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Spontaneously emerging cortical representations of visual attributes

Abstract

Spontaneous cortical activity—ongoing activity in the absence of intentional sensory input—has been studied extensively1, using methods ranging from EEG (electroencephalography)2,3,4, through voltage sensitive dye imaging5,6,7, down to recordings from single neurons8,9. Ongoing cortical activity has been shown to play a critical role in development10,11,12,13,14, and must also be essential for processing sensory perception, because it modulates stimulus-evoked activity5,15,16, and is correlated with behaviour17. Yet its role in the processing of external information and its relationship to internal representations of sensory attributes remains unknown. Using voltage sensitive dye imaging, we previously established a close link between ongoing activity in the visual cortex of anaesthetized cats and the spontaneous firing of a single neuron6. Here we report that such activity encompasses a set of dynamically switching cortical states, many of which correspond closely to orientation maps. When such an orientation state emerged spontaneously, it spanned several hypercolumns and was often followed by a state corresponding to a proximal orientation. We suggest that dynamically switching cortical states could represent the brain's internal context, and therefore reflect or influence memory, perception and behaviour.

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Figure 1: Comparing instantaneous patterns of spontaneous and evoked activity to the averaged functional map.
Figure 2: Spontaneously emerging orientation states.
Figure 3: Dynamics of ongoing activity.
Figure 4: Spontaneous states revealed using a Kohonen algorithm.

References

  1. Lestienne, R. Spike timing, synchronization and information processing on the sensory side of the central nervous system. Prog. Neurobiol. 65, 545–591 (2001)

    CAS  Article  Google Scholar 

  2. Creutzfeldt, O. D., Watanabe, S. & Lux, H. D. Relations between EEG phenomena and potentials of single cortical cells: II. Spontaneous and convulsoid activity. Electroenceph. Clin. Neurophysiol. 20, 19–37 (1966)

    CAS  Article  Google Scholar 

  3. Scherrer, J. Organization of spontaneous electrical activity in the neocortex. Prog. Brain Res. 45, 309–325 (1976)

    CAS  Article  Google Scholar 

  4. Elul, R. The genesis of the EEG. Int. Rev. Neurobiol. 15, 227–272 (1971)

    CAS  Article  Google Scholar 

  5. 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)

    ADS  CAS  Article  Google Scholar 

  6. 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)

    CAS  Article  Google Scholar 

  7. Arieli, A., Shoham, D., Hildesheim, R. & Grinvald, A. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual-cortex. J. Neurophysiol. 73, 2072–2093 (1995)

    CAS  Article  Google Scholar 

  8. Noda, H. & Adey, W. R. Firing variability in cat association cortex during sleep and wakefulness. Brain Res. 18, 513–526 (1970)

    CAS  Article  Google Scholar 

  9. Softky, W. R. & Koch, C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J. Neurosci. 13, 334–350 (1993)

    CAS  Article  Google Scholar 

  10. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996)

    ADS  CAS  Article  Google Scholar 

  11. Thompson, I. Cortical development: A role for spontaneous activity? Curr. Biol. 7, R324–R326 (1997)

    CAS  Article  Google Scholar 

  12. McCormick, D. A. Developmental neuroscience — Spontaneous activity: Signal or noise? Science 285, 541–543 (1999)

    CAS  Article  Google Scholar 

  13. Sur, M., Angelucci, A. & Sharma, J. Rewiring cortex: The role of patterned activity in development and plasticity of neocortical circuits. J. Neurobiol. 41, 33–43 (1999)

    CAS  Article  Google Scholar 

  14. Chiu, C. & Weliky, M. Relationship of correlated spontaneous activity to functional ocular dominance columns in the developing visual cortex. Neuron 35, 1123–1134 (2002)

    CAS  Article  Google Scholar 

  15. Kisley, M. A. & Gerstein, G. L. Trial-to-trial variability and state-dependent modulation of auditory-evoked responses in cortex. J. Neurosci. 19, 10451–10460 (1999)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  17. Adrian, E. D. & Matthews, B. H. C. The Berger rhythm: Potential changes from the occipital lobes in man. Brain 57, 355–385 (1934)

    Article  Google Scholar 

  18. Grinvald, A. et al. in Modern Techniques in Neuroscience Research (eds Windhorst, U. & Johansson, H.) 893–969 (Springer, Heidelberg, 1999)

    Book  Google Scholar 

  19. Petersen, C. C., Grinvald, A. & Sakmann, B. Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J. Neurosci. 23, 1298–1309 (2003)

    CAS  Article  Google Scholar 

  20. Li, B., Peterson, M. R. & Freeman, R. D. Oblique effect: A neural basis in the visual cortex. J. Neurophysiol. 90, 204–217 (2003)

    Article  Google Scholar 

  21. Wang, G., Ding, S. & Yunokuchi, K. Difference in the representation of cardinal and oblique contours in cat visual cortex. Neurosci. Lett. 338, 77–81 (2003)

    CAS  Article  Google Scholar 

  22. Bonhoeffer, T. & Grinvald, A. The layout of iso-orientation domains in area-18 of cat visual-cortex—optical imaging reveals a pinwheel-like organization. J. Neurosci. 13, 4157–4180 (1993)

    CAS  Article  Google Scholar 

  23. Chapman, B. & Bonhoeffer, T. Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. Proc. Natl Acad. Sci. USA 95, 2609–2614 (1998)

    ADS  CAS  Article  Google Scholar 

  24. Coppola, D. M., White, L. E., Fitzpatrick, D. & Purves, D. Unequal representation of cardinal and oblique contours in ferret visual cortex. Proc. Natl Acad. Sci. USA 95, 2621–2623 (1998)

    ADS  CAS  Article  Google Scholar 

  25. Kohonen, T. Self-Organizing Maps (Springer, Berlin, 2000)

    MATH  Google Scholar 

  26. Fries, P., Neuenschwander, S., Engel, A. K., Goebel, R. & Singer, W. Rapid feature selective neuronal synchronization through correlated latency shifting. Nature Neurosci. 4, 194–200 (2001)

    CAS  Article  Google Scholar 

  27. Ben-Yishai, R., Bar-Or, R. L. & Sompolinsky, H. Theory of orientation tuning in visual-cortex. Proc. Natl Acad. Sci. USA 92, 3844–3848 (1995)

    ADS  CAS  Article  Google Scholar 

  28. Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995)

    CAS  Article  Google Scholar 

  29. Ernst, U. A., Pawelzik, K. R., Sahar-Pikielny, C. & Tsodyks, M. V. Intracortical origin of visual maps. Nature Neurosci. 4, 431–436 (2001)

    CAS  Article  Google Scholar 

  30. Shoham, D. et al. Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24, 791–802 (1999)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank A. Aertsen, N. Tishbi, R. Malach and J. M. Herrmann for discussions and insights, R. Hildesheim for the dyes, B. Blumenfeld for his suggestion for the orientation preference map in Fig. 4B, and D. Etner and Y. Toledo for technical assistance. This work was supported by grants from the Israeli Science Foundation, Grodetsky Center and Irving B. Harris Foundation (to M.T.), the Grodetsky Center, the Korber and Israeli Science foundations and the BMBF/MOS (to A.G.) and the Minerva Foundation (to D.B.).

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Correspondence to Tal Kenet.

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Kenet, T., Bibitchkov, D., Tsodyks, M. et al. Spontaneously emerging cortical representations of visual attributes. Nature 425, 954–956 (2003). https://doi.org/10.1038/nature02078

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