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.

  • Article
  • Published:

Synaptic background activity controls spike transfer from thalamus to cortex

Nature Neuroscience volume 8, pages 1760–1767 (2005)Cite this article

Abstract

Characterizing the responsiveness of thalamic neurons is crucial to understanding the flow of sensory information. Typically, thalamocortical neurons possess two distinct firing modes. At depolarized membrane potentials, thalamic cells fire single action potentials and faithfully relay synaptic inputs to the cortex. At hyperpolarized potentials, the activation of T-type calcium channels promotes burst firing, and the transfer is less accurate. Our results suggest that this duality no longer holds if synaptic background activity is taken into account. By injecting stochastic conductances into guinea-pig thalamocortical neurons in slices, we show that the transfer function of these neurons is strongly influenced by conductance noise. The combination of synaptic noise with intrinsic properties gives a global responsiveness that is more linear, mixing single-spike and burst responses at all membrane potentials. Because in thalamic neurons, background synaptic input originates mainly from cortex, these results support a determinant role of corticothalamic feedback during sensory information processing.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: The influence of conductance (g) noise changes the transfer function of thalamocortical cells recorded in vitro.
Figure 2: Voltage and frequency dependence of the response gain of thalamocortical cells, without noise.
Figure 3: Influence of noise on voltage and frequency dependence of gain.
Figure 4: Physiologically realistic Poisson-distributed inputs.
Figure 5: Noise increases occurrence of bursts at resting potential.
Figure 6: Noise mixes single-spike and burst responses of thalamocortical neurons.

Similar content being viewed by others

References

  1. Erisir, A., Van Horn, S.C. & Sherman, S.M. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc. Natl. Acad. Sci. USA 94, 1517–1520 (1997).

    Article  CAS  Google Scholar 

  2. Van Horn, S.C., Erisir, A. & Sherman, S.M. Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J. Comp. Neurol. 416, 509–520 (2000).

    Article  CAS  Google Scholar 

  3. Sherman, S.M. & Koch, C. The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp. Brain Res. 63, 1–20 (1986).

    Article  CAS  Google Scholar 

  4. Koch, C. The action of the corticofugal pathway on sensory thalamic nuclei: a hypothesis. Neuroscience 23, 399–406 (1987).

    Article  CAS  Google Scholar 

  5. Ahissar, E., Haidarliu, S. & Zacksenhouse, M. Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. Proc. Natl. Acad. Sci. USA 94, 11633–11638 (1997).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Sillito, A.M. & Jones, H.E. Corticothalamic interactions in the transfer of visual information. Phil. Trans. R. Soc. Lond. B 357, 1739–1752 (2002).

    Article  Google Scholar 

  8. McCormick, D.A. & Bal, T. Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 20, 185–215 (1997).

    Article  CAS  Google Scholar 

  9. Jahnsen, H. & Llinas, R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. (Lond.) 349, 205–226 (1984).

    Article  CAS  Google Scholar 

  10. Llinas, R.R. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242, 1654–1664 (1988).

    Article  CAS  Google Scholar 

  11. Le Masson, G., Renaud-Le Masson, S., Debay, D. & Bal, T. Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 417, 854–858 (2002).

    Article  CAS  Google Scholar 

  12. Steriade, M. Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol. 86, 1–39 (2001).

    Article  CAS  Google Scholar 

  13. Destexhe, A., Rudolph, M. & Pare, D. The high-conductance state of neocortical neurons in vivo. Nat. Rev. Neurosci. 4, 739–751 (2003).

    Article  CAS  Google Scholar 

  14. Ho, N. & Destexhe, A. Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J. Neurophysiol. 84, 1488–1496 (2000).

    Article  CAS  Google Scholar 

  15. Anderson, J.S., Lampl, I., Gillespie, D.C. & Ferster, D. The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290, 1968–1972 (2000).

    Article  CAS  Google Scholar 

  16. Chance, F.S., Abbott, L.F. & Reyes, A.D. Gain modulation from background synaptic input. Neuron 35, 773–782 (2002).

    Article  CAS  Google Scholar 

  17. Shu, Y., Hasenstaub, A., Badoual, M., Bal, T. & McCormick, D.A. Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J. Neurosci. 23, 10388–10401 (2003).

    Article  CAS  Google Scholar 

  18. Larkum, M.E., Senn, W. & Luscher, H.R. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14, 1059–1070 (2004).

    Article  Google Scholar 

  19. Contreras, D., Timofeev, I. & Steriade, M. Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J. Physiol. 494, 251–264 (1996).

    Article  CAS  Google Scholar 

  20. Wilson, J.R., Friedlander, M.J. & Sherman, S.M. Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proc. R. Soc. Lond. B 221, 411–436 (1984).

    Article  CAS  Google Scholar 

  21. Liu, X.B., Honda, C.N. & Jones, E.G. Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J. Comp. Neurol. 352, 69–91 (1995).

    Article  CAS  Google Scholar 

  22. 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 

  23. Steriade, M., Jones, E.G. & McCormick, D.A. Thalamus Vol. 1 (Elsevier, Amsterdam, 1997).

    Google Scholar 

  24. 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  Google Scholar 

  25. 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).

    Article  Google Scholar 

  26. Prinz, A.A., Abbott, L.F. & Marder, E. The dynamic clamp comes of age. Trends Neurosci. 27, 218–224 (2004).

    Article  CAS  Google Scholar 

  27. Destexhe, A., Rudolph, M., Fellous, J.M. & Sejnowski, T.J. Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 107, 13–24 (2001).

    Article  CAS  Google Scholar 

  28. Sillito, A.M., Jones, H.E., Gerstein, G.L. & West, D.C. Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479–482 (1994).

    Article  CAS  Google Scholar 

  29. McCormick, D.A. & Feeser, H.R. Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39, 103–113 (1990).

    Article  CAS  Google Scholar 

  30. Perez-Reyes, E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol. Rev. 83, 117–161 (2003).

    Article  CAS  Google Scholar 

  31. Troy, J.B. & Robson, J.G. Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Vis. Neurosci. 9, 535–553 (1992).

    Article  CAS  Google Scholar 

  32. Turner, J.P., Leresche, N., Guyon, A., Soltesz, I. & Crunelli, V. Sensory input and burst firing output of rat and cat thalamocortical cells: the role of NMDA and non-NMDA receptors. J. Physiol. (Lond.) 480, 281–295 (1994).

    Article  CAS  Google Scholar 

  33. Usrey, W.M., Reppas, J.B. & Reid, R.C. Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395, 384–387 (1998).

    Article  CAS  Google Scholar 

  34. 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  Google Scholar 

  35. 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  Google Scholar 

  36. 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  Google Scholar 

  37. Leresche, N., Hering, J. & Lambert, R.C. Paradoxical potentiation of neuronal T-type Ca2+ current by ATP at resting membrane potential. J. Neurosci. 24, 5592–5602 (2004).

    Article  CAS  Google Scholar 

  38. Hirsch, J.C., Fourment, A. & Marc, M.E. Sleep-related variations of membrane potential in the lateral geniculate body relay neurons of the cat. Brain Res. 259, 308–312 (1983).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  40. Steriade, M. To burst, or rather, not to burst. Nat. Neurosci. 4, 671 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  42. Lewis, J.E. Sensory processing and the network mechanisms for reading neuronal population codes. J. Comp. Physiol. A 185, 373–378 (1999).

    Article  CAS  Google Scholar 

  43. Barber, M.J., Clark, J.W. & Anderson, C.H. Neural representation of probabilistic information. Neural Comput. 15, 1843–1864 (2003).

    Article  CAS  Google Scholar 

  44. Tanaka, K. Organization of geniculate inputs to visual cortical cells in the cat. Vision Res. 25, 357–364 (1985).

    Article  CAS  Google Scholar 

  45. Alonso, J.M., Usrey, W.M. & Reid, R.C. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815–819 (1996).

    Article  CAS  Google Scholar 

  46. Montero, V.M. Amblyopia decreases activation of the corticogeniculate pathway and visual thalamic reticularis in attentive rats: a 'focal attention' hypothesis. Neuroscience 91, 805–817 (1999).

    Article  CAS  Google Scholar 

  47. Hines, M.L. & Carnevale, N.T. The NEURON simulation environment. Neural Comput. 9, 1179–1209 (1997).

    Article  CAS  Google Scholar 

  48. Destexhe, A., Mainen, Z.F. & Sejnowski, T.J. Kinetic models of synaptic transmission. in Methods in Neuronal Modeling 2nd edn. (eds. Koch, C. & Segev, I.) Ch. 1, 1–26 (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  49. Rudolph, M., Piwkowska, Z., Badoual, M., Bal, T. & Destexhe, A. A method to estimate synaptic conductances from membrane potential fluctuations. J. Neurophysiol. 91, 2884–2896 (2004).

    Article  Google Scholar 

Download references

Acknowledgements

We thank M. Rudolph, G. Sadoc and L. Focsa for help with computation and Z. Piwkowska and D. Shulz for comments on the manuscript. This work was supported by the Centre National de la Recherche Scientifique, the Human Frontier Science Program, the European Commission (IST-2001-34712) and the Action Concertée Initiative 'Neurosciences integratives et computationnelles'. J.W. is the recipient of a European Union Marie Curie fellowship.

Author information

Author notes

  1. Jakob Wolfart

    Present address: Neurozentrum, Department of Neurosurgery, University Hospital Freiburg, Breisacher Strasse 64, 79106, Freiburg, Germany

  2. Jakob Wolfart and Damien Debay: These authors contributed equally to this work.

Authors and Affiliations

  1. Unité de Neurosciences Integratives et Computationnelles, Centre National de la Recherche Scientifique, Gif-sur-Yvette, 91198, France

    Jakob Wolfart, Damien Debay, Alain Destexhe & Thierry Bal

  2. Institut National de la Santé et de la Recherche Médicale (INSERM) 358, Université Victor Segalen Bordeaux 2, Bordeaux, France

    Gwendal Le Masson

Authors
  1. Jakob Wolfart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Damien Debay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gwendal Le Masson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alain Destexhe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thierry Bal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jakob Wolfart or Thierry Bal.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Subthreshold response variability of thalamocortical cells at hyperpolarized potential (Hyp) and 5 Hz random strength stimulation. (PDF 885 kb)

Supplementary Fig. 2

Comparison of pre-response potential and background conductances preceding burst and single spike responses during noise recordings at resting potential. (PDF 758 kb)

Supplementary Fig. 3

Test of the dynamic-clamp method by comparing real and model membrane potential fluctuations. (PDF 826 kb)

Supplementary Methods (PDF 85 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wolfart, J., Debay, D., Le Masson, G. et al. Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8, 1760–1767 (2005). https://doi.org/10.1038/nn1591

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1591

This article is cited by

Search

Advanced 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