The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures

Nature Communications

Volumn 7, Issue , 2016, Pages

  Smith, Elliot H ^a   Liou, Jyun You ^b   Davis, Tyler S ^c   Merricks, Edward M ^d   Kellis, Spencer S ^e   Weiss, Shennan A ^f   Greger, Bradley ^g   House, Paul A ^c   McKhann Ii, Guy M ^a   Goodman, Robert R ^h   Emerson, Ronald G ⁱ   Bateman, Lisa M ^a   Trevelyan, Andrew J ^d   Schevon, Catherine A ^a  

^a Department of Medicine   (United States)

^b Columbia University ^*  (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e California Institute of Technology   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g Arizona State University   (United States)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

ⁱ WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CELLS AND CELL COMPONENTS; EVOLUTION; NEUROLOGY; SPATIOTEMPORAL ANALYSIS;

ACTION POTENTIAL; ARTICLE; DEPOLARIZATION; DYNAMICS; ELECTRIC POTENTIAL; ELECTROCORTICOGRAPHY; ELECTROENCEPHALOGRAM; LATENT PERIOD; NONHUMAN; SEIZURE; SYNAPSE; SYNAPTIC POTENTIAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; HUMAN; MICROELECTRODE; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PHYSIOLOGY;

BRAIN WAVES; COMPUTER SIMULATION; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; HUMANS; MICROELECTRODES; MODELS, NEUROLOGICAL; NERVE NET; SEIZURES;

EID: 84962683987     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11098     Document Type: Article

References (68)

1. Penfield, W., Erickson, T. C Epilepsy and Cerebral Localization (ed. Thomas, C. C.) 623 (Oxford, UK, 1941).
2. Kramer, M. A., Cash, S. S. Epilepsy as a disorder of cortical network organization. Neuroscientist 18, 360-372 (2012).
3. Kramer, M. A. et al. Coalescence and fragmentation of cortical networks during focal seizures. J. Neurosci. 30, 10076-10085 (2010).
4. Kramer, M. A. et al. Human seizures self-terminate across spatial scales via a critical transition. Proc. Natl Acad. Sci. USA 109, 21116-21121 (2012).
5. Schindler, K., Elger, C. E., Lehnertz, K. Increasing synchronization may promote seizure termination: evidence from status epilepticus. Clin. Neurophysiol. 118, 1955-1968 (2007).
6. Jiruska, P. et al. Synchronization and desynchronization in epilepsy: controversies and hypotheses. J. Physiol. 591, 787-797 (2013).
7. Timofeev, I., Steriade, M. Neocortical seizures: initiation, development and cessation. Neuroscience 123, 299-336 (2004).
8. Krishnan, G. P., Bazhenov, M. Ionic dynamics mediate spontaneous termination of seizures and postictal depression state. J. Neurosci. 31, 8870-8882 (2011).
9. Lado, F. A., Moshe, S. L. How do seizures stop Epilepsia 49, 1651-1664 (2008).
10. Pinto, D. J., Patrick, S. L., Huang, W. C., Connors, B. W. Initiation, propagation, and termination of epileptiform activity in rodent neocortex in vitro involve distinct mechanisms. J. Neurosci. 25, 8131-8140 (2005).
11. Ziemann, A. E. et al. Seizure termination by acidosis depends on ASIC1a. Nat. Neurosci. 11, 816-822 (2008).
12. D'Ambrosio, R., Miller, J. W. What is an epileptic seizure Unifying definitions in clinical practice and animal research to develop novel treatments. Epilepsy Curr. 10, 61-66 (2010).
13. Schevon, C. A. et al. Evidence of an inhibitory restraint of seizure activity in humans. Nat. Commun. 3, 1060 (2012).
14. Weiss, S. A. et al. Ictal high frequency oscillations distinguish two types of seizure territories in humans. Brain 136, 3796-3808 (2013).
15. Trevelyan, A. J., Baldeweg, T., van Drongelen, W., Yuste, R., Whittington, M. The source of afterdischarge activity in neocortical tonic-clonic epilepsy. J. Neurosci. 27, 13513-13519 (2007).
16. Ma, H., Zhao, M., Schwartz, T. H. Dynamic neurovascular coupling and uncoupling during ictal onset, propagation, and termination revealed by simultaneous in vivo optical imaging of neural activity and local blood volume. Cereb. Cortex 23, 885-899 (2013).
17. Ellender, T. J., Raimondo, J. V., Irkle, A., Lamsa, K. P., Akerman, C. J. Excitatory effects of parvalbumin-expressing interneurons maintain hippocampal epileptiform activity via synchronous afterdischarges. J. Neurosci. 34, 15208-15222 (2014).
18. Truccolo, W. et al. Neuronal ensemble synchrony during human focal seizures. J. Neurosci. 34, 9927-9944 (2014).
19. Trevelyan, A. J., Sussillo, D., Watson, B. O., Yuste, R. Modular propagation of epileptiform activity: evidence for an inhibitory veto in neocortex. J. Neurosci. 26, 12447-12455 (2006).
20. Schevon, C. A. et al. Spatial characterization of interictal high frequency oscillations in epileptic neocortex. Brain 132, 3047-3059 (2009).
21. Kellis, S. et al. Multi-scale analysis of neural activity in humans: implications for micro-scale electrocorticography. Clin. Neurophysiol. 127, 591-601 (2015).
22. Normann, R. A. Technology insight: future neuroprosthetic therapies for disorders of the nervous system. Nat. Clin. Pract. Neurol. 3, 444-452 (2007).
23. Trevelyan, A. J., Sussillo, D., Yuste, R. Feedforward inhibition contributes to the control of epileptiform propagation speed. J. Neurosci. 27, 3383-3387 (2007).
24. Penfield, W., Jasper, H. Epilepsy and the functional anatomy of the human brain (Little, Brown & Co, 1954).
25. Benucci, A., Frazor, R. A., Carandini, M. Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55, 103-117 (2007).
26. Zanos, T. P., Mineault, P. J., Nasiotis, K. T., Guitton, D., Pack, C. C. A sensorimotor role for traveling waves in primate visual cortex. Neuron 85, 615-627 (2015).
27. Sato, T. K., Nauhaus, I., Carandini, M. Traveling waves in visual cortex. Neuron 75, 218-229 (2012).
28. Alarcon, G. et al. Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. Brain 120, 2259-2282 (1997).
29. Emerson, R. G., Turner, C. A., Pedley, T. A., Walczak, T. S., Forgione, M. Propagation patterns of temporal spikes. Electroencephalogr. Clin. Neurophysiol. 94, 338-348 (1995).
30. Gonzalez-Ramrez, L. R., Ahmed, O. J., Cash, S. S., Wayne, C. E., Kramer, M. A. A biologically constrained, mathematical model of cortical wave propagation preceding seizure termination. PLoS Comput. Biol. 11, e1004065 (2015).
31. Mongillo, G., Barak, O., Tsodyks, M. Synaptic theory of working memory. Science 319, 1543-1546 (2008).
32. Vladimirski, B. B., Tabak, J., O'Donovan, M. J., Rinzel, J. Episodic activity in a heterogeneous excitatory network, from spiking neurons to mean field. J. Comput. Neurosci. 25, 39-63 (2008).
33. Merricks, E. M. et al. Single unit action potentials in humans and the effect of seizure activity. Brain 138, 2891-2906 (2015).
34. Ray, S., Maunsell, J. H. R. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 67, 885-896 (2010).
35. Manning, J. R., Jacobs, J., Fried, I., Kahana, M. J. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J. Neurosci. 29, 13613-13620 (2009).
36. Miller, K. J., Sorensen, L. B., Ojemann, J. G., Nijs & den, M. Power-law scaling in the brain surface electric potential. PLoS Comput .Biol. 5, e1000609 (2009).
37. Zanos, T. P., Mineault, P. J., Pack, C. C. Removal of spurious correlations between spikes and local field potentials. J. Neurophysiol. 105, 474-486 (2011).
38. Ray, S., Maunsell, J. H. R. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol. 9, e1000610 (2011).
39. Cymerblit-Sabba, A., Schiller, Y. Development of hypersynchrony in the cortical network during chemoconvulsant-induced epileptic seizures in vivo. J. Neurophysiol. 107, 1718-1730 (2012).
40. Bettus, G. et al. Interictal functional connectivity of human epileptic networks assessed by intracerebral EEG and BOLD signal fluctuations. PLoS ONE 6, e20071 (2011).
41. Engel, J., Pedley, T. A. Epilepsy (Wolters Kluwer Health/Lippincott Williams and Wilkins, Philadephia, 2008).
42. Beverlin, B., Kakalios, J., Nykamp, D., Netoff, T. I. Dynamical changes in neurons during seizures determine tonic to clonic shift. J. Comput. Neurosci. 33, 41-51 (2011).
43. Abbott, L., Van Vreeswijk, C. Asynchronous states in networks of pulse-coupled oscillators. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 48, 1483-1490 (1993).
44. Engel, J. Models of focal epilepsy. Suppl. Clin. Neurophysiol. 57, 392-399 (2004).
45. Bragin, A., Csicsvari, J., Penttonen, M., Buzsaki, G. Epileptic afterdischarge in the hippocampal-entorhinal system: current source density and unit studies. Neuroscience 76, 1187-1203 (1997).
46. Alger, B., Nicoll, R. Epileptiform burst afterhyperolarization: calciumdependent potassium potential in hippocampal CA1 pyramidal cells. Science 210, 1122-1124 (1980).
47. Timofeev, I., Grenier, F., Steriade, M. Contribution of intrinsic neuronal factors in the generation of cortically driven electrographic seizures. J. Neurophysiol. 92, 1133-1143 (2004).
48. Bal, T., McCormick, D. A. What stops synchronized thalamocortical oscillations Neuron 17, 297-308 (1996).
49. Norden, A. D., Blumenfeld, H. The role of subcortical structures in human epilepsy. Epilepsy Behav. 3, 219-231 (2002).
50. Mitsuya, K., Nitta, N., Suzuki, F. Persistent zinc depletion in the mossy fiber terminals in the intrahippocampal kainate mouse model of mesial temporal lobe epilepsy. Epilepsia 50, 1979-1990 (2009).
51. Hamil, N. E., Cock, H. R., Walker, M. C. Acute down-regulation of adenosine A(1) receptor activity in status epilepticus. Epilepsia 53, 177-188 (2012).
52. Van Gompel, J. J. et al. Increased cortical extracellular adenosine correlates with seizure termination. Epilepsia 55, 233-244 (2014).
53. Crone, N. E., Miglioretti, D. L., Gordon, B., Lesser, R. P. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121, 2301-2315 (1998).
54. Buzsaki, G., Horvath, Z., Urioste, R., Hetke, J., Wise, K. High-frequency network oscillation in the hippocampus. Science 256, 1025-1027 (1992).
55. Einevoll, G. T., Kayser, C., Logothetis, N. K., Panzeri, S. Modelling and analysis of local fieldpotentials for studying the function ofcortical circuits. Nat. Rev. Neurosci. 14, 770-785 (2013).
56. Miller, K. J. Broadband spectral change: evidence for a macroscale correlate of population firing rate J. Neurosci. 30, 6477-6479 (2010).
57. Bragin, A., Benassi, S. K., Kheiri, F., Engel, J. Further evidence that pathologic high-frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus. Epilepsia 52, 45-52 (2011).
58. Modur, P. N., Vitaz, T. W., Zhang, S. Seizure localization using broadband EEG: comparison of conventional frequency activity, high-frequency oscillations, and infraslow activity. J. Clin. Neurophysiol. 29, 309-319 (2012).
59. Zelmann, R., Lina, J. M., Schulze-Bonhage, A., Gotman, J., Jacobs, J. Scalp EEG is not a blur: it can see high frequency oscillations although their generators are small. Brain Topogr. 27, 683-704 (2014).
60. Bragin, A., Engel, J., Staba, R. J. High-frequency oscillations in epileptic brain. Curr. Opin. Neurol. 23, 151-156 (2010).
61. Wilson, H. R., Cowan, J. D. Excitatory and inhibitory interactions in localized populations of model neurons. Biophys. J. 12, 1-24 (1972).
62. Khodagholy, D. et al. NeuroGrid: recording action potentials from the surface of the brain. Nat. Neurosci. 18, 310-315 (2015).
63. Gallmetzer, P. et al. Postictal paresis in focal epilepsies-incidence, duration, and causes: a video-EEG monitoring study. Neurology 62, 2160-2164 (2004).
64. Bateman, L. M., Li, C.-S., Seyal, M. Ictal hypoxemia in localization-related epilepsy: analysis of incidence, severity and risk factors. Brain 131, 3239-3245 (2008).
65. House, P. A., MacDonald, J. D., Tresco, P. A., Normann, R. A. Acute microelectrode array implantation into human neocortex: preliminary technique and histological considerations. Neurosurg. Focus 20, E4 (2006).
66. Berens, P. CircStat: a MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1-20 (2009).
67. Schindler, K., Leung, H., Elger, C. E., Lehnertz, K. Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. Brain 130, 65-77 (2007).
68. Shannon, C. A mathematical theory of communications. Bell Syst. Tech. J. 27, 379-423 (1948).