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Rapid feature selective neuronal synchronization through correlated latency shifting

Nature Neuroscience volume 4, pages 194–200 (2001)Cite this article

Abstract

Spontaneous brain activity could affect processing if it were structured, . We show that neuron pairs in cat primary visual cortex exhibited correlated fluctuations in response latency, particularly when they had overlapping receptive fields or similar orientation preferences. Correlations occurred within and across hemispheres, but only when local field potentials (LFPs) oscillated in the gamma-frequency range (40–70 Hz). In this range, LFP fluctuations preceding response onset predicted response latencies; negative (positive) LFPs were associated with early (late) responses. Oscillations below 10 Hz caused covariations in response amplitude, but exhibited no columnar selectivity or coordinating effect on latencies. Thus, during high gamma activity, spontaneous activity exhibits distinct, column-specific correlation patterns. Consequently, cortical cells undergo coherent fluctuations in excitability that enhance temporal coherence of responses to contours that are spatially contiguous or have similar orientation. Because synchronized responses are more likely than dispersed responses to undergo rapid and joint processing, spontaneous activity may be important in early visual processes.

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Figure 1: Determination of response onset latencies.
Figure 2: Covariation of latencies.
Figure 3: Distributions of latency correlations.
Figure 4: Interhemispheric latency covariation.
Figure 5: Prediction of spike response latencies by LFP phase.
Figure 6: Influence of prestimulus LFP power on latencies, firing rates and their correlations.
Figure 7: Rapid feature-selective neuronal synchronization through correlated latency shifting.

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References

  1. Arieli, A., Sterkin, A., Grinvald, A. & Aertsen, A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868–1871 (1996).

    Article  CAS  Google Scholar 

  2. Gawne, T. J., Kjaer, T. W. & Richmond, B. J. Latency: another potential code for feature binding in striate cortex. J. Neurophysiol. 76, 1356–1360 (1996).

    Article  CAS  Google Scholar 

  3. Gur, M., Beylin, A. & Snodderly, D. M. Response variability of neurons in primary visual cortex (V1) of alert monkeys. J. Neurosci. 17, 2914–2920 (1997).

    Article  CAS  Google Scholar 

  4. Shadlen, M. N. & Newsome, W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870–3896 (1998).

    Article  CAS  Google Scholar 

  5. 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 

  6. Brecht, M., Singer, W. & Engel, A. K. Correlation analysis of corticotectal interactions in the cat visual system. J. Neurophysiol. 79, 2394–2407 (1998).

    Article  CAS  Google Scholar 

  7. Singer, W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49–65 (1999).

    Article  CAS  Google Scholar 

  8. Tsodyks, M., Kenet, T., Grinvald, A. & Arieli, A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286, 1943–1946 (1999).

    Article  CAS  Google Scholar 

  9. Lampl, I. & Yarom, Y. Subthreshold oscillations of the membrane potential: a functional synchronizing and timing device. J. Neurophysiol. 70, 2181–2186 (1993).

    Article  CAS  Google Scholar 

  10. Volgushev, M., Chistiakova, M. & Singer, W. Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience 83, 15–25 (1998).

    Article  CAS  Google Scholar 

  11. Nowak, L. G., Sanchez-Vives, M. V. & McCormick, D. A. Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb. Cortex 7, 487–501 (1997).

    Article  CAS  Google Scholar 

  12. Mainen, Z. F. & Sejnowski, T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503–1506 (1995).

    Article  CAS  Google Scholar 

  13. Stevens, C. F. & Zador, A. M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1, 210–217 (1998).

    Article  CAS  Google Scholar 

  14. Azouz, R. & Gray, C. M. Cellular mechanisms contributing to response variability of cortical neurons in vivo. J. Neurosci. 19, 2209–2223 (1999).

    Article  CAS  Google Scholar 

  15. 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 

  16. Amzica, F. & Steriade, M. Short- and long-range neuronal synchronization of the slow (< 1 Hz) cortical oscillation. J. Neurophysiol. 73, 20–38 (1995).

    Article  CAS  Google Scholar 

  17. Mitzdorf, U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65, 37–100 (1985).

    Article  CAS  Google Scholar 

  18. Engel, A. K., König, P., Kreiter, A. K. & Singer, W. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252, 1177–1179 (1991).

    Article  CAS  Google Scholar 

  19. Das, A. & Gilbert, C. D. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399, 655–661 (1999).

    Article  CAS  Google Scholar 

  20. Schmidt, K. E., Kim, D. S., Singer, W., Bonhoeffer, T. & Löwel, S. Functional specificity of long-range intrinsic and interhemispheric connections in the visual cortex of strabismic cats. J. Neurosci. 17, 5480–5492 (1997).

    Article  CAS  Google Scholar 

  21. Contreras, D. & Steriade, M. State-dependent fluctuations of low-frequency rhythms in corticothalamic networks. Neuroscience 76, 25–38 (1997).

    Article  CAS  Google Scholar 

  22. Diesmann, M., Gewaltig, M. O. & Aertsen, A. Stable propagation of synchronous spiking in cortical neural networks. Nature 402, 529–533 (1999).

    Article  CAS  Google Scholar 

  23. Thorpe, S., Fize, D. & Marlot, C. Speed of processing in the human visual system. Nature 381, 520–522 (1996).

    Article  CAS  Google Scholar 

  24. Herculano-Houzel, S., Munk, M. H. J., Neuenschwander, S. & Singer, W. Precisely synchronized oscillatory firing patterns require electroencephalographic activation. J. Neurosci. 19, 3992–4010 (1999).

    Article  CAS  Google Scholar 

  25. Makeig, S. & Jung, T. P. Tonic, phasic, and transient EEG correlates of auditory awareness in drowsiness. Brain Res. Cogn. Brain Res. 4, 15–25 (1996).

    Article  CAS  Google Scholar 

  26. Bouyer, J. J., Montaron, M. F. & Rougeul, A. Fast fronto-parietal rhythms during combined focused attentive behaviour and immobility in cat: cortical and thalamic localizations. Electroencephalogr. Clin. Neurophysiol. 51, 244–252 (1981).

    Article  CAS  Google Scholar 

  27. Sanes, J. N. & Donoghue, J. P. Oscillations in local field potentials of the primate motor cortex during voluntary movement. Proc. Natl. Acad. Sci. USA 90, 4470–4474 (1993).

    Article  CAS  Google Scholar 

  28. Murthy, V. N. & Fetz, E. E. Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. J. Neurophysiol. 76, 3949–3967 (1996).

    Article  CAS  Google Scholar 

  29. Roelfsema, P. R., Engel, A. K., König, P. & Singer, W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385, 157–161 (1997).

    Article  CAS  Google Scholar 

  30. Fries, P., Reynolds, J. H., Rorie, A. E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science (in press).

  31. Swindale, N. V. Orientation tuning curves: empirical description and estimation of parameters. Biol. Cybern. 78, 45–56 (1998).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Supported by the MPG and the Heisenberg program of the DFG. We thank S. Herculano-Houzel for suggestions, J.-H. Schröder and M. Stephan for help with data analysis, and J. Reynolds and R. Desimone for help in recording monkey data and for comments on the manuscript.

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Author notes

  1. Pascal Fries

    Present address: Laboratory of Neuropsychology, National Institute of Mental Health, Building 49, 49 Convent Drive, MSC 4415, Bethesda, Maryland, 20892, USA

  2. Andreas K. Engel

    Present address: Research Centre Juelich, Institute for Medicine, Cellular Neurobiology Group, 52425, Juelich, Germany

  3. Rainer Goebel

    Present address: Department of Psychology, University of Maastricht, Neurocognition Group, Postbus 616, 6200, MD, Maastricht, The Netherlands

Authors and Affiliations

  1. Max-Planck Institute for Brain Research, Deutshcordenstraße 46, Frankfurt am Main, 60528, Germany

    Pascal Fries, Sergio Neuenschwander, Andreas K. Engel, Rainer Goebel & Wolf Singer

  2. Department of Psychiatry, Johann Wolfgang Goethe-University, Heinrich-Hoffmann Straße 10, Frankfurt am Main, 60528, Germany

    Pascal Fries

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Correspondence to Wolf Singer.

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Fries, P., Neuenschwander, S., Engel, A. et al. Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 4, 194–200 (2001). https://doi.org/10.1038/84032

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