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Lack of cortical contrast gain control in human photosensitive epilepsy

Abstract

Television and video games may be powerful triggers for visually induced epileptic seizures. To better understand the triggering elements of visual stimuli and cortical mechanisms of hyperexcitability, we examined eleven patients with idiopathic photosensitive epilepsy by recording visually evoked potentials (VEPs) in response to temporally modulated patterns of different contrast. For stimuli of low–medium, but not high, temporal frequency, the contrast dependence of VEP amplitude and latency is remarkably abnormal for luminance contrast (black–white), but not so for chromatic contrast (equiluminant red–green) stimuli. We conclude that cortical mechanisms of contrast gain control for pattern stimuli of relatively low temporal frequency and high luminance contrast are lacking or severely impaired in photosensitive subjects.

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References

  1. 1

    Kasteleijn-Nolst Trenité, D. G. A. in Reflex Epilepsies and Reflex Seizures. Advances in Neurology (eds. Zifkin, B. Andermann, F. Beaumanoir, A. & Rowan, J.) 99–121 (Lippincott-Raven, Philadelphia, 1998).

  2. 2

    Harding, G. F. A. & Jeavons, P. M. Photosensitive Epilepsy (Mac Keith, London, 1994).

  3. 3

    Sullivan, K. Perplexity and outrage over TV show. 200 remain hospitalized in Japan after seizures from viewing cartoon. The Herald International Tribune December 19, 5 (1997).

  4. 4

    Ishida, S. et al. Photosensitive seizures provoked while viewing “Pocket Monsters” a made-for-television animation program in Japan. Epilepsia 39, 1340–1344 (1998).

  5. 5

    Christie, T. Death after an attack precipitated by playing Nintendo game. The Sun January 21, 5 (1993).

  6. 6

    Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 30, 389–399 (1989).

  7. 7

    Wilkins, A. J., Darby, C. E. & Binnie, C. D. Neurophysiological aspects of pattern-sensitive epilepsy. Brain 102, 1–25 (1979).

  8. 8

    Binnie, C. D., Findlay, J. & Wilkins, A. J. Mechanisms of epileptogenesis in photosensitive epilepsy implied by the effects of moving patterns. Electroenceph. Clin. Neurophysiol. 61, 1–6 (1985).

  9. 9

    Guerrini, R. et al. Idiopathic photosensitive occipital lobe epilepsy [published erratum appears in Epilepsia 37, 310, 1996] Epilepsia 36, 9, 883–91 (1995).

  10. 10

    Guerrini, R., Bonanni, P., Parmeggiani, L. & Belmonte, A. Adolescent onset of idiopathic photosensitive occipital epilepsy after remission of benign rolandic epilepsy. Epilepsia 38, 777–781 (1997).

  11. 11

    Porciatti, V., Burr, D. C., Morrone, C. & Fiorentini, A. The effects of ageing on the pattern electroretinogram and visual evoked potential in humans. Vision Res. 32, 1199–1209 (1992).

  12. 12

    Simon, F. The phase of PVEP in Maxwellian view: influence of contrast, spatial and temporal frequency. Vision Res. 32, 591–599 (1992).

  13. 13

    Campbell, F. W. & Maffei, L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. J. Physiol. (Lond.) 207, 635–652 (1970).

  14. 14

    Carandini, M., Heeger, D. J. & Movshon, J. A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17, 8621–8644 (1997).

  15. 15

    Shapley, R. M. & Victor, J.D. How the contrast gain control modifies the frequency response of cat retinal ganglion cells. J. Physiol. (Lond.) 318, 161–179 (1981).

  16. 16

    Geisler, W. S. & Albrecht, D. G. Cortical neurons: isolation of contrast gain control. Vision Res. 8, 149–1410 (1992).

  17. 17

    Fiorentini, A., Porciatti, V., Morrone, M. C. & Burr, D. C. Visual ageing: unspecific decline of the responses to luminance and colour. Vision Res. 36, 3557–3566 (1996).

  18. 18

    Newmark, M. E. & Penry, J. K. Photosensitivity and Epilepsy (Raven, New York, 1979).

  19. 19

    Binnie, C. D. & Wilkins, A. J. in Reflex Epilepsies and Reflex Seizures. Advances in Neurology (eds. Zifkin, B., Andermann, F., Beaumanoir, A. & Rowan, J.) 123–138 (Lippicott-Raven, Philadelphia, 1998).

  20. 20

    Binnie, C. D. in Epileptic Seizures and Syndrome (ed. Wolf, P.) 49–54 (John Libbey, London, 1994).

  21. 21

    Guerrini, R. et al. in Reflex Epilepsies and Reflex Seizures. Advances in Neurology (eds. Zifkin, B., Andermann, F., Beaumanoir, A. & Rowan, J.) 159–178 (Lippincott-Raven, Philadelphia, 1998).

  22. 22

    Spekreijse, H., Tweel, L. H. & Zuidema, T. Contrast evoked responses in man. Vision Res. 13, 1577–1601 (1973).

  23. 23

    Albrecht, D. G. & Hamilton, D. B. Striate cortex of monkey and cat: contrast response function. J. Neurophysiol. 48, 217–237 (1982).

  24. 24

    Carandini, M. & Heeger, D. J. Summation and division by neurons in primate visual cortex. Science 264, 1333–1336 (1994).

  25. 25

    Morrone, M. C., Burr, D. C. & Speed, H. D. Cross-orientation inhibition in cat is GABA mediated. Exp. Brain Res. 67, 635–644 (1987).

  26. 26

    Bernardete, E. A. & Kaplan, E. The dynamics of primate M retinal ganglion cells. Vis. Neurosci. 16, 355–368 (1999).

  27. 27

    Morrone, M. C., Porciatti, V., Fiorentini, A. & Burr, D. C. Pattern electroretinogram in response to chromatic stimuli: I Human. Vis. Neurosci. 11, 861–871 (1994).

  28. 28

    Wilkins, A. J., Binnie, C. D., Darby, C. E. & Kasteleijn-Nolst Trenité, D. G. A. in Reflex Seizures and Reflex Epilepsies (eds. Beaumanoir, A., Gastaut, H. & Naquet, R.) 153–162 (Editions Médicine & Hygiène, Geneva, 1989).

  29. 29

    Porciatti, V., Di Bartolo, E., Nardi, M. & Fiorentini, A. Responses to chromatic and luminance contrast in glaucoma: a psychophysical and electrophysiological study. Vision Res. 37, 1975–1987 (1997).

  30. 30

    Mullen, K. T. The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J. Physiol.(Lond.) 359, 381–400 (1985).

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Acknowledgements

The authors would like to thank M. C. Morrone for suggestions and discussion and C. Orsini for technical help.

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Correspondence to Vittorio Porciatti.

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Figure 1: Luminance-contrast gratings: effect of temporal frequency.
Figure 2: Luminance-contrast gratings: effect of contrast.
Figure 3: Luminance-contrast gratings of 4–10 Hz temporal frequency: effect of contrast in individual subjects.
Figure 4: Chromatic-contrast gratings: effect of temporal frequency and contrast.