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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.

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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.

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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.

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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

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Correspondence to Jakob Wolfart or Thierry Bal.

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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)

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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

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