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Gamma Oscillations and Photosensitive Epilepsy

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The Importance of Photosensitivity for Epilepsy

Abstract

Gamma oscillations (GO) have a frequency between 30 and 100 Hz and a bandwidth of about 30 Hz and have been related to neuronal synchrony involved both in generation of seizures and cognitive processes. Human and animal studies suggest that a circuitry including excitatory and inhibitory neurons is a potential generator of GO, but they are also highly dependent on the characteristics of the visual stimulus. These stimuli that are effective in eliciting photoparoxysmal responses (PPR) are also able to drive narrowband GO (30–80 Hz) in visual cortex PPRs elicited by intermittent photic stimulation in photosensitive patients were preceded by a prominent gamma component with increase in intra- and interhemispheric mean coherence values of the gamma band. Gratings with spatial frequency and color that trigger more frequently PPRs were also found to elicit more prominent GO. Modeling studies have shown that such a circuit can generate stimulus varying gamma oscillations and epileptic activity when it acts as an inhibition-stabilized network.

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References

  1. Hubel DH, Wiesel TN. Receptive fields of single neurones in the cat’s striate cortex. J Physiol. 1959;148:574–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Jasper HH, Andrews HL. Brain potentials and voluntary muscle activity in man. J Neurophysiol. 1938;1(2):87–100.

    Article  Google Scholar 

  3. Das N, Gastaut H. Variations de l’activite electrique du cerveau, du coeur et des muscles squelettiques au cours de la meditation et de l’extase yogique. Electroencephalogr Clin Neurophysiol. 1955;6:211.

    Google Scholar 

  4. Ainsworth M, Lee S, Cunningham MO, Traub RD, Kopell NJ, Whittington MA. Rates and rhythms: a synergistic view of frequency and temporal coding in neuronal networks. Neuron. 2012;75(4):572–83.

    Article  CAS  PubMed  Google Scholar 

  5. Buzsaki G, Wang XJ. Mechanisms of gamma oscillations. Annu Rev Neurosci. 2012;35:203–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ray S, Maunsell JH. Do gamma oscillations play a role in cerebral cortex? Trends Cogn Sci. 2015;19(2):78–85.

    Article  PubMed  Google Scholar 

  7. Womelsdorf T, Valiante TA, Sahin NT, Miller KJ, Tiesinga P. Dynamic circuit motifs underlying rhythmic gain control, gating and integration. Nat Neurosci. 2014;17(8):1031–9.

    Article  CAS  PubMed  Google Scholar 

  8. Lopes da Silva F. EEG and MEG: relevance to neuroscience. Neuron. 2013;80(5):1112–28.

    Article  CAS  PubMed  Google Scholar 

  9. Fries P, Scheeringa R, Oostenveld R. Finding gamma. Neuron. 2008;58(3):303–5.

    Article  CAS  PubMed  Google Scholar 

  10. Bedard C, Kroger H, Destexhe A. Does the 1/f frequency scaling of brain signals reflect self-organized critical states? Phys Rev Lett. 2006;97(11):118102.

    Article  CAS  PubMed  Google Scholar 

  11. Burke JF, Ramayya AG, Kahana MJ. Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility? Curr Opin Neurobiol. 2015;31:104–10.

    Article  CAS  PubMed  Google Scholar 

  12. Manning JR, Jacobs J, Fried I, Kahana MJ. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci. 2009;29(43):13613–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Miller KJ, Honey CJ, Hermes D, Rao RP, denNijs M, Ojemann JG. Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations. NeuroImage. 2014;85(Pt 2):711–20.

    Article  PubMed  Google Scholar 

  14. Miller KJ, Sorensen LB, Ojemann JG, den Nijs M. Power-law scaling in the brain surface electric potential. PLoS Comput Biol. 2009;5(12):e1000609.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Ray S, Maunsell JH. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol. 2011;9(4):e1000610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Winawer J, Kay KN, Foster BL, Rauschecker AM, Parvizi J, Wandell BA. Asynchronous broadband signals are the principal source of the BOLD response in human visual cortex. Curr Biol. 2013;23(13):1145–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Parra J, Kalitzin SN, Iriarte J, Blanes W, Velis DN, Lopes da Silva FH. Gamma-band phase clustering and photosensitivity: is there an underlying mechanism common to photosensitive epilepsy and visual perception? Brain. 2003;126(Pt 5):1164–72.

    Article  CAS  PubMed  Google Scholar 

  18. Varotto G, Visani E, Canafoglia L, Franceschetti S, Avanzini G, Panzica F. Enhanced frontocentral EEG connectivity in photosensitive generalized epilepsies: a partial directed coherence study. Epilepsia. 2012;53(2):359–67.

    Article  PubMed  Google Scholar 

  19. Visani E, Varotto G, Binelli S, Fratello L, Franceschetti S, Avanzini G, Panzica F. Photosensitive epilepsy: spectral and coherence analyses of EEG using 14Hz intermittent photic stimulation. Clin Neurophysiol. 2010;121(3):318–24.

    Article  CAS  PubMed  Google Scholar 

  20. Parra Gómez J. Phase synchrony dynamics in photosensitive epilepsy. Ph.D. thesis. Pamplona: University of Navarra; 2002.

    Google Scholar 

  21. Schillen TB, Konig P. Binding by temporal structure in multiple feature domains of an oscillatory neuronal network. Biol Cybern. 1994;70(5):397–405.

    Article  CAS  PubMed  Google Scholar 

  22. Singer W. Neuronal synchrony: a versatile code for the definition of relations? Neuron. 1999;24(1):49–65; 111–25.

    Article  CAS  PubMed  Google Scholar 

  23. Sayers BM, Beagley HA. Objective evaluation of auditory evoked EEG responses. Nature. 1974;251(5476):608–9.

    Article  CAS  PubMed  Google Scholar 

  24. Makeig S, Westerfield M, Jung TP, Enghoff S, Townsend J, Courchesne E, Sejnowski TJ. Dynamic brain sources of visual evoked responses. Science. 2002;295(5555):690–4.

    Article  CAS  PubMed  Google Scholar 

  25. Buzsaki G, Leung LW, Vanderwolf CH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983;287(2):139–71.

    Article  CAS  PubMed  Google Scholar 

  26. Penttonen M, Kamondi A, Acsady L, Buzsaki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci. 1998;10(2):718–28.

    Article  CAS  PubMed  Google Scholar 

  27. Mann EO, Paulsen O. Mechanisms underlying gamma (’40 Hz’) network oscillations in the hippocampus—a mini-review. Prog Biophys Mol Biol. 2005;87(1):67–76.

    Article  PubMed  Google Scholar 

  28. Mann EO, Radcliffe CA, Paulsen O. Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back. J Physiol. 2005;562(Pt 1):55–63.

    Article  CAS  PubMed  Google Scholar 

  29. Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern. 1988;60(2):121–30.

    Article  CAS  PubMed  Google Scholar 

  30. Gray CM, Konig P, Engel AK, Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989;338(6213):334–7.

    Article  CAS  PubMed  Google Scholar 

  31. Gray CM, Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A. 1989;86(5):1698–702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Tiesinga P, Sejnowski TJ. Cortical enlightenment: are attentional gamma oscillations driven by ING or PING? Neuron. 2009;63(6):727–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Angelucci A, Bijanzadeh M, Nurminen L, Federer F, Merlin S, Bressloff PC. Circuits and mechanisms for surround modulation in visual cortex. Annu Rev Neurosci. 2017;40:425–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 2004;5(10):793–807.

    Article  CAS  PubMed  Google Scholar 

  35. Petilla Interneuron Nomenclature G, Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci. 2008;9(7):557–68.

    Article  CAS  Google Scholar 

  36. Chen G, Zhang Y, Li X, Zhao X, Ye Q, Lin Y, Tao HW, Rasch MJ, Zhang X. Distinct inhibitory circuits orchestrate cortical beta and gamma band oscillations. Neuron. 2017;96(6):1403–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O. Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J Physiol. 2000;529(Pt 1):205–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 2009;459(7247):698–702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kisvarday ZF, Kim DS, Eysel UT, Bonhoeffer T. Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex. Eur J Neurosci. 1994;6(10):1619–32.

    Article  CAS  PubMed  Google Scholar 

  40. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 2009;459(7247):663–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Henrie JA, Shapley R. LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J Neurophysiol. 2005;94(1):479–90.

    Article  PubMed  Google Scholar 

  42. Hermes D, Miller KJ, Wandell BA, Winawer J. Gamma oscillations in visual cortex: the stimulus matters. Trends Cogn Sci. 2015a;19(2):57–8.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Hermes D, Miller KJ, Wandell BA, Winawer J. Stimulus dependence of gamma oscillations in human visual cortex. Cereb Cortex. 2015b;25(9):2951–9.

    Article  CAS  PubMed  Google Scholar 

  44. Jia X, Xing D, Kohn A. No consistent relationship between gamma power and peak frequency in macaque primary visual cortex. J Neurosci. 2013;33(1):17–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lima B, Singer W, Chen NH, Neuenschwander S. Synchronization dynamics in response to plaid stimuli in monkey V1. Cereb Cortex. 2010;20(7):1556–73.

    Article  PubMed  Google Scholar 

  46. Hermes D, Kasteleijn-Nolst Trenite DGA, Winawer J. Gamma oscillations and photosensitive epilepsy. Curr Biol. 2017;27(9):R336–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Singer W, Gray CM. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci. 1995;18:555–86.

    Article  CAS  PubMed  Google Scholar 

  48. Kang K, Shelley M, Henrie JA, Shapley R. LFP spectral peaks in V1 cortex: network resonance and cortico-cortical feedback. J Comput Neurosci. 2010;29(3):495–507.

    Article  PubMed  Google Scholar 

  49. Parra J, Lopes da Silva FH, Stroink H, Kalitzin S. Is colour modulation an independent factor in human visual photosensitivity? Brain. 2007;130(Pt 6):1679–89.

    Article  PubMed  Google Scholar 

  50. Takahashi T, Tsukahara Y. Influence of color on the photoconvulsive response. Electroencephalogr Clin Neurophysiol. 1976;41(2):124–36.

    Article  CAS  PubMed  Google Scholar 

  51. Harding GF, Fylan F. Two visual mechanisms of photosensitivity. Epilepsia. 1999;40(10):1446–51.

    Article  CAS  PubMed  Google Scholar 

  52. Shirakawa S, Funatsuka M, Osawa M, Fujita M, Oguni H. A study of the effect of color photostimulation from a cathode-ray tube (CRT) display on photosensitive patients: the effect of alternating red-cyan flicker stimulation. Epilepsia. 2001;42(7):922–9.

    Article  CAS  PubMed  Google Scholar 

  53. Haigh SM, Barningham L, Berntsen M, Coutts LV, Hobbs ES, Irabor J, Lever EM, Tang P, Wilkins AJ. Discomfort and the cortical haemodynamic response to coloured gratings. Vis Res. 2013;89:47–53.

    Article  PubMed  Google Scholar 

  54. Haigh SM, Cooper NR, Wilkins AJ. Chromaticity separation and the alpha response. Neuropsychologia. 2018;108:1–5.

    Article  CAS  PubMed  Google Scholar 

  55. Bartoli E, Bosking W, Chen Y, Li Y, Sheth SA, Beauchamp MS, Yoshor D, Foster BL. Functionally distinct gamma range activity revealed by stimulus tuning in human visual cortex. Curr Biol. 2019;29(20):3345–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Shirhatti V, Ray S. Long-wavelength (reddish) hues induce unusually large gamma oscillations in the primate primary visual cortex. Proc Natl Acad Sci U S A. 2018;115(17):4489–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL. Paradoxical effects of external modulation of inhibitory interneurons. J Neurosci. 1997;17(11):4382–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ozeki H, Finn IM, Schaffer ES, Miller KD, Ferster D. Inhibitory stabilization of the cortical network underlies visual surround suppression. Neuron. 2009;62(4):578–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mann EO, Kohl MM, Paulsen O. Distinct roles of GABA(a) and GABA(B) receptors in balancing and terminating persistent cortical activity. J Neurosci. 2009;29(23):7513–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Li Z. Computational design and nonlinear dynamics of a recurrent network model of the primary visual cortex. Neural Comput. 2001;13(8):1749–80.

    Article  CAS  PubMed  Google Scholar 

  61. Ray S, Maunsell JH. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron. 2010;67(5):885–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Gnatkovsky V, Librizzi L, Trombin F, de Curtis M. Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann Neurol. 2008;64(6):674–86.

    Article  PubMed  Google Scholar 

  63. Gnatkovsky V, Wendling F, de Curtis M. Cellular correlates of spontaneous periodic events in the medial entorhinal cortex of the in vitro isolated Guinea pig brain. Eur J Neurosci. 2007;26(2):302–11.

    Article  PubMed  Google Scholar 

  64. Cammarota M, Losi G, Chiavegato A, Zonta M, Carmignoto G. Fast spiking interneuron control of seizure propagation in a cortical slice model of focal epilepsy. J Physiol. 2013;591(4):807–22.

    Article  CAS  PubMed  Google Scholar 

  65. Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, Engel J Jr, Forsgren L, French JA, Glynn M, Hesdorffer DC, Lee BI, Mathern GW, Moshe SL, Perucca E, Scheffer IE, Tomson T, Watanabe M, Wiebe S. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55(4):475–82.

    Article  PubMed  Google Scholar 

  66. Avanzini G, Manganotti P, Meletti S, Moshe SL, Panzica F, Wolf P, Capovilla G. The system epilepsies: a pathophysiological hypothesis. Epilepsia. 2012;53(5):771–8.

    Article  PubMed  Google Scholar 

  67. Wolf P, Yacubian EM, Avanzini G, Sander T, Schmitz B, Wandschneider B, Koepp M. Juvenile myoclonic epilepsy: a system disorder of the brain. Epilepsy Res. 2015;114:2–12.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Istituto Neurologico Carlo Besta, Milan, Italy

    Giuliano Avanzini

  2. Epilepsy Unit, Hospital San Rafael, Madrid, Spain

    Jaime Parra

  3. Brain Center Rudolf Magnus, Department of Neurology and Neurosurgery, University Medical Center Utrecht, Utrecht, The Netherlands

    Dora Hermes

  4. Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN, USA

    Dora Hermes

Authors
  1. Giuliano Avanzini
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  2. Jaime Parra
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  3. Dora Hermes
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Correspondence to Giuliano Avanzini .

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Editors and Affiliations

  1. Department of Neurosurgery and Epilepsy, University Medical Center Utrecht, Utrecht, The Netherlands

    Dorothee Kasteleijn-Nolst Trenite

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Avanzini, G., Parra, J., Hermes, D. (2021). Gamma Oscillations and Photosensitive Epilepsy. In: Kasteleijn-Nolst Trenite, D. (eds) The Importance of Photosensitivity for Epilepsy. Springer, Cham. https://doi.org/10.1007/978-3-319-05080-5_17

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  • DOI: https://doi.org/10.1007/978-3-319-05080-5_17

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