst or Not to Burst? Journal of Computational Neuroscience 17: 127-136.
39. Deemyad T, Maler L, Chacron MJ, (2011) Inhibition of SK and M channel mediated currents by 5-HT enables parallel processing by bursts and isolated spikes. Journal of Neurophysiology 105: 1276-1294.
40. Gabbiani F, Koch C, (1996) Coding of Time-Varying Signals in Spike Trains of Integrate-and-Fire Neurons with Random Threshold. Neural Computation 8: 44-66.
41. Kepecs A, Lisman J, (2003) Information encoding and computation with spikes and bursts. Network 14: 103-118.
42. Lesica NA, Stanley GB, (2004) Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. Journal of Neuroscience 24: 10731-10740.
43. Martinez-Conde S, Macknik SL, Hubel DH, (2002) The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. PNAS 99: 13920-13925.
44. Oswald AMM, Chacron MJ, Doiron B, Bastian J, Maler L, (2004) Parallel Processing of Sensory Input by Bursts and Isolated Spikes. Journal of Neuroscience 24: 4351-4362.
45. Sherman SM, (2001) Tonic and burst firing: dual modes of thalamocortical relay. Trends in Neurosciences 24: 122-126.
46. Avila-Akerberg O, Krahe R, Chacron MJ, (2010) Neural heterogeneities and stimulus properties affect burst coding in vivo. Neuroscience 168: 300-313.
47. Avila Akerberg O, Chacron MJ, (2011) Nonrenewal spike train statistics: causes and functional consequences on neural coding. Experimental Brain Research 210: 353-371.
48. DeBusk BC, DeBruyn EJ, Snider RK, Kabara JF, Bonds AB, (1997) Stimulus-dependent modulation of spike burst length in cat striate cortical cells. Journal of Neurophysiology 78: 199-213.
49. Eyherabide HG, Rokem A, Herz AV, Samengo I, (2008) Burst firing is a neural code in an insect auditory system. Front Comput Neurosci 2: 3.
50. Gaudry KS, Reinagel P, (2008) Information measure for analyzing specific spiking patterns and applications to LGN bursts. Network 19: 69-94.
51. Kepecs A, Wang XJ, Lisman J, (2002) Bursting Neurons Signal Input Slope. Journal of Neuroscience 22: 9053-9062.
52. Marsat G, Pollack GS, (2010) The structure and size of sensory bursts encode stimulus information but only size affects behavior. Journal of Comparative Physiology A 196: 315-320.
53. Oswald AM, Doiron B, Maler L, (2007) Interval coding. I. Burst interspike intervals as indicators of stimulus intensity.[see comment]. Journal of Neurophysiology 97: 2731-2743.
54. Samengo I, Montemurro MA, (2010) Conversion of phase information into a spike-count code by bursting neurons. PLoS One 5: e9669.
55. Chacron MJ, Longtin A, Maler L, (2011) Efficient computation via sparse coding in electrosensory neural networks. Current Opinion in Neurobiology 21: 752-760.
56. Turner RW, Maler L, Burrows M, (1999) Electroreception and electrocommunication. Journal of Experimental Biology 202: 1167-1458.
57. Hodgkin AL, Huxley AF, (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology London 117: 500-544.
58. Carr CE, Maler L, (1986) Electroreception in gymnotiform fish. Central anatomy and physiology. In: Bullock TH, Heiligenberg W, editors. pp. 319-373 editors. Electroreception. New York: Wiley.
59. Rush ME, Rinzel J, (1994) Analysis of bursting in a thalamic neuron model. Biol Cybern 71: 281-291.
60. Sherman SM, Guillery RW, (2006) Exploring the Thalamus and its Role in Cortical Function. Cambridge, MA: MIT Press.
61. Destexhe A, Rudolph M, Pare D, (2003) The high-conductance state of neocortical neurons in vivo. Nature Reviews Neuroscience 4: 739-751.
62. Vonderschen K, Chacron MJ, (2011) Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations. Journal of Neurophysiology 106: 3102-3118.
63. Leary CJ, Edwards CJ, Rose GJ, (2008) Midbrain auditory neurons integrate excitation and inhibition to generate duration selectivity: an in vivo whole-cell patch study in anurans. Journal of Neuroscience 28: 5481-5493.
64. Edwards CJ, Leary CJ, Rose GJ, (2008) Mechanisms of long-interval selectivity in midbrain auditory neurons: roles of excitation, inhibition, and plasticity. Journal of Neurophysiology 100: 3407-3416.
65. Green D, Swets J, (1966) Signal Detection Theory and Psychophysics. New York: John Wiley & Sons.
66. Marsat G, Proville RD, Maler L, (2009) Transient signals trigger synchronous bursts in an identified population of neurons. Journal of Neurophysiology 102: 714-723.
67. Marsat G, Pollack GS, (2004) Differential Temporal Coding of Rhythmically Diverse Acoustic Signals by a Single Interneuron. Journal of Neurophysiology 92: 939-948.
68. Avila Akerberg O, Chacron MJ, (2011) In vivo conditions influence the coding of stimulus features by bursts of action potentials. Journal of Computational Neuroscience 31: 369-383.
69. Marsat G, Maler L, (2010) Neural heterogeneity and efficient population codes for communication signals. Journal of Neurophysiology 104: 2543-2555.
70. Lisman JE, (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends in Neurosciences 20: 38-43.
71. George AA, Lyons-Warren AM, Ma X, Carlson BA, (2011) A diversity of synaptic filters are created by temporal summation of excitation and inhibition. Journal of Neuroscience 31: 14721-14734.
72. Carlson BA, (2009) Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. Journal of Neuroscience 29: 9417-9428.
73. Bastian J, (1982) Vision and electroreception. Integration of sensory information in the optic tectum of the weakly electric fish Apteronotus Albibrons. Journal of Comparative Physiology A 147: 287-297.
74. Krahe R, Gabbiani F, (2004) Burst Firing in Sensory Systems. Nature Reviews Neuroscience 5: 13-23.
75. Lu SM, Guido W, Sherman SM, (1992) Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. Journal of Neurophysiology 68: 2185-2198.
76. Jahnsen H, Llinas R, (1984) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. Journal of Physiology (London) 349: 205-226.
77. Sherman SM, Guillery RW, (2002) The role of the thalamus in the flow of information to the cortex. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences 357: 1695-1708.
78. McCormick DA, Huguenard JR, (1992) A model of the electrophysiological properties of thalamocortical relay neurons. Journal of Neurophysiology 68: 1384-1400.
79. Mukherjee P, Kaplan E, (1995) Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. Journal of Neurophysiology 74: 1222-1243.
80. Smith GD, Cox CL, Sherman SM, Rinzel J, (2000) Fourier analysis of sinusoidally driven thalamocortical relay neurons and a minimal integrate-and fire-or-burst model. Journal of Neurophysiology 83: 588-610.
81. Reinagel P, Godwin D, Sherman SM, Koch C, (1999) Encoding of visual information by LGN bursts. Journal of Neurophysiology 81: 2558-2569.
82. Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T, (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nature Neuroscience 8: 1760-1767.
83. Sherman SM, (1996) Dual response modes in lateral geniculate neurons: mechanisms and functions. Visual Neuroscience 13: 205-213.
84. Hitschfeld ÉM, Stamper SA, Vonderschen K, Fortune ES, Chacron MJ, (2009) Effects of Restraint and Immobilization on Electrosensory Behaviors of Weakly Electric Fish. ILAR Journal 50: 361-372.
85. Bastian J, Chacron MJ, Maler L, (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. Journal of Neuroscience 22: 4577-4590.
86. Chacron MJ, (2006) Nonlinear information processing in a model sensory system. Journal of Neurophysiology 95: 2933-2946.
87. Toporikova N, Chacron MJ, (2009) Dendritic SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro. Journal of Neurophysiology 102: 2273-2287.
88. McGillivray P, Vonderschen K, Fortune ES, Chacron MJ, (2012) Parallel coding of first and second order stimulus attributes by midbrain electrosensory neurons. Journal of Neuroscience 32: 5510-5524.
89. Rose GJ, Fortune ES, (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neuroscience Research 26: 89-94.
90. Frank K, Becker MC, (1964) Microelectrodes for recording and stimulation. Physical Techniques in Biological Research, part A. New York: Academic pp. 23-84.
91. Chacron MJ, Lindner B, Longtin A, (2007) Threshold fatigue and information transfer. Journal of Computational Neuroscience 23: 301-311.
92. Chacron MJ, Longtin A, Maler L, (2005) Delayed excitatory and inhibitory feedback shape neural information transmission. Physical Review E 72: 051917.
93. Ramcharitar JU, Tan EW, Fortune ES, (2005) Effects of global electrosensory signals on motion processing in the midbrain of Eigenmannia. Journal of Comparative Physiology A-Sensory Neural & Behavioral Physiology 191: 865-872.
94. Vonderschen K, Chacron MJ, (2009) Sparse Coding of Natural Communication Signals in Midbrain Neurons. Biomedical Central Neuroscience 10: O3.
95. Bastian J, Nguyenkim J, (2001) Dendritic Modulation of Burst-like firing in sensory neurons. Journal of Neurophysiology 85: 10-22.
96. Saunders J, Bastian J, (1984) The physiology and morphology of two classes of electrosensory neurons in the weakly electric fish Apteronotus Leptorhynchus. Journal of Comparative Physiology A 154: 199-209.
97. Chacron MJ, Maler L, Bastian J, (2005) Feedback and Feedforward Control of Frequency Tuning to Naturalistic Stimuli. Journal of Neuroscience 25: 5521-5532.
98. Krahe R, Bastian J, Chacron MJ, (2008) Temporal processing across multiple topographic maps in the electrosensory system. Journal of Neurophysiology 100: 852-867.
99. Carr CE, Maler L, (1985) A Golgi study of the cell types of the dorsal torus semicircularis of the electric fish Eigenmannia: functional and morphological diversity in the midbrain. Journal of Comparative Neurology 235: 207-240.
100. Manwani A, Koch C, (1999) Detecting and estimating signals in noisy cable structure, I: neuronal noise sources. Neural Computation 11: 1797-1829.
101. Lewis JE, Maler L, (2002) Dynamics of electrosensory feedback: short-term plasticity and inhibition in a parallel fiber pathway. Journal of Neurophysiology 88: 1695-1706.
102. Lewis JE, Maler L, (2004) Synaptic dynamics on different time scales in a parallel fiber feedback pathway of the weakly electric fish. Journal of Neurophysiology 91: 1064-1070.
103. Lindner B, Gangloff D, Longtin A, Lewis JE, (2009) Broadband coding with dynamic synapses. Journal of Neuroscience 29: 2076-2087.
104. Harvey-Girard E, Lewis JE, Maler L, (2010) Burst-induced anti-Hebbian depression acts through short-term synaptic dynamics to cancel redundant sensory signals. Journal of Neuroscience 30: 6152-6169.