Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Burst firing in sensory systems

Key Points

  • Burst firing — the intermittent discharge of rapid action-potential sequences — is a prominent feature of many sensory neurons. Its functional role is not fully understood, in spite of the considerable progress that has been made in the past 20 years. This review draws together recent findings on the biophysical mechanisms of burst firing, its control through feedback from higher brain centres, and its potential role in sensory information transmission.

  • In vitro studies and compartmental modelling demonstrate that bursting relies on intrinsic ionic mechanisms that couple the fast process of action potential generation to slower processes that govern burst occurrence and duration. In compact neurons, both these slow and fast mechanisms are located at the soma. In neurons with extensive dendritic structures, the fast and slow processes can also be distributed over the dendrites, leading to qualitatively different mechanisms of bursting.

  • The occurrence of bursts does not only rely on strong excitation by sensory inputs and intrinsic cellular mechanisms. Bursts also seem to be gated by inputs from additional brain areas. In neurons of the mammalian thalamus for example, brainstem inputs convey information on the level of vigilance of the animal, and drowsiness or sleep states might result in large-scale synchronized bursting. By contrast, burst probability is low during wakefulness. Cortical feedback onto the same neurons, on the other hand, might be able to gate sensory-driven bursting during wakefulness.

  • In the hindbrain of weakly electric fish, synchronized burst responses seem to be gated by the behavioural context of sensory stimuli. Spatially extended stimuli that mimic communication with conspecifics favour synchronized firing patterns and increase periodic (oscillatory) bursting. By contrast, spatially localized stimuli that mimic small prey lead to non-oscillatory responses with low burst probability. The shift between these two response modes can be explained by the level of activation of a spatially diffuse inhibitory feedback pathway, which is strongly activated only by large-scale stimuli.

  • Support for a distinct role of bursts in sensory systems comes from two main sources. First, bursts can increase the reliability of synaptic transmission. At facilitating synapses, this presumably occurs through accumulation of Ca2+ in the presynaptic terminal during high frequency firing. At depressing synapses of the thalamocortical system, the silent period preceding bursts acts to relieve depression and so enhances synaptic efficacy. Second, bursts occur as responses to sensory stimulation in alert animals and carry distinct information about these stimuli. In some systems, bursts improve the signal-to-noise ratio of sensory responses. In others, such as the electrosensory system of weakly electric fish, bursts might be involved in the detection of specific, behaviourally relevant stimulus features.

Abstract

Neurons that fire high-frequency bursts of spikes are found in various sensory systems. Although the functional implications of burst firing might differ from system to system, bursts are often thought to represent a distinct mode of neuronal signalling. The firing of bursts in response to sensory input relies on intrinsic cellular mechanisms that work with feedback from higher centres to control the discharge properties of these cells. Recent work sheds light on the information that is conveyed by bursts about sensory stimuli, on the cellular mechanisms that underlie bursting, and on how feedback can control the firing mode of burst-capable neurons, depending on the behavioural context. These results provide strong evidence that bursts have a distinct function in sensory information transmission.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Biophysical mechanisms of burst generation.
Figure 2: Response properties and simplified connectivity diagram of thalamic relay and electrosensory lateral-line lobe (ELL) pyramidal cells.
Figure 3: Network control of bursting in the lateral geniculate nucleus (LGN) and electrosensory lateral-line lobe (ELL).
Figure 4: Role of facilitation and depression in burst filtering.
Figure 5: Burst firing improves the signal-to-noise ratio of cortical sensory responses.
Figure 6: Transformation from stimulus encoding to feature extraction in weakly electric fish.

Similar content being viewed by others

References

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  3. McCormick, D. A. & Contreras, D. On the cellular and network bases of epileptic seizures. Annu. Rev. Physiol. 63, 815–846 (2001).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Llinás, R. L. & Jahnsen, H. Electrophysiology of mammalian thalamic neurons in vitro. Nature 297, 406–408 (1982). Demonstrates that the activation/de-inactivation kinetics of a low-threshold Ca2+ conductance underlies the switching between tonic and burst firing in thalamic relay neurons.

    Article  PubMed  Google Scholar 

  6. Steriade, M., McCormick, D. A. & Sejnowski, T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679–685 (1993).

    Article  CAS  PubMed  Google Scholar 

  7. McCormick, D. A. Functional properties of a slowly inactivating potassium current IAs in guinea pig dorsal lateral geniculate relay neurons. J. Neurophysiol. 66, 1176–1189 (1991).

    Article  CAS  PubMed  Google Scholar 

  8. Huguenard, J. R. & Prince, D. A. A novel T-type current underlies prolonged Ca2+-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J. Neurosci. 12, 3804–3817 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  11. D'Angelo, E. et al. Theta-frequency bursting and resonance in cerebellar granule cells: experimental evidence and modeling of a slow K+-dependent mechanism. J. Neurosci. 21, 759–770 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  21. Lemon, N. & Turner, R. W. Conditional spike backpropagation generates burst discharge in a sensory neuron. J. Neurophysiol. 84, 1519–1530 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Rashid, A. J., Morales, E., Turner, R. W. & Dunn, R. J. The contribution of dendritic Kv3 K+ channels to burst threshold in a sensory neuron. J. Neurosci. 21, 125–135 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Doiron, B., Noonan, L., Lemon, N. & Turner, R. W. Persistent Na+ current modifies burst discharge by regulating conditional backpropagation of dendritic spikes. J. Neurophysiol. 89, 324–337 (2003).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Amir, R., Michaelis, M. & Devor, M. Burst discharge in primary sensory neurons: triggered by subthreshold oscillations, maintained by depolarizing afterpotentials. J. Neurosci. 22, 1187–1198 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Google Scholar 

  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.

    Article  Google Scholar 

  30. Doiron, B., Laing, C., Longtin, A. & Maler, L. Ghostbursting: a novel neuronal burst mechanism. J. Comput. Neurosci. 12, 5–25 (2002).

    Article  PubMed  Google Scholar 

  31. Laing, C. R. et al. Type I burst excitability. J. Comput. Neurosci. 14, 329–342 (2003).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. McCormick, D. A. & Huguenard, J. R. A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68, 1384–1400 (1992).

    Article  CAS  PubMed  Google Scholar 

  34. Destexhe, A., Neubig, M., Ulrich, D. & Huguenard, J. Dendritic low-threshold calcium currents in thalamic relay cells. J. Neurosci. 18, 3574–3588 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Munsch, T., Budde, T. & Pape, H. -C. Voltage-activated intracellular calcium transients in thalamic relay cells and interneurons. Neuroreport 8, 2411–2418 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  40. Connors, B. W. & Gutnick, M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13, 99–104 (1990).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  44. Wang, X. -J. Fast burst firing and short-term synaptic plasticity: a model of neocortical chattering neurons. Neuroscience 89, 347–362 (1999).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  46. Colbert, C. M., Magee, J. C., Hoffman, D. A. & Johnston, D. Slow recovery from inactivation of Na+ channels underlies the activity-dependent attentuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J. Neurosci. 17, 6512–6521 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Destexhe, A. Modelling corticothalamic feedback and the gating of the thalamus by the cerebral cortex. J. Physiol. (Paris) 94, 391–410 (2000).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Sherman, S. M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122–126 (2001).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  53. Turner, R. W. et al. Oscillatory burst discharge generated through conditional backpropagation of dendritic spikes. J. Physiol. (Paris) 96, 517–530 (2002).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hubel, D. H. & Wiesel, T. N. Integrative action in the cat's lateral geniculate body. J. Physiol. (Lond.) 155, 385–398 (1961).

    Article  CAS  Google Scholar 

  57. Shumway, C. Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J. Neurosci. 9, 4388–4399 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  61. Maler, L. The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J. Comp. Neurol. 183, 323–363 (1979).

    Article  CAS  PubMed  Google Scholar 

  62. Updyke, B. V. Topographic organization of the projections from cortical areas 17, 18 and 19 onto the thalamus, pretectum and superior colliculus in the cat. J. Comp. Neurol. 173, 81–122 (1977).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  68. Bastian, J. & Nguyenkim, J. Dendritic modulation of burst-like firing in sensory neurons. J. Neurophysiol. 85, 10–22 (2001).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  71. Allen, C. & Stevens, C. F. An evaluation of causes for unreliability of synaptic transmission. Proc. Natl Acad. Sci. USA 91, 10380–10383 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  73. Lisman, J. E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20, 38–43 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  76. Gil, Z., Connors, B. W. & Amitai, Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19, 679–686 (1997).

    Article  CAS  PubMed  Google Scholar 

  77. Gil, Z., Connors, B. W. & Amitai, Y. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23, 385–397 (1999).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  82. Eggermont, J. J. & Smith, G. M. Burst-firing sharpens frequency-tuning in primary auditory cortex. Neuroreport 7, 753–757 (1996).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  87. Carandini, M. & Ferster, D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470–484 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  92. Guido, W. & Weyand, T. Burst responses in thalamic relay cells of the awake behaving cat. J. Neurophysiol. 74, 1782–1786 (1995).

    Article  CAS  PubMed  Google Scholar 

  93. Edeline, J. M., Manunta, Y. & Hennevin, E. Auditory thalamus neurons during sleep: changes in frequency selectivity, threshold, and receptive field size. J. Neurophysiol. 84, 934–952 (2000).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Lu, S. M., Guido, W. & Sherman, S. M. Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. J. Neurophysiol. 68, 2185–2198 (1992).

    Article  CAS  PubMed  Google Scholar 

  99. Reinagel, P., Godwin, D., Sherman, S. M. & Koch, C. Encoding of visual information by LGN bursts. J. Neurophysiol. 81, 2558–2569 (1999).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  101. Wessel, R., Koch, C. & Gabbiani, F. Coding of time-varying electric field amplitude modulations in a wave-type electric fish. J. Neurophysiol. 75, 2280–2293 (1996).

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Gabbiani, F., Metzner, W., Wessel, R. & Koch, C. From stimulus encoding to feature extraction in weakly electric fish. Nature 384, 564–567 (1996).

    Article  CAS  PubMed  Google Scholar 

  104. Kreiman, G., Krahe, R., Metzner, W., Koch, C. & Gabbiani, F. Robustness and variability of neuronal coding by amplitude-sensitive afferents in the weakly electric fish Eigenmannia. J. Neurophysiol. 84, 189–204 (2000).

    Article  CAS  PubMed  Google Scholar 

  105. Chacron, M. J., Longtin, A. & Maler, L. Negative interspike interval correlations increase the neuronal capacity for encoding time-dependent stimuli. J. Neurosci. 21, 5328–5343 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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, 77–81 (2003).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Hutcheon, B. & Yarom, Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216–222 (2000).

    Article  CAS  PubMed  Google Scholar 

  110. Kepecs, A., Wang, X. -J. & Lisman, J. Bursting neurons signal input slope. J. Neurosci. 22, 9053–9062 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Kepecs, A. & Lisman, J. Information encoding and computation with spikes and bursts. Network Comput. Neural. Syst. 14, 103–118 (2003).

    Article  Google Scholar 

  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 striate cortical cells. J. Neurophysiol. 78, 199–213 (1997).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  114. Furukawa, S. & Middlebrooks, J. C. Cortical representation of auditory space: Information-bearing features of spikes. J. Neurophysiol. 87, 1749–1762 (2002).

    Article  PubMed  Google Scholar 

  115. Hagedorn, M. & Heiligenberg, W. Court and spark: electric signals in the courtship and mating of gymnotoid electric fish. Anim. Behav. 33, 254–265 (1985).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  117. Gabbiani, F. A switch for oscillatory bursting. Nature Neurosci. 6, 212–213 (2003).

    Article  CAS  PubMed  Google Scholar 

  118. Sherman, S. M. in Thalamic Networks for Relay and Modulation (eds Minciacchi, D., Molinari, M., Macchi, G. & Jones, E. G.) 61–79 (Pergamon, Tarrytown, New York, 1993).

    Book  Google Scholar 

  119. Thomson, A. M. Molecular frequency filters at central synapses. Prog. Neurobiol. 62, 159–196 (2000).

    Article  CAS  PubMed  Google Scholar 

  120. Gabbiani, F. & Metzner, W. Encoding and processing of sensory information in neural spike trains. J. Exp. Biol. 202, 1267–1279 (1999).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the provision of figure material by J. Bastian, E. D'Angelo and B. Doiron. We also would like to thank L. Chen for help with electric field modelling, and B. Boudreau and D. Sparks for critically reading the manuscript. F.G. is an Alfred P. Sloan Fellow. Funding from NIMH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabrizio Gabbiani.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Gabbiani's Laboratory homepage

Glossary

SLOW-WAVE SLEEP

A phase of the sleep cycle that is characterized by the appearance of slow oscillations in the electroencephalogram.

COMPARTMENTAL MODELLING

A computer modelling technique that breaks a neuron down into small electrical compartments and can simulate the propagation of electrical signals inside the neuron and across its membrane surface.

SOMATOSENSORY SYSTEM

The system that mediates the sensation of touch, temperature, pain and movement of the joints.

VENTROBASAL COMPLEX OF THE THALAMUS

Subdivision of the thalamus that relays somatosensory information to the cortex.

MICROSACCADES

Small and abrupt involuntary eye movements that occur during fixation of an object and last for only a brief period of time.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krahe, R., Gabbiani, F. Burst firing in sensory systems. Nat Rev Neurosci 5, 13–23 (2004). https://doi.org/10.1038/nrn1296

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn1296

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing