Random noise paradoxically improves light-intensity encoding in Hermissenda photoreceptor network

Journal of Neurophysiology

Volumn 99, Issue 1, 2008, Pages 146-154

  Butson, Christopher R ^a   Clark, Gregory A ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL;

ARTICLE; EYE; HERMISSENDA; HODGKIN HUXLEY EQUATION; LIGHT INTENSITY; MODEL; NOISE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RANDOMIZATION; STATISTICAL SIGNIFICANCE; STATISTICS;

ACTION POTENTIALS; ANIMALS; ARTIFACTS; COMPUTER SIMULATION; EYE; HERMISSENDA; ION CHANNELS; NERVE NET; NEURONS; OCULAR PHYSIOLOGY; PHOTIC STIMULATION; PHOTORECEPTORS, INVERTEBRATE; PHOTOTRANSDUCTION; SENSORY THRESHOLDS; STOCHASTIC PROCESSES; SYNAPTIC TRANSMISSION; VISION;

EID: 38349031420     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01247.2006     Document Type: Article

References (67)

1. Akaike T, Alkon DL. Sensory convergence on central visual neurons in Hermissenda. J Neurophysiol 44: 501-513, 1980.
2. Alkon DL. Associative training of Hermissenda. J Gen Physiol 64: 70-84, 1974.
3. Alkon DL. Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226: 1037-1045, 1984.
4. Alkon DL, Fuortes MG. Responses of photoreceptors in Hermissenda. J Gen Physiol 60: 631-649, 1972.
5. Alkon DL, Grossman Y. Long-lasting depolarization and hyperpolarization in eye of Hermissenda. J Neurophysiol 41: 1328-1342, 1978.
6. Bialek W, Rieke F, de Ruyter van Steveninck RR, Warland D. Reading a neural code. Science 252: 1854-1857, 1991.
7. Blackwell KT. Ionic currents underlying difference in light response between type A and type B photoreceptors. J Neurophysiol 95: 3060-3072, 2006.
8. Bower JM, Beeman D. The Book of GENESIS: Exploring Realistic Neural Models with the GEneral NEural SImulation System (2nd ed.). New York: Springer-Verlag, 1998.
9. Butson CR, Clark GA. Random noise confers a paradoxical improvement in the ability of a simulated Hermissenda photoreceptor network to encode light intensity. Soc Neurosci Abstr 954.6, 2001.
10. Butson CR, Clark GA. Noise alters contextual spike timing relationships and improves light encoding accuracy in a simulated Hermissenda photoreceptor network. Soc Neurosci Abstr 848.6, 2002.
11. Butson CR, Clark GA. Mechanisms of noise-induced improvement in lightintensity encoding in Hermissenda photoreceptor network. J Neurophysiol (January 2008). doi:10.1152/jn.01250.2006.
12. + channels in spike broadening observed in soma and axon of Hermissenda type-B photoreceptors: a simulation study. J Comput Neurosci 21: 89-99, 2006.
13. Cecchi GA, Sigman M, Alonso J, Martinez L, Chialvo DR. Noise in neurons is message dependent. Proc Natl Acad Sci USA 97: 5557-5561, 2000.
14. Chialvo DR, Guillermo AC, Marcelo OM. Noise-induced memory in extended excitable systems. Phys Rev E Stat Nonlin Soft Matter Phys 61: 5654-5657, 2000.
15. Chow CC, White JA. Spontaneous action potentials due to channel fluctuations. Biophys J 71: 3013-3021, 1996.
16. Crow T. Conditioned modification of locomotion in Hermissenda crassicornis: analysis of time-dependent associative and nonassociative components. J Neurosci 3: 2621-2628, 1983.
17. Crow T, Offenbach N. Modification of the initiation of locomotion in Hermissenda: behavioral analysis. Brain Res 271: 301-310, 1983.
18. Crow T, Tian LM. Interneuronal projections to identified cilia-activating pedal neurons in Hermissenda. J Neurophysiol 89: 2420-2429, 2003a.
19. Crow T, Tian LM. Neural correlates of Pavlovian conditioning in components of the neural network supporting ciliary locomotion in Hermissenda. Learn Mem 10: 209-216, 2003b.
20. Crow T, Tian LM. Statocyst hair cell activation of identified interneurons and foot contraction motor neurons in Hermissenda. J Neurophysiol 91: 2874-2883, 2004.
21. Crow TJ, Alkon DL. Retention of an associative behavioral change in Hermissenda. Science 201: 1239-1241, 1978.
22. Crow TJ, Alkon DL. Associative behavioral modification in Hermissenda: cellular correlates. Science 209: 412-414, 1980.
23. DeFelice LJ, Alkon DL. Voltage noise from hair cells during mechanical stimulation. Nature 269: 613-615, 1977.
24. Dennis MJ. Electrophysiology of the visual system in a nudibranch mollusc. J Neurophysiol 30: 1439-1465, 1967.
25. Detwiler PB. Multiple light-evoked conductance changes in the photoreceptors of Hermissenda crassicornis. J Physiol 256: 691-708, 1976.
26. Farley J, Alkon DL. Neural organization predicts stimulus specificity for a retained associative behavioral change. Science 210: 1373-1375, 1980.
27. Farley J, Alkon DL. Associative neural and behavioral change in Hermissenda: consequences of nervous system orientation for light and pairing specificity. J Neurophysiol 48: 785-807, 1982.
28. Fost JW, Clark GA. Contributions of enhanced type-B cell excitability and synaptic strength to inhibition of type-A cells in Hermissenda: a physiological analysis. Soc Neurosci Abstr 553.1, 1996a.
29. C to type-B cell plasticity. J Comput Neurosci 3: 137-153, 1996b.
30. Fost JW, Clark GA. Modeling Hermissenda: II. Effects of variations in type-B cell excitability, synaptic strength, and network architecture. J Comput Neurosci 3: 155-172, 1996c.
31. Frysztak RJ, Crow T. Enhancement of type B and A photoreceptor inhibitory synaptic connections in conditioned Hermissenda. J Neurosci 14: 1245-1250, 1994.
32. Gandhi CC, Matzel LD. Modulation of pre-synaptic action potential kinetics underlies synaptic facilitation of type B photoreceptors after associative conditioning in Hermissenda. J Neurosci 20: 2022-2035, 2000.
33. Goh Y, Alkon DL. Sensory, interneuronal, and motor interactions within Hermissenda visual pathway. J Neurophysiol 52: 156-169, 1984.
34. Goh Y, Lederhendler I, Alkon DL. Input and output changes of an identified neural pathway are correlated with associative learning in Hermissenda. J Neurosci 5: 536-543, 1985.
35. Grossman Y, Alkon DL, Heldman E. A common origin of voltage noise and generator potentials in statocyst hair cells. J Gen Physiol 73: 23-48, 1979.
36. Grover L, Farley J, Vold L. Training and testing determinants of short-term associative suppression of phototaxic behavior in Hermissenda. Behav Neural Biol 47: 275-306, 1987.
37. Han Y, Gandhi CC, Matzel LD. Influence of blocking the A-current in Hermissenda type B cells on transmission during spike trains and photoresponses. Soc Neurosci Abstr 384.9, 2001.
38. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544, 1952.
39. Holt GR, Softky WR, Koch C, Douglas RJ. Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75: 1806-1814, 1996.
40. Horikawa Y. Noise effects on spike propagation in the stochastic Hodgkin-Huxley models. Biol Cybern 66: 19-25, 1991.
41. Keeler JD, Elgar EP, Ross J. Noise in neural networks: thresholds, hysteresis, and neuromodulation of signal-to-noise. Proc Natl Acad Sci USA 86: 1712-1716, 1989.
42. Lederhendler II, Alkon DL. Associatively reduced withdrawal from shadows in Hermissenda: a direct behavioral analog of photoreceptor responses to brief light steps. Behav Neural Biol 47: 227-249, 1987.
43. Lederhendler II, Gart S, Alkon DL. Classical conditioning of Hermissenda: origin of a new response. J Neurosci 6: 1325-1331, 1986.
44. Liu F, Yu Y, Wang W. Signal-to-noise ratio gain in neuronal systems. Phys Rev E Stat Nonlin Soft Matter Phys 63: 051912, 2001.
45. Luk WK, Aihara K. Synchronization and sensitivity enhancement of the Hodgkin-Huxley neurons due to inhibitory inputs. Biol Cybern 82: 455-467, 2000.
46. Mar DJ, Chow CC, Gerstner W, Adams RW, Collins JJ. Noise shaping in populations of coupled model neurons. Proc Natl Acad Sci USA 96: 10450-10455, 1999.
47. Matzel LD, Lederhendler II, Alkon DL. Regulation of short-term associative memory by calcium-dependent protein kinase. J Neurosci 10: 2300-2307, 1990b.
48. Matzel LD, Schreurs BG, Alkon DL. Pavlovian conditioning of distinct components of Hermissenda's responses to rotation. Behav Neural Biol 54: 131-145, 1990a.
49. Mo JL, Blackwell KT. Comparison of Hermissenda type A and type B photoreceptors: response to light as a function of intensity and duration. J Neurosci 23: 8020-8028, 2003.
50. Perkel DH, Bullock TH. Neural coding. Neurosci Res Program Bull 6: 221-343, 1968.
51. Plesser H, Gerstner W. Noise in integrate-and-fire neurons: from stochastic input to escape rates. Neural Comput 12: 367-384, 2000.
52. Read HL, Siegel RM. The origins of aperiodicities in sensory neuron entrainment. Neuroscience 75: 301-314, 1996.
53. Roddey JC, Girish B, Miller JP. Assessing the performance of neural encoding models in the presence of noise. J Comput Neurosci 8: 95-112, 2000.
54. Rogers RF, Talk AC, Matzel LD. Trial-spacing effects in Hermissenda suggest contributions of associative and nonassociative cellular mechanisms. Behav Neurosci 108: 1030-1042, 1994.
55. Sakakibara M, Ikeno H, Usui S, Collin C, Alkon DL. Model of Hermissenda type-B photoreceptors based on principal soma currents. Vision, Memory, and the Temporal Lobe (Proceedings of the Tokyo Symposium on Vision, Memory, and the Temporal Lobe, Tokyo, Japan), edited by Iwai E, Mishkin M. New York: Elsevier, 1989, p. 421-426.
56. Schneidman E, Freedman B, Segev I. Ion channel stochasticity may be critical in determining the reliability and precision of spike timing. Neural Comput 10: 1679-1703, 1998.
57. Schultz LM, Butson CR, Clark GA. Post-light potentiation at type B to A photoreceptor connections in Hermissenda. Neurobiol Learn Mem 76: 7-32, 2001.
58. Schuman EM, Clark GA. Synaptic facilitation at connections of Hermissenda type B photoreceptors. J Neurosci 14: 1613-1622, 1994.
59. Smith BR, Farley J. Computer model of the Hermissenda type B photoreceptor: examination of light-induced responses and learning effects on photoresponses. Soc Neurosci Abstr 813.16, 2006.
60. Steinmetz PN, Manwani A, Koch C. Subthreshold voltage noise due to channel fluctuations in active neuronal membranes. J Comput Neurosci 9: 133-148, 2000.
61. Tabak J, Murphey CR, Moore LE. Parameter estimation methods for single neuron models. J Comput Neurosci 9: 215-236, 2000.
62. Vanier MC, Bower JM. A comparative survey of automated parameter-search methods for compartmental neural models. J Comput Neurosci 7: 149-171, 1999.
63. Wang Y, Chik DT, Wang ZD. Coherence resonance and noise-induced synchronization in globally coupled Hodgkin-Huxley neurons. Phys Rev E Stat Nonlin Soft Matter Phys 61: 740-746, 2000.
64. Werness SA, Fay SD, Blackwell KT, Vogl TP, Alkon DL. Associative learning in a network model of Hermissenda crassicornis. I. Theory. Biol Cybern 68: 125-133, 1992.
65. White JA, Klink R, Alonso A, Kay AR. Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol 80: 262-269, 1998.
66. White JA, Rubinstein JT, Kay AR. Channel noise in neurons. Trends Neurosci 23: 131-137, 2000.
67. Willms AR, Baro DJ, Harris-Warrick RM, Guckheimer J. An improved parameter estimation method for Hodgkin-Huxley models. J Comput Neurosci 6: 145-168, 1999.