Skip to main content
SpringerLink
Log in

Temporal binding at gamma frequencies in the brain: paving the way to epilepsy?

  • Published:
Australasian Physics & Engineering Sciences in Medicine Aims and scope Submit manuscript

Abstract

Fast (beta-gamma band 20-100 Hz) rhythms of electrical activity of the brain have been suggested to play an important role in perception, cognition and consciousness providing temporal binding of neural activities and allowing the formation of mental representations. The recent advances in the concept of temporal binding and their relation to the theory of neural networks (connectionism) are reviewed here as well as some experimental results concerning the intensified gamma rhythms and epilepsy. The hippocampal-neocortical gamma rhythms are extremely intense and hypersynchronous at onset of the epileptiform discharges induced by systemic kainic acid in the rat. Those gamma rhythms are followed by a slow rhythm of epileptiform spikes/sharp waves or spike-wave complexes (‘spike-wave’ activity). During spike-wave activity, gamma synchronisation is significantly decreased. A novel unifying concept is proposed which relates the associative principle of neural networks to the mechanism of temporal binding at high frequencies. It suggests that for each memory stored in an associative network there is a corresponding quasi-stable state of synchronous oscillation at some frequency within the gamma band. It also suggests that excessive temporal binding (“over-binding”) occurs at seizure onset when abnormally intensified and globally synchronous fast activity is often observed. “Over-binding” may cause the undesirable formation of false associations due to inadequate synaptic modifications. To prevent this process, spike-wave discharge develops as an extreme activation of the mechanism capable to desynchronise and eventually suppress fast activity and erase the spurious modes of activity associated with hypersynchronous gamma rhythms. Thus, spike-wave activity is suggested to be the “anti-binding” mechanism. This mechanism is also related to the spikes/sharp waves normally occurring in the brain mostly in sleep. It is qualititively similar to the “unlearning” mechanism of Crick and Mitchison presumably associated with the PG0 spikes of the REM sleep33.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Jasper, H.H. and Andrews, H.L., Electroencephalography. III.Normal differentiation of occipital and precentral regions in man., Arch Neurol Psychiatry. 39: 96–115, 1938.

    Google Scholar 

  2. Heeb, D. O.The Organisation of Behavior.Wiley.New York, 1949.

    Google Scholar 

  3. Malsburg, C. von der,The correlation theory of brain Function. Internal Report 81-2. Max-Planck-Inst. Biophys. Chem., Gottingen (1981). Reprinted. In: (eds. Domany, E., van Hemmen, J.L. & Schulten, K.),Models of Neural Networks 11. Temporal Aspects of Coding and Information Processing in Biological Systems, Springer-Verlag, New York, 95–119, 1994.

    Google Scholar 

  4. Malsburg, C. von der,Am I thinking assemblies? In: (eds. Palm, G. & Aertsen, A.), Brain Theory, Springer-Verlag, Berlin Heidelberg, 161–176, 1986.

    Google Scholar 

  5. Stryker, M.P., Cortical physiology.Is grandmother an Oscillation?, Nature. 338: 297–298, 1989.

    Article  CAS  PubMed  Google Scholar 

  6. Milner, P.M.,A model for visual shape recognition, Psychol Rev. 81: 521–535, 1974.

    Article  CAS  PubMed  Google Scholar 

  7. Crick, F.,Function of the thalamic reticular complex: the searchlight hypothesis, Proc Natl Acad Sci USA. 81: 4586–4590, 1984.

    Article  CAS  PubMed  Google Scholar 

  8. Damasio, A.R.,Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition, Cognition. 33: 25–62, 1989.

    Article  CAS  PubMed  Google Scholar 

  9. Konig, P. and Schillen, T.B.,Stimulus-dependent assembly formation of oscillatory responses: I. Synchronisation, Neural Comput. 3: 155–66, 1991.

    Article  Google Scholar 

  10. Freeman, W. J.Mass action in the nervous system, Acad Press, New York, 1975.

    Google Scholar 

  11. Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M. and Reitboeck, H.J.,Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat, Biol Cybern. 60: 121–130, 1988.

    Article  CAS  PubMed  Google Scholar 

  12. Gray, C.M. and Singer, W.,Stimulus-speclfic neuronal oscillations in orientation columns of cat visual cortex, Proc Natl Acad Sci USA. 86: 1698–1702, 1989;

    Article  CAS  PubMed  Google Scholar 

  13. Engel, A.K., Konig, P., Kreiter, A.K., Schillen, T.B. and Singer, W.,Temporal coding in the visual cortex: new vistas on integration in the nervous system, Trends Neurosci. 15: 218–226, 1992.

    Article  CAS  PubMed  Google Scholar 

  14. Eckhorn, R., Frien, A., Bauer, R., Woelbern, T. and Kehr, H.,High frequency (60-90 Hz) oscillations in primary visual cortex of awake monkey, Neuroreport. 4: 243–246, 1993.

    Article  CAS  PubMed  Google Scholar 

  15. Engel, A.K., Kreiter, A.K., Konig, P. and Singer, W.,Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat, Proc Natl Acad Sci USA. 88: 6048–6052, 1991.

    Article  CAS  PubMed  Google Scholar 

  16. Engel, A.K., Konig, P., Kreiter, A.K. and Singer, W.,Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex, Science. 252: 1177–1179, 1991.

    Article  CAS  Google Scholar 

  17. Ribary, U., Ioannides, A.A., Singh, K.D., Hasson, R., Bolton, J.P., Lado, F., Mogilner, A. and Llinas, R.,Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans, Proc Natl Acad Sci USA. 88: 11037–11041, 1991.

    Article  CAS  PubMed  Google Scholar 

  18. Desmedt, J.E. and Tomberg, C.,Transient phase-locking of 40 Hz electrical oscillations in prefrontal and parietal human cortex reflects the process of conscious somatic perception, Neurosci Lett. 168: 126–129, 1994.

    Article  CAS  PubMed  Google Scholar 

  19. Gevins, A., Cutillo, B., Desmond, J., Ward, M., Bressler, S., Barbero, N. and Laxer, K.,Subdural grid recordings of distributed neocortical networks involved with somatosensory discrimination, Electroencephalogr Clin Neurophysiol. 92: 282–290, 1994.

    Article  CAS  PubMed  Google Scholar 

  20. Eckhorn, R.,Oscillatory and non-oscillatory synchronizations in the visual cortex and their possible roles in associations of visual features, Prog Brain Res. 102: 405–26, 1994.

    Article  CAS  PubMed  Google Scholar 

  21. Pulvermuller, F.,Hebb’s concept of cell assemblies and the psychophysiology of word processing, Psychophysiology 33: 317–333, 1996.

    Article  CAS  PubMed  Google Scholar 

  22. Donoghue, J.P., Sanes, J.N., Hatsopoulos, N.G. and Gaal, G.,Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements, J Neurophysiol. 79: 159–173, 1998.

    CAS  PubMed  Google Scholar 

  23. Hatsopoulos, N.G., Ojakangas, C.L., Paninski, L. and Donoghue, J.P.,Information about movement direction obtained from synchronous activity of motor cortical neurons, Proc Natl Acad Sci USA. 95: 15706–15711, 1998.

    Article  CAS  PubMed  Google Scholar 

  24. Maynard, E.M., Hatsopoulos., N.G., Ojakangas, C.L., Acuna, B.D., Sanes, J.N., Normann, R.A. and Donoghue, J.P.,Neuronal interactions improve cortical population coding of movement direction, J Neurosci. 19: 8083–8093, 1999.

    CAS  PubMed  Google Scholar 

  25. Whittington, M.A., Traub, R.D.,. Faulkner, H.J., Stanford, I.M. and Jefferys, J.G.,Recurrent excitatoty postsynaptic potentials induced by synchronized fast cortical oscillations, Proc Natl Acad Sci USA. 94: 12198–12203, 1997.

    Article  CAS  PubMed  Google Scholar 

  26. Traub, R.D., Whittington, M.A., Buhl, E.H., Jefferys, J.G. and Faulkner, H.J.,On the mechanism of the gamma → beta frequency shift in neuronal oscillations induced in rat hippocampal slices by tetanic stimulation, J Neurosci. 19: 1088- 105, 1999.

    CAS  PubMed  Google Scholar 

  27. Traub, R.D., Jefferys, J.G. & Whittington, M.A.,Fast Oscillations in Cortical Circuits, MIT Press, Cambridge, Massachusetts, 1999.

    Google Scholar 

  28. Bauer, H.-U. and Pawelzik, K.,Alternating oscillatory and stochastic dynamics in a model for a neuronal assembly, Physica. D69: 380–393, 1993.

    Google Scholar 

  29. Hopfield, J.J. and Herz, A.V.,Rapid local synchronization of action potentials: towardcomputation with coupled integrateand-fireneurons, Proc Natl Acad Sci USA. 92: 6655–6662, 1995.

    Article  CAS  PubMed  Google Scholar 

  30. Rennie, C.J., Wright, J.J. and Robinson, P.A.,Mechanisms of cortical electrical activity and emergence of gamma rhythm, J Theor Biol. 205: 17–35, 2000.

    Article  CAS  PubMed  Google Scholar 

  31. Hopfield, J.J.,Neural networks and physical systems with emergent collective computational abilities, Proc Natl Acad Sci USA. 79: 2554–2558, 1982.

    Article  CAS  PubMed  Google Scholar 

  32. Hopfield, J.J., Feinstein, D.I. and Palmer, R.G.,‘Unlearning’ has a stabilizing effect in collective memories, Nature. 304: 158–159, 1983.

    Article  CAS  PubMed  Google Scholar 

  33. Crick, F. and Mitchison, G.,The function of dream sleep, Nature. 304: 111–114, 1983.

    Article  CAS  PubMed  Google Scholar 

  34. Nadler, J.V.,Minireview. Kainic acid as a tool for the study of temporal lobe epilepsy, Life Sci. 29: 2031–2042, 1981.

    Article  CAS  PubMed  Google Scholar 

  35. Medvedev, A. and Willoughby, J.O.,Autoregressive modeling of the EEG in systemic kainic acid-induced epileptogenesis, Int J Neurosci. 97: 149–167, 1999.

    Article  CAS  PubMed  Google Scholar 

  36. Medvedev, A., Mackenzie, L., Hiscock, J.J. and Willoughby, J.O.,Kainic acid induces distinct types of epileptiform discharge with differential involvement of hippocampus and neocortex, Brain Res Bull. 52: 89–98, 2000.

    Article  CAS  PubMed  Google Scholar 

  37. Jenkins, G.M. & Watts, D.G.,Spectral Analysis and Its Applications, Holden-Day, San Francisco, 1968.

    Google Scholar 

  38. Franaszczuk, P.J., Blinowska, K.J. and Kowalczyk, M.,The application of parametric multichannel spectral estimates in the study of electrical brain activity, Biol Cybern. 51: 239–247, 1985.

    Article  CAS  PubMed  Google Scholar 

  39. Alarcon G, Binnie CD, Elwes RD and Polkey CE,Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy, Electroencephalogr Clin Neurophysiol. 94: 326–337, 1995.

    Article  CAS  PubMed  Google Scholar 

  40. Allen, P.J., Fish, D.R. and Smith, S.J.,Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy, Electroencephalogr Clin Neurophysiol. 82: 155–159, 1992.

    Article  CAS  PubMed  Google Scholar 

  41. Fisher, R.S., Webber, W.R., Lesser, R.P., Arroyo, S. and Uematsu, S.,High-frequency EEG activity at the start of Seizures, J Clin Neurophysiol. 9: 441–448, 1992.

    Article  CAS  PubMed  Google Scholar 

  42. Lee, S.A., Spencer, D.D. and Spencer, S.S., Intracranial EEG seizure-onset patterns in neocortical epilepsy, Epilepsia. 41: 297–307, 2000.

    Article  CAS  PubMed  Google Scholar 

  43. Gloor, P.,Contributions of electroencephalography and electrocorticography to the neurosurgical treatment of the epilepsies. In: (eds. Purpura, D., Penry, J. & Walter, R.), Neurosurgical Management of the Epilepsies, Raven Press, New York, 59–105, 1975.

    Google Scholar 

  44. Faught, E., Kuzniecky, R.I. and Hurst, D.C.,Ictal EEG wave forms from epidural electrodes predictive of seizure control after temporal lobectorny, Electroencephalogr Clin Neurophysiol. 83: 229–235, 1992.

    Article  CAS  PubMed  Google Scholar 

  45. Baldeweg, T., Spence, S., Hirsch, S.R. and Gruzelier, J.,Gamma-band electroencephalographic oscillations in a patient with somatic hallucinations, Lancet. 352: 620–621, 1998.

    Article  CAS  PubMed  Google Scholar 

  46. Hasselmo, M.E., Anderson, B.P. and Bower, J.M.,Cholinergic modulation of cortical associative memory Function, J Neurophysiol. 67: 1230–1246, 1992.

    CAS  PubMed  Google Scholar 

  47. Elazar, Z. and Hobson, J.A.,Neuronal excitability control in health and disease: a neurophysiological comparison of REM sleep and epilepsy, Prog Neurobiol. 25: 141–188, 1985.

    Article  CAS  PubMed  Google Scholar 

  48. Stevens, J.R.,All that spikes is not fits.In: (eds. Trimble, M.R. &Reynolds, E.H.).What Is Epilepsy? The Clinical and Scientific Basis of Epilepsy, Churchill Livingstone, Edinburgh, 97–115, 1986.

    Google Scholar 

  49. Engel, J., Alzerman, R., Caldecott-Hazard, F. & Kuhl, D.E.,Epileptic activation of antagonistic systems may explain paradoxical features of experimental and human epilepsy: a review. In: (ed. Wada, J.), Kindling Vol 2, Raven Press, New York, 1981.

    Google Scholar 

  50. Masco, D., Sahibzada, N., Switzer, R. and Gale, K.,Electroshock seizures protect against apoptotic hippocampal cell death induced by adrenalectomy, Neuroscience. 91: 1315–1319, 1999.

    Article  CAS  PubMed  Google Scholar 

  51. Niederrneyer, E. & Lopes da Silva, F.H., (eds.)EIectroencephalography: Basic Principles, Clinical Applications, and Related Fields, Williams & Wilkins, Baltimore, 1999.

    Google Scholar 

  52. Laidlaw, J., Richens, A. & Chadwick, D., (eds.)A Textbook of Epilepsy, Churchill Livingstone, Edinburgh, 1993.

    Google Scholar 

  53. Stein, D.J. & Ludik, J., (eds.)Neural Networks and Psychopathology.Cambridge University Press, Cambridge, UK, 1998.

    Google Scholar 

  54. Fink, M.,Convulsive therapy and epilepsy research.In: (eds. Trimble. M.R. & Reynolds, E.H.).What Is Epilepsy? The Clinical and Scientific Basis of Epilepsy, Churchill Livingstone, Edinburgh, 217–228, 1986.

    Google Scholar 

  55. Traub, R.D., Whittington, M.A., Stanford, I.M. and Jefferys, J.G.,A mechanism for generation of long-range synchronous fast oscillations in the cortex, Nature. 383: 621–624, 1996.

    Article  CAS  PubMed  Google Scholar 

  56. Jefferys, J.G., Traub, R.D. and Whittington, M.A.,Neuronal networks for induced ‘40 Hz’ rhythms, Trends Neurosci. 19: 202–208, 1996.

    Article  CAS  PubMed  Google Scholar 

  57. Dingledine, R. and Somjen, G.,Calcium dependence of synaptic transmission in the hippocampal slice, Brain Res. 207: 218–222, 1981.

    Article  CAS  PubMed  Google Scholar 

  58. Pumain, R., Menini, C., Heinemann, U., Louvel, J. and Silva-Barrat, C.,Chemical synaptic transmission is not Necessary for epileptic seizures to persist in the baboon Papio papio, Exp Neurol. 89: 250–258, 1985.

    Article  CAS  PubMed  Google Scholar 

  59. Yaari, Y., Konnerth, A. and Heinemann, U.,Spontaneous epileptiform activify of CA1 hippocampal neurons in low extracellular calcium solutions, Exp Brain Res. 51: 153–166, 1983.

    Article  CAS  PubMed  Google Scholar 

  60. Konnerth, A., Heinemann, U. and Yaari, Y.,Nonsynaptic epiliptogenesis in the mammalian hippocampus in vitro. I. Development of seizurelike activity in low extracellular Calcium, J Neurophysiol. 56: 409–423, 1986.

    CAS  PubMed  Google Scholar 

  61. Heinemann, U., Konnerth, A., Pumain, R. and Wadman, W.J.,Extracellular calcium and potassium concentration changes in chronic epileptic brain tissue, Adv Neurol. 44: 641–661, 1986.

    CAS  PubMed  Google Scholar 

  62. Traub, R.D., Dudek, F.E., Taylor, C.P. and Knowles, W.D.,Simulation of hippocampal afterdischarges synchronized by electrical interactions, Neuroscience. 14: 1033–1038, 1985.

    Article  CAS  PubMed  Google Scholar 

  63. Traub, R.D.,Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances, J Comput Neurosci. 2: 283–289, 1995.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine and Centre for Neuroscience, Flinders University and Medical Centre, Bedford Park, South Australia

    A. V. Medvedev

Authors
  1. A. V. Medvedev
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Medvedev, A.V. Temporal binding at gamma frequencies in the brain: paving the way to epilepsy?. Australas. Phys. & Eng. Sci. Med. 24, 37–48 (2001). https://doi.org/10.1007/BF03178284

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03178284

Keywords

Search

Navigation