Parallel Processing of Sensory Input by Bursts and Isolated Spikes

Journal of Neuroscience

Volumn 24, Issue 18, 2004, Pages 4351-4362

  Oswald, Anne Marie M ^a   Chacron, Maurice J ^a   Doiron, Brent ^a   Bastian, Joseph ^b   Maler, Leonard ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Burst; Dendritic backpropagation; Feature detection; Neural code; Sensory systems; Stimulus estimation

Indexed keywords

ANIMAL TISSUE; ARTICLE; BEHAVIOR; BIOPHYSICS; BRAIN SLICE; BURST FIRING; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INFORMATION SYSTEM; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORY STIMULATION; SENSORY SYSTEM ELECTROPHYSIOLOGY; SIGNAL PROCESSING; SPIKE; STIMULUS; STIMULUS RESPONSE;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; COMPUTER SIMULATION; ELECTRIC STIMULATION; GYMNOTIFORMES; MODELS, NEUROLOGICAL; NORMAL DISTRIBUTION; PYRAMIDAL CELLS; SIGNAL PROCESSING, COMPUTER-ASSISTED;

EID: 2342668030     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0459-04.2004     Document Type: Article

References (54)

1. Bastian J (1982) Vision and electroreception: integration of sensory information in the optic tectum of the weakly electric fish Apteronotus albifrons. J Comp Physiol 147:287-297.
2. Bastian J (1996a) Plasticity in an electrosensory system. I. General features of a dynamic sensory filter. J Neurophysiol 76:2483-2496.
3. Bastian J (1996b) Plasticity in an electrosensory system. II. Postsynaptic events associated with a dynamic sensory filter. J Neurophysiol 76:2497-2507.
4. Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85:10-22.
5. Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22:4577-4590.
6. Bastian J, Chacron MJ, Maler L (2004) Plastic and non plastic cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41:767-779.
7. Bell CC, Maler L (2004) Central neuroanatomy of electrosensory systems in fish. In: Evolution of the vertebrate auditory system, Vol 22 (Manley GA, Popper AN, Fay RR, eds). Berlin: Springer.
8. Berman NJ, Maler L (1998) Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish. J Neurophysiol 80:3173-3196.
9. Berman NJ, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202:1243-1253.
10. Berman NJ, Plant J, Turner P, Maler L (1997) Excitatory amino acid transmission at a feedback pathway in the electrosensory system. J Neurophysiol 78:1869-1881.
11. Borst A, Haag J (2001) Effects of mean firing on neural information rate. J Comput Neurosci 10:213-221.
12. Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423:77-81.
13. Debusk BC, Debruyn EJ, Snider RK, Kabara JF, Bonds AB (1997) Stimulus-dependent modulation of spike burst length in cat striate cortical cells. J Neurophysiol 78:199-213.
14. Doiron B, Longtin A, Turner RW, Maler L (2001) Model of gamma frequency burst discharge generated by conditional backpropagation. J Neurophysiol 86:1523-1545.
15. Doiron B, Laing C, Longtin A, Maler L (2002) Ghostbursting: a novel neuronal burst mechanism. J Comput Neurosci 12:5-25.
16. Doiron B, Chacron M, Maler L, Longtin A, Bastian J (2003a) Inhibitory feedback required for network oscillatory responses but not prey stimuli. Nature 421:539-543.
17. Doiron B, Noonan L, Lemon N, Turner RW (2003b) Persistent Na+ current modifies burst discharge by regulating conditional backpropagation of dendritic spikes. J Neurophysiol 89:324-337.
18. Eggermont JJ (1998) Is there a neural code? Neurosci Biobehav Rev 22:355-370.
19. Fortune ES, Rose GJ (1997) Passive and active membrane properties contribute to the temporal filtering properties of midbrain neurons in vivo. J Neurosci 17:3815-3825.
20. Fortune ES, Rose GJ (2001) Short-term synaptic plasticity as a temporal filter. Trends Neurosci 24:381-385.
21. Gabbiani F, Koch C (1998) Principles of spike train analysis. In: Methods in neuronal modeling (Koch C, Segev I, eds), pp 313-360. Cambridge, MA: MIT.
22. Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384:564-567.
23. Heiligenberg W, Keller CH, Metzner W, Kawasaki M (1991) Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: detection and processing of electric signals in social communication. J Comp Physiol A 169:151-164.
24. Herrington J, Newton KR, Bookman RJ (1995) B PULSE CONTROL V4.5: IGOR XOPS for patch clamp data acquisition and capacitance measurements. Miami, FL.
25. Izhikevich EM, Desai NS, Walcott EC, Hoppensteadt FC (2003) Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci 26:161-167.
26. Keat J, Reinagel P, Reid RC, Meister M (2001) Predicting every spike: a model for the responses of visual neurons. Neuron 30:803-817.
27. Kepecs A, Lisman J (2003) Information encoding and computation with spikes and bursts. Network 14:103-118.
28. Kepecs A, Wang X-J, Lisman J (2002) Bursting neurons signal input slope. J Neurosci 22:9053-9062.
29. Koch C (1999) Biophysics of computation: information processing in single neurons. New York: Oxford UP.
30. Koch C, Segev I (1999) The Hodgkin-Huxley model of action potential generation. In: Biophysics of computation (Stryker M, ed). New York: Oxford UP.
31. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Neurosci 5:13-23.
32. Laing CR, Longtin A (2003) Periodic forcing of a model sensory neuron. Phys Rev E Stat Nonlin Soft Matter Phys 67:051928.
33. Laing CR, Doiron B, Longtin A, Noonan L, Turner RW, Maler L (2003) Type 1 burst excitability. J Comput Neurosci 14:329-342.
34. Lemon N, Turner RW (2000) Conditional spike backpropagation generates burst discharge in a sensory neuron. J Neurophysiol 84:1519-1530.
35. Lestienne R (2001) Spike timing, synchronization and information processing on the sensory side of the central nervous system. Prog Neurobiol 65:545-591.
36. Lisman J (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43.
37. 2+ conductance. J Neurophysiol 68:2185-2198.
38. 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.
39. 2+ entry through the N-methyl-D-aspartate channel. Proc Natl Acad Sci USA 91:8170-8174.
40. Martinez-Conde S, Macknik S, Hubel D (2002) The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proc Natl Acad Sci USA 99:13920-13925.
41. McCormick DA, Huguenard JR (1992) A model of the electrophysiological properties of thalamocortical relay neurons. J Neurophysiol 68:1384-1400.
42. Metzner W, Koch C, Wessel R, Gabbiani F (1998) Feature extraction by burst-like spike patterns in multiple sensory maps. J Neurosci 18:2283-2300.
43. Mukherjee P, Kaplan E (1995) Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. J Neurophysiol 74:1222-1243.
44. Noonan L, Doiron B, Laing C, Longtin A, Turner RW (2003) A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. J Neurosci 23:1524-1534.
45. Reinagel P, Godwin D, Sherman M, Koch C (1999) Encoding of visual information by LGN bursts. J Neurophysiol 81:2558-2569.
46. Rieke F, Warland D, de Ruyter van Steveninck RR, Bialek W (1997) Spikes: exploring the neural code. Cambridge, MA: MIT.
47. Roddey JC, Girish B, Miller JP (2000) Assessing the performance of neural encoding models in the presence of noise. J Comput Neurosci 8:95-112.
48. Rolls ET, Tovee MJ (1995) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J Neurophysiol 73:713-726.
49. Sherman SM (2001) Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24:122-126.
50. Smith GD, Cox CL, Sherman M, Rinzel J (2000) Fourier analysis of sinusoidally driven thalamocortical relay neurons and a minimal integrate-and-fire-or-burst model. J Neurophysiol 83:588-610.
51. Turner RW, Maler L, Deerinick T, Levinson SR, Ellisman MH (1994) TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron. J Neurosci 14:6453-6471.
52. Turner RW, Plant JR, Maler L (1996) Oscillatory and burst discharge across electrosensory topographic maps. J Neurophysiol 76:2364-2382.
53. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273-1276.
54. Zupanc GKH, Maler L (1993) Evoked chirping in the weakly electric fish Apteronotus leptorhynchus: a quantitative biophysical analysis. Can J Zool 71:2301-2310.