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.

  • Letter
  • Published:

Coherence of gamma-band EEG activity as a basis for associative learning

Abstract

Different regions of the brain must communicate with each other to provide the basis for the integration of sensory information, sensory-motor coordination and many other functions that are critical for learning, memory, information processing, perception and the behaviour of organisms. Hebb1 suggested that this is accomplished by the formation of assemblies of cells whose synaptic linkages are strengthened whenever the cells are activated or ‘ignited’ synchronously. Hebb's seminal concept has intrigued investigators since its formulation, but the technology to demonstrate its existence had been lacking until the past decade. Previous studies have shown that very fast electroencephalographic activity in the gamma band (20–70 Hz) increases during, and may be involved in, the formation of percepts and memory2,3,4,5,6, linguistic processing7, and other behavioural and preceptual functions8,9,10,11,12. We show here that increased gamma-band activity is also involved in associative learning. In addition, we find that another measure, gamma-band coherence, increases between regions of the brain that receive the two classes of stimuli involved in an associative-learning procedure in humans. An increase in coherence could fulfil the criteria required for the formation of hebbian cell assemblies1, binding together parts of the brain that must communicate with one another in order for associative learning to take place. In this way, coherence may be a signature for this and other types of learning.

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

Access options

Buy this article

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

Figure 1: Pairs of electrode sites displaying significantly greater coherence in the 37–43-Hz gamma band during CS+ than during CS trials in the 2,750–3,000-ms time window for the 120 acquisition trials.
Figure 2: Difference in evoked-response-potential waves between CS+ and CS at each electrode involved in response to the UCS when the UCS was administered to the left (grey line) and right (black line) midfingers.

Similar content being viewed by others

References

  1. Hebb, D. O. The Organization of Behavior (Wiley, New York, (1949)).

    Google Scholar 

  2. Singer, W. & Gray, C. M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).

    Article  CAS  Google Scholar 

  3. Basar, E., Basar-Eroglu, C. & Schürmann, M. Sensory and cognitive components of brain resonance responses. Acta Otolaryngol (Stockh.) 491, 25–35 (1991).

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  5. Pantev, C. Evoked and induced gamma-band activity of the human cortex. Brain Topogr. 7, 321–330 (1995).

    Article  CAS  Google Scholar 

  6. Singer, W. The formation of cooperative cell assemblies in the visual cortex. J. Exp. Biol. 153, 177–197 (1990).

    CAS  PubMed  Google Scholar 

  7. Pulvermüller, F., Lutzenberger, W., Preißl, H. & Birbaumer, N. Spectral responses in the gamma-band: physiological signs of higher cognitive processes? Neuroreport 6, 2059–2064 (1995).

    Article  Google Scholar 

  8. Murthy, V. N., Aoki, F. & Fetz, E. E. in Oscillatory Event-Related Brain Dynamics (eds Pantev, C., Elbert,T. & Lütkenhöner, B.) 213–226 (Plenum, New York, (1994)).

    Google Scholar 

  9. Llinas, R. R. & Ribary, U. Coherent 40-Hz oscillation characterizes dream state in humans. Proc. Natl Acad. Sci. USA 90, 2078–2081 (1993).

    Article  ADS  CAS  Google Scholar 

  10. Sheer, D. E. in Self-regulation of the Brain and Behavior (eds Elbert, T., Rockstroh, B., Lutzenberg, W. & Birbaumer, N.) 64–84 (Springer, Berlin, (1984)).

    Book  Google Scholar 

  11. Steriade, M., Amzica, F. & Contreras, D. Synchronization of fast (30–40 Hz) spontaneous cortical rhythms during brain activation. J. Neurosci. 16, 392–417 (1996).

    Article  CAS  Google Scholar 

  12. Tiitinen, H. et al. Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364, 59–60 (1993).

    Article  ADS  CAS  Google Scholar 

  13. Oldfield, R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychology 9, 97–113 (1971).

    Article  CAS  Google Scholar 

  14. Pulvermüller, F., Birbaumer, N., Lutzenberger, W. & Mohr, B. High-frequency brain activity: its possible role in attention, perception and language processing. Prog. Neurobiol. 52, 427–445 (1997).

    Article  Google Scholar 

  15. Arnold, M., Miltner, W. H. R., Bauer, R. & Braun, C. Adaptive AR modeling of nonstationary time series by means of Kalnan filtering. IEEE Trans. Biomed. Eng. 45, 553–562 (1998).

    Article  CAS  Google Scholar 

  16. Rockstroh, B., Elbert, T., Canavan, A., Lutzenberger, W. & Birbaumer, N. Slow Cortical Potentials and Behaviour (Urban & Schwarzenberg, Munich, (1989)).

    Google Scholar 

  17. Waschulewski Floruss, H., Miltner, W., Brody, S. & Braun, C. Classical conditioning of pain responses. Int. J. Neurosci. 78, 21–32 (1994).

    Article  CAS  Google Scholar 

  18. Gray, C. M. & McCormick, D. A. Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science 274, 109–113 (1996).

    Article  ADS  CAS  Google Scholar 

  19. Gray, C. M., Konig, 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 

  20. Jefferys, J. G., Traub, R. D. & Whittington, M. A. Neuronal networks for induced ‘40 Hz’ rhythms. Trends Neurosci. 19, 202–208 (1996).

    Article  CAS  Google Scholar 

  21. Traub, R. D., Whittington, M. A., Stanford, I. M. & Jefferys, J. G. Amechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621–624 (1996).

    Article  ADS  CAS  Google Scholar 

  22. Bromm, B. & Meier, W. The intracutaneous stimulus: a new pain model for algesimetric studies. Meth. Find. Exp. Clin. Pharmacol. 6, 405–410 (1984).

    CAS  Google Scholar 

  23. Gratton, G., Coles, M. G. & Donchin, E. Anew method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 55, 468–484 (1983).

    Article  CAS  Google Scholar 

  24. Perrin, F., Pernier, J., Bertrand, O. & Echallier, J. F. Spherical splines for scalp potential and current density mapping. Electroencephalogr. Clin. Neurophysiol. 72, 184–187 (1989).

    Article  CAS  Google Scholar 

  25. Biggins, C. A., Fein, G., Raz, J. & Amir, A. Artifactually high coherences result from using spherical spline computation of scalp current density. Electroencephalogr. Clin. Neurophysiol. 79, 413–419 (1991).

    Article  CAS  Google Scholar 

  26. Perrin, F. Comments on article by Biggins et al. Electroencephalogr. Clin. Neurophysiol. 83, 171–174 (1992).

    Article  CAS  Google Scholar 

  27. Haykin, S. Adaptive Filter Theory (Prentice-Hall, Englewood Cliffs, New Jersey, (1986)).

    MATH  Google Scholar 

  28. Chen, H. H. & Guo, L. Identification and Stochastic Adaptive Control (Birkhäuser, Boston, Massachusetts, (1991)).

    Book  Google Scholar 

Download references

Acknowledgements

We thank I. Gutberlet for assistance in data analysis. This research was supported by a grant from the Deutsche Forschungsgemeinschaft to W.H.R.M. and a grant from the Rehabilitation Research and Development service, US Department of Veterans Affairs to E.T.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miltner, W., Braun, C., Arnold, M. et al. Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397, 434–436 (1999). https://doi.org/10.1038/17126

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/17126

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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