Burst firing in sensory systems

Nature Reviews Neuroscience

Volumn 5, Issue 1, 2004, Pages 13-23

  Krahe, Rüdiger ^a   Gabbiani, Fabrizio ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIOR; FEEDBACK SYSTEM; HUMAN; INFORMATION PROCESSING; NERVE CONDUCTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORY SYSTEM; SPIKE;

EID: 0346024189     PISSN: 1471003X     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrn1296     Document Type: Review

References (120)

1. Pike, F. G., Meredith, R. M., Olding, A. W. A. & Paulsen, O. Postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J. Physiol (Lond.) 518, 571-576 (1999).
2. Izhikevich, E. M., Desai, N. S., Walcott, E. C. & Hoppensteadt, F. C. Bursts as a unit of neural information: selective communication via resonance. Trends Neurosci. 26, 161-167 (2003).
3. McCormick, D. A. & Contreras, D. On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol. 63, 815-846 (2001).
4. Crick, F. Function of the thalamic reticular complex: the searchlight hypothesis. Proc. Natl Acad. Sci. USA 81, 4586-4590 (1984). Based, in part, on the results of reference 5, this article presents possible scenarios for the role of bursts in sensory processing.
5. 2+ conductance underlies the switching between tonic and burst firing in thalamic relay neurons.
6. Steriade, M., McCormick, D. A. & Sejnowski, T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679-685 (1993).
7. As in guinea pig dorsal lateral geniculate relay neurons. J. Neurophysiol. 66, 1176-1189 (1991).
8. 2+-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J. Neurosci. 12, 3804-3817 (1992).
9. Zhan, X. J., Cox, C. L., Rinzel, J & Sherman, S. M. Current clamp and modeling studies of low-threshold calcium spikes in cells of the cat's lateral geniculate nucleus. J. Neurophysiol. 81, 2360-2373 (1999).
10. Ramcharan, E. J., Cox, C. L., Zhan, X. J., Sherman, S. M. & Gnadt, J. W. Cellular mechanisms underlying activity patterns in the monkey thalamus during visual behavior. J. Neurophysiol. 84, 1982-1987 (2000).
11. +-dependent mechanism. J. Neurosci. 21, 759-770 (2001).
12. Azouz, R., Jensen, M. S. & Yaari, Y. Ionic basis for spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. (Lond.) 492, 211-223 (1996).
13. Golding, N. L., Jung, H.-Y., Mickus, T. & Spruston, N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J. Neurosci. 19, 8789-8798 (1999).
14. Magee, J. C. & Carruth, M. Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 82, 1895-1901 (1999).
15. Su, H., Alroy, G., Kirson, E. D. & Yaari, Y. Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J. Neurosci. 21, 4173-4182 (2001).
16. Jung, H.-Y., Staff, N. P. & Spruston, N. Action potential bursting in subicular pyramidal neurons is driven by a calcium tail current. J. Neurosci. 21, 3312-3321 (2001).
17. Schwindt, P. & Crill, W. Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. J. Neurophysiol. 81, 1341-1354 (1999).
18. Williams, S. R. & Stuart, G. J. Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J. Physiol. (Lond.) 521, 467-482 (1999).
19. Brumberg, J. C., Nowak, L. G. & McCormick, D. A. Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J. Neurosci. 20, 4829-4843 (2000).
20. Nishimura, Y. et al. Ionic mechanisms underlying burst firing of layer III sensorimotor cortical neurons of the cat: an in vitro slice study. J. Neurophysiol. 86, 771-781 (2001).
21. Lemon, N. & Turner, R. W. Conditional spike backpropagation generates burst discharge in a sensory neuron. J. Neurophysiol. 84, 1519-1530 (2000).
22. + channels to burst threshold in a sensory neuron. J. Neurosci. 21, 125-135 (2001).
23. + current modifies burst discharge by regulating conditional backpropagation of dendritic spikes. J. Neurophysiol. 89, 324-337 (2003).
24. Noonan, L., Doiron, B., Laing, C., Longtin, A. & Turner, R. W. A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. J. Neurosci. 23, 1524-1534 (2003).
25. Amir, R., Michaelis, M. & Devor, M. Burst discharge in primary sensory neurons: triggered by subthreshold oscillations, maintained by depolarizing after potentials. J. Neurosci. 22, 1187-1198 (2002).
26. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367-1395 (1996).
27. Sherman, S. M. & Guillery, R. W. The role of the thalamus in the flow of information to the cortex. Phil. Trans. R. Soc. Lond. B 357, 1695-1708 (2002).
28. Wang, X.-J. & Rinzel, J. in The Handbook of Brain Theory and Neural Networks (ed. Arbib, M. A.) 835-840 (MIT Press, Cambridge, Massachusetts, 2003).
29. Izhikevich, E. M. Neural excitability, spiking and bursting. Int. J. Bifurc. Chaos 10, 1171-1266 (2000). A comprehensive review of the spiking properties of neurons from a dynamic systems perspective presenting a classification of bursting mechanisms.
30. Doiron, B., Laing, C., Longtin, A. & Maler, L. Ghostbursting: a novel neuronal burst mechanism. J. Comput. Neurosci. 12, 5-25 (2002)
31. Laing, C. R. et al. Type 1 burst excitability. J. Comput. Neurosci. 14, 329-342 (2003).
32. Wu, N., Hsiao, C.-S. & Chandler, S. H. Membrane resonance and subthreshold membrane oscillations in mesencephalic V neurons: participants in burst generation. J. Neurosci. 21, 3729-3739 (2001).
33. McCormick, D. A. & Huguenard, J. R. A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68, 1384-1400 (1992).
34. Destexhe, A., Neubig, M., Ulrich, D. & Huguenard, J. Dendritic low-threshold calcium currents in thalamic relay cells. J. Neurosci. 18, 3574-3588 (1998).
35. Munsch, T., Budde, T. & Pape, H.-C. Voltage-activated intracellular calcium transients in thalamic relay cells and interneurons. Neuroreport 8, 2411-2418 (1997).
36. Zhou, Q., Godwin, D. W., O'Malley D. M. & Adams, P. R. Visualization of calcium influx through channels that shape the burst and tonic firing modes of thalamic relay cells. J. Neurophysiol. 77, 2816-2825 (1997).
37. Williams, S. R. & Stuart, G. J. Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J. Neurosci. 20, 1307-1317 (2000).
38. Pinsky, P. F. & Rinzel, J. Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neurosci. 1, 39-60 (1994).
39. Mainen, Z. F. & Sejnowski, T. J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363-366 (1996). Compartmental modelling is used to show that the dendritic structure of neocortical neurons - that is, the size and electrotonic properties of their dendritic arbours - can determine their firing properties.
40. Connors, B. W. & Gutnick, M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99-104 (1990).
41. Mason, A. & Larkman, A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J. Neurosci. 10, 1415-1428 (1990).
42. Gray, C. M. & McCormick, D. A. Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous firing in the visual cortex. Science 274, 109-113 (1996).
43. Nowak, L. G., Azouz, R., Sanchez-Vives, M. V., Gray, C. M. & McCormick, D. A. Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. J. Neurophysiol. 89, 1541-1566 (2003).
44. Wang, X.-J. Fast burst firing and short-term synaptic plasticity: a model of neocortical chattering neurons. Neuroscience 89, 347-362 (1999).
45. Doiron, B., Longtin, A., Turner, R. W. & Maler, L. Model of gamma frequency burst discharge generated by conditional backpropagation. J. Neurophysiol. 86, 1523-1545 (2001).
46. + channels underlies the activity-dependent attentuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J. Neurosci. 17, 6512-6521 (1997).
47. Destexhe, A. Modelling corticothalamic feedback and the gating of the thalamus by the cerebral cortex. J. Physiol. (Paris) 94, 391-410 (2000).
48. Fanselow, E. E., Sameshima, K., Baccala, L. A. & Nicolelis M. A. Thalamic bursting in rats during different awake behavioral states. Proc. Natl Acad. Sci. USA 98, 15330-15335 (2001).
49. Sherman, S. M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122-126 (2001).
50. Destexhe, A. & Sejnowski, T. J. The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity. Phil. Trans. R. Soc. Lond. B 357, 1649-1657 (2002). A modelling study detailing how cortical feedback might differentially affect thalamic relay neurons and thalamic reticular cells.
51. Sillito, A. M. & Jones, H. E. Corticothalamic interactions in the transfer of visual information. Phil. Trans. R. Soc. Lond. B 357, 1739-1752 (2002). A summary of the authors' studies on the effects of visually driven feedback on thalamic processing.
52. Doiron, B., Chacron, M. J., Maler, L., Longtin, A. & Bastian, J. Inhibitory feedback required for network oscillatory responses to communication but not prey stimuli. Nature 421, 539-543 (2003). The spatial characteristics of electrical stimuli, and presumably their behavioural context, are shown to determine neuronal response properties (including bursting) through the action of feedback.
53. Turner, R. W. et al. Oscillatory burst discharge generated through conditional backpropagation of dendritic spikes. J. Physiol. (Paris) 96, 517-530 (2002).
54. Bastian, J. Electrolocation. II. The effects of moving objects and other electrical stimuli on the activities of two categories of posterior lateral line lobe cells in Apteronotus albifrons. J. Comp Physiol. A 144, 481-494 (1981).
55. Bastian, J., Chacron, M. J. & Maler, L. Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J. Neurosci. 22, 4577-4590 (2002).
56. Hubel, D. H. & Wiesel, T. N. Integrative action in the cat's lateral geniculate body. J. Physiol. (Lond.) 155, 385-398 (1961).
57. Shumway C. Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J. Neurosci. 9, 4388-4399 (1989).
58. Maler, L., Sas, E. K. & Rogers, J. The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (Gymnotidae): dendritic differentiation and synaptic specificity in a simple cortex. J. Comp. Neurol. 195, 87-139 (1981).
59. Berman, N. J. & Maler, L. 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 (1999).
60. Erşir, A., Van Horn, S. C., Bickford, M. E. & Sherman, S. M. Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: a comparison with corticogeniculate terminals. J. Comp. Neurol. 377, 535-549 (1997).
61. Maler, L. The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J. Comp. Neurol. 183, 323-363 (1979).
62. Updyke, B. V. Topographic organization of the projections from ccrtical areas 17, 18 and 19 onto the thalamus, pretectum and superior colliculus in the cat. J. Comp. Neurol. 173, 81-122 (1977)
63. Bratton, B. & Bastian, J. Descending control of electroreception. II. Properties of nucleus praeeminentialis neurons projecting directly to the electrosensory lateral line lobe. J. Neurosci. 10, 1241-1253 (1990).
64. Sas, E. & Maler, L. The nucleus praeeminentialis: a Golgi study of a feedback center in the electrosensory system of gymnotid fish. J. Comp. Neurol. 221, 127-144 (1983).
65. Sas, E. & Maler, L. The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anat. Embryol. 177, 55-79 (1987).
66. Maler, L & Mugnaini, E. Correlating γ-aminobutyric acidergic circuits and sensory function in the electrosensory lateral line lobe of a gymnotiform fish. J. Comp. Neurol. 345, 224-252 (1994).
67. Wiest, M. C. & Nicolelis, M. A. Behavioral detection of tactile stimuli during 7-12 Hz cortical oscillations in awake rats. Nature Neurosci. 6, 913-914 (2003).
68. Bastian, J. & Nguyenkim, J. Dendritic modulation of burst-like firing in sensory neurons. J. Neurophysiol. 85, 10-22 (2001).
69. Krahe, R., Kreiman, G., Gabbiani, F., Koch, C. & Metzner, W. Stimulus encoding and feature extraction by multiple sensory neurons. J. Neurosci. 22, 2374-2382 (2002).
70. Weyand, T. G., Boudreaux, M. & Guido, W. Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J. Neurophysiol. 85, 1107-1118 (2001).
71. Allen, C. & Stevens, C. F. An evaluation of causes for unreliability of synaptic transmission. Proc. Natl Acad. Sci. USA 91, 10380-10383 (1994)
72. Thomson, A. M. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J. Physiol. (Lond.) 502, 131-147 (1997).
73. Lisman, J. E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20, 38-43 (1997).
74. Snider, R. K., Kabara, J. F., Roig, B. R. & Bonds, A. B. Burst firing and modulation of functional connectivity in cat striate cortex. J. Neurophysiol. 80, 730-744 (1998).
75. Csicsvari, J., Hirase, H., Czurko, A. & Buzsáki, G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21, 179-189 (1998).
76. Gil, Z., Connors, B. W. & Amitai, Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19, 679-686 (1997).
77. Gil, Z., Connors, B. W. & Amitai, Y. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23, 385-397 (1999).
78. Chung, S., Li, X. & Nelson, S. B. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo Neuron 34, 437-446 (2002).
79. Swadlow, H. A. & Gusev, A. G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nature Neurosci. 4, 402-408 (2001). Bursts of thalamic relay cells are shown to have increased efficacy in eliciting spikes in cortical target neurons in vivo. The gain in efficacy is correlated with the silent period preceding the bursts.
80. Usrey, W. M., Alonso, J.-M. & Reid, R. C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. J. Neurosci. 20, 5461-5467 (2000).
81. Stratford, K. J., Tarczy-Hornoch, K., Martin, K. A. C., Bannister, N. J. & Jack, J. J. B. Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382, 258-261 (1996).
82. Eggermont, J. J. & Smith, G. M. Burst-firing sharpens frequency-tuning in primary auditory cortex. Neuroreport 7, 753-757 (1996).
83. Cattaneo, A., Maffei, L. & Morrone, C. Patterns in the discharge of simple and complex visual cortical cells. Proc. R. Soc. Lond. B 212, 279-297 (1981). Contains an early analysis correlating bursts to neuronal tuning in complex cells of cat primary visual cortex.
84. Livingstone, M. S., Freeman, D. C. & Hubel, D. H. Visual responses in V1 of freely viewing monkeys. Cold Spring Harb. Symp. Quant. Biol. 61, 27-37 (1996).
85. Ferster, D. & Jagadeesh, B. EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording J. Neurosci. 12, 1262-1274 (1992).
86. Frégnac, Y., Bringuier, V., Chavane, F., Glaeser, L. & Lorenceau, J. An intracellular study of space and time representation in primary visual cortical receptive fields. J. Physiol. (Paris) 90, 189-197 (1996).
87. Carandini, M. & Ferster, D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470-484 (2000).
88. Volgushev, M., Pernberg, J. & Eysel, U. T. Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex. Eur. J. Neurosci. 12, 257-263 (2000).
89. Peña, J. L. & Konishi, M. From postsynaptic potentials to spikes in the genesis of auditory spatial receptive fields. J. Neurosci. 22, 5652-5658 (2002)
90. Mukherjee, P. & Kaplan, E. Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. J. Neurophysiol. 74, 1222-1243 (1995).
91. McCarley, R. W., Benoit, O. & Barrionuevo, G. Lateral geniculate nucleus unitary discharge in sleep and waking: state- and rate-specific aspects. J. Neurophysiol. 50, 798-818 (1983).
92. Guido, W. & Weyand, T. Burst responses in thalamic relay cells of the awake behaving cat. J. Neurophysiol. 74, 1782-1786 (1995).
93. Edeline, J. M., Manunta, Y. & Hennevin, E. Auditory thalamus neurons during sleep: changes in frequency selectivity, threshold, and receptive fold size. J. Neurophysiol. 84, 934-952 (2000).
94. Ramcharan, E. J., Gnadt, J. W. & Sherman, S. M. Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis. Neurosci. 17, 55-62 (2000).
95. Ramcharan, E. J., Gnadt, J. W. & Sherman, S. M. The effects of saccadic eye movements on the activity of geniculate relay neurons in the monkey. Vis. Neurosci. 18, 253-258 (2001).
96. Ramcharan, E. J., Gnadt, J. W. & Sherman, S. M. Single-unit recording in the lateral geniculate nucleus of the awake behaving monkey. Methods 30, 142-151 (2003).
97. Martinez-Conde, S., Macknik, S. L. & Hubel, D. H. 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 (2002). A study showing that microsaccade-driven bursts in LGN might indicate stimulus visibility, whereas burst size in V1 neurons might serve as a neural code for stimulus optimality.
98. 2+ conductance. J. Neurophysiol. 68, 2185-2198 (1992).
99. Reinagel, P., Godwin, D., Sherman, S. M. & Koch, C. Encoding of visual information by LGN bursts. J. Neurophysiol. 81, 2558-2569 (1999).
100. Guido, W., Lu, S. M., Vaughan, J. W., Godwin, D. W. & Sherman, S. M. Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode. Vis. Neurosci. 12, 723-741 (1995). The first application of signal detection methods to the analysis of the information conveyed by the response modes of LGN neurons. Suggests that the burst mode supports signal detection better than the tonic mode.
101. Wessel, R., Kcch, C. & Gabbiani, F. Coding of time-varying electric field amplitude modulations in a wave-type electric fish. J. Neurophysiol. 75, 2280-2293 (1996).
102. Metzner W., Koch, C., Wessel, R. & Gabbiani, F. Feature extraction by burst-like spike patterns in multiple sensory maps. J. Neurosci. 18, 2283-2300 (1998). Demonstrates a transformation between the encoding of stimulus detail and the extraction of stimulus features by bursts at two successive stages of the electrosensory system in weakly electric fish.
103. Gabbiani, F., Metzner, W., Wessel, R. & Koch, C. From stimulus encoding to feature extraction in weakly electric fish. Nature 384, 564-567 (1996).
104. Kreiman, G., Krahe, R., Metzner, W., Koch, C. & Gabbiani, F. Robustness and variability of neuronal coding by amplitude-sensitive afferents in the weakly electrc fish Eigenmannia. J. Neurophysiol. 84, 189-204 (2000).
105. Chacron, M. J., Longtin, A. & Maler, L. Negative interspike interval correlations increase the neuronal capacity for encoding time-dependent stimull. J. Neurosci. 21, 5328-5343 (2001).
106. Chacron, M. J., Doiron, B., Maler, L., Longtin, A. & Bastian, J. Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423, 77-61 (2003).
107. Lewicki, M. S. & Konishi, M. Mechanisms underlying the sensitivity of songbird forebrain neurons to temporal order. Proc. Natl Acad. Sci. USA 92, 5582-5586 (1995).
108. Markram, H., Wang, Y. & Tsodyks, M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc. Natl. Acad. Sci. USA 95, 5323-5328 (1998).
109. Hutcheon, B. & Yarom, Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216-222 (2000).
110. Kepecs, A., Wang, X.-J. & Lisman, J. Bursting neurons signal input slope. J. Neurosci. 22, 9053-9062 (2002).
111. Kepecs, A. & Lisman, J. Information encoding and computation with spikes and bursts. Network Comput. Neural. Syst. 14, 103-118 (2003).
112. DeBusk, B. C., DeBruyn, E. J., Snider, R. K., Kabara, J. F. & Bonds, A. B. Stimulus-dependent modulation of spike burst length in cat stnate cortical cells. J. Neurophysiol. 78, 199-213 (1997)
113. Middlebrooks, J. C., Clock, A. E., Xu, L. & Green, D. M. A panoramic code for sound location by cortical neurons Science 264, 842-844 (1994).
114. Furukawa, S. & Middlebrooks, J. C. Cortical representation of auditory space: Information-bearing features of spikes. J. Neurophysiol. 87, 1749-1762 (2002).
115. Hagedorn, M. & Halligenberg, W. Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim. Behav. 33, 254-265 (1985)
116. Nelson, M. E. & MacIver, M. A. Prey capture in the weakly electric fish Apteronotus albifrons: Sensory acquisition strategies and electrosensory consequences. J. Exp. Biol. 202, 1195-1203 (1999).
117. Gabbiani, F. A switch for oscillatory bursting. Nature Neurosci. 6, 212-213 (2003).
118. Sherman, S. M. in Thalami Networks for Relay and Modulation (eds Minciacchi, D., Molinari, M., Macchi, G. & Jones, E. G.) 61-79 (Pergamon, Tarrytown, New York, 1993).
119. Thomson, A. M. Molecular frequency filters at central synapses. Prog. Neurobiol. 62, 159-196 (2000).
120. Gabbiani, F. & Metzner, W. Encoding and processing of sensory information in neural spike trains. J. Exp. Biol. 202, 1267-1279 (1999).