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Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice

Nature volume 454, pages 881–885 (2008)Cite this article

Abstract

Internal brain states form key determinants for sensory perception, sensorimotor coordination and learning1,2. A prominent reflection of different brain states in the mammalian central nervous system is the presence of distinct patterns of cortical synchrony, as revealed by extracellular recordings of the electroencephalogram, local field potential and action potentials. Such temporal correlations of cortical activity are thought to be fundamental mechanisms of neuronal computation3,4,5,6,7,8,9,10,11. However, it is unknown how cortical synchrony is reflected in the intracellular membrane potential (Vm) dynamics of behaving animals. Here we show, using dual whole-cell recordings from layer 2/3 primary somatosensory barrel cortex in behaving mice, that the Vm of nearby neurons is highly correlated during quiet wakefulness. However, when the mouse is whisking, an internally generated state change reduces the Vm correlation, resulting in a desynchronized local field potential and electroencephalogram. Action potential activity was sparse during both quiet wakefulness and active whisking. Single action potentials were driven by a large, brief and specific excitatory input that was not present in the Vm of neighbouring cells. Action potential initiation occurs with a higher signal-to-noise ratio during active whisking than during quiet periods. Therefore, we show that an internal brain state dynamically regulates cortical membrane potential synchrony during behaviour and defines different modes of cortical processing.

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Figure 1: Internal brain state determines membrane potential dynamics.
Figure 2: EEG, LFP and V m are highly correlated during quiet wakefulness but not during active whisking.
Figure 3: Subthreshold membrane potential synchrony in layer 2/3 barrel cortex depends on the internal brain state.
Figure 4: Action potentials result from large, brief and specific input during both quiet wakefulness and whisking.

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References

  1. Gilbert, C. D. & Sigman, M. Brain states: top-down influences in sensory processing. Neuron 54, 677–696 (2007)

    Article  CAS  Google Scholar 

  2. Petersen, C. C. H. The functional organization of the barrel cortex. Neuron 56, 339–355 (2007)

    Article  CAS  Google Scholar 

  3. Buzsaki, G. & Draguhn, A. Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004)

    Article  ADS  CAS  Google Scholar 

  4. Engel, A. K., Fries, P. & Singer, W. Dynamic predictions: oscillations and synchrony in top-down processing. Nature Rev. Neurosci. 2, 704–716 (2001)

    Article  CAS  Google Scholar 

  5. Gray, C. M., König, P., Engel, A. K. & Singer, W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989)

    Article  ADS  CAS  Google Scholar 

  6. Logothetis, N. K., Kayser, C. & Oeltermann, A. In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron 55, 809–823 (2007)

    Article  CAS  Google Scholar 

  7. Riehle, A., Grun, S., Diesmann, M. & Aertsen, A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278, 1950–1953 (1997)

    Article  ADS  CAS  Google Scholar 

  8. Salinas, E. & Sejnowski, T. J. Correlated neuronal activity and the flow of neural information. Nature Rev. Neurosci. 2, 539–550 (2001)

    Article  CAS  Google Scholar 

  9. Steinmetz, P. N. et al. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature 404, 187–190 (2000)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  11. Timofeev, I., Grenier, F. & Steriade, M. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc. Natl Acad. Sci. USA 98, 1924–1929 (2001)

    Article  ADS  CAS  Google Scholar 

  12. Kleinfeld, D., Ahissar, E. & Diamond, M. E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435–444 (2006)

    Article  CAS  Google Scholar 

  13. Crochet, S. & Petersen, C. C. H. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nature Neurosci. 9, 608–610 (2006)

    Article  CAS  Google Scholar 

  14. Castro-Alamancos, M. A. Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41, 455–464 (2004)

    Article  CAS  Google Scholar 

  15. Ferezou, I. et al. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56, 907–923 (2007)

    Article  CAS  Google Scholar 

  16. Huber, D. et al. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451, 61–64 (2008)

    Article  ADS  CAS  Google Scholar 

  17. Dombeck, D. A., Khabbaz, A. N., Collman, F., Adelman, T. L. & Tank, D. W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56, 43–57 (2007)

    Article  CAS  Google Scholar 

  18. Leiser, S. C. & Moxon, K. A. Responses of trigeminal ganglion neurons during natural whisking behaviors in the awake rat. Neuron 53, 117–133 (2007)

    Article  CAS  Google Scholar 

  19. Szwed, M., Bagdasarian, K. & Ahissar, E. Encoding of vibrissal active touch. Neuron 40, 621–630 (2003)

    Article  CAS  Google Scholar 

  20. Fee, M. S., Mitra, P. P. & Kleinfeld, D. Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J. Neurophysiol. 78, 1144–1149 (1997)

    Article  CAS  Google Scholar 

  21. Ahrens, K. F. & Kleinfeld, D. Current flow in vibrissa motor cortex can phase-lock with exploratory rhythmic whisking in rat. J. Neurophysiol. 92, 1700–1707 (2004)

    Article  Google Scholar 

  22. Lampl, I., Reichova, I. & Ferster, D. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22, 361–374 (1999)

    Article  CAS  Google Scholar 

  23. Petersen, C. C. H., Hahn, T. T. G., Mehta, M., Grinvald, A. & Sakmann, B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl Acad. Sci. USA 100, 13638–13643 (2003)

    Article  ADS  CAS  Google Scholar 

  24. Volgushev, M., Chauvette, S., Mukovski, M. & Timofeev, I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations. J. Neurosci. 26, 5665–5672 (2006)

    Article  CAS  Google Scholar 

  25. Berger, H. Electroencephalogram in humans. Arch. Psychiatr. Nervenkr. 87, 527–570 (1929)

    Article  Google Scholar 

  26. Azouz, R. & Gray, C. M. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo . Proc. Natl Acad. Sci. USA 97, 8110–8115 (2000)

    Article  ADS  CAS  Google Scholar 

  27. Brecht, M., Schneider, M., Sakmann, B. & Margrie, T. W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704–710 (2004)

    Article  ADS  CAS  Google Scholar 

  28. Hahnloser, R. H., Kozhevnikov, A. A. & Fee, M. S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (2002)

    Article  ADS  CAS  Google Scholar 

  29. Houweling, A. R. & Brecht, M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451, 65–68 (2008)

    Article  ADS  CAS  Google Scholar 

  30. Lee, A. K., Manns, I. D., Sakmann, B. & Brecht, M. Whole-cell recordings in freely moving rats. Neuron 51, 399–407 (2006)

    Article  CAS  Google Scholar 

  31. Dörfl, J. The innervation of the mystacial region of the white mouse: a topographical study. J. Anat. 142, 173–184 (1985)

    PubMed  PubMed Central  Google Scholar 

  32. Hattox, A., Li, Y. & Keller, A. Serotonin regulates rhythmic whisking. Neuron 39, 343–352 (2003)

    Article  CAS  Google Scholar 

  33. Gao, P., Hattox, A. M., Jones, L. M., Keller, A. & Zeigler, H. P. Whisker motor cortex ablation and whisker movement patterns. Somatosens. Mot. Res. 20, 191–198 (2003)

    Article  Google Scholar 

  34. Welker, W. I. Analysis of sniffing of the albino rat. Behaviour 22, 223–244 (1964)

    Article  Google Scholar 

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Acknowledgements

We thank D. Hill and D. Kleinfeld for help with coherence analyses. We thank S. Crochet, L. Gentet, I. Ferezou and S. Lefort for discussions and critical reading of the manuscript. This work was funded by a Long Term Fellowship from the Human Frontier Science Program and a grant from the Swiss National Science Foundation.

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Authors and Affiliations

  1. Laboratory of Sensory Processing, Brain Mind Institute, Faculty of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), CH-1015 Lausanne, Switzerland ,

    James F. A. Poulet & Carl C. H. Petersen

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  1. James F. A. Poulet
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  2. Carl C. H. Petersen
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Correspondence to Carl C. H. Petersen.

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The file contains Supplementary Movie 1 showing dual whole-cell recording during behaviour. (MOV 2040 kb)

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Poulet, J., Petersen, C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008). https://doi.org/10.1038/nature07150

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