doi: 10.1111/epi.16356.
Epub 2019 Oct 24.
Prince Antwi
1
, Barbara C Banz
3
4
, Peter Vincent
1
, Rick Saha
1
, Christopher A Arencibia
1
, Jun H Ryu
1
, Ece Atac
1
5
, Nehan Saleem
1
, Shiori Tomatsu
1
, Kohleman Swift
1
, Claire Hu
1
, Heinz Krestel
1
6
, Pue Farooque
1
, Susan Levy
1
, Jia Wu
4
7
, Michael Crowley
4
7
, Federico E Vaca
3
4
7
, Hal Blumenfeld
1
8
9
Affiliations
PMID:
31646628
PMCID:
PMC7424790
DOI:
10.1111/epi.16356
Realistic driving simulation during generalized epileptiform discharges to identify electroencephalographic features related to motor vehicle safety: Feasibility and pilot study
Eli Cohen et al.
Epilepsia.
2020 Jan.
Abstract
Objective:
Generalized epileptiform discharges (GEDs) can occur during seizures or without obvious clinical accompaniment. Motor vehicle driving risk during apparently subclinical GEDs is uncertain. Our goals were to develop a feasible, realistic test to evaluate driving safety during GEDs, and to begin evaluating electroencephalographic (EEG) features in relation to driving safety.
Methods:
Subjects were aged ≥15 years with generalized epilepsy, GEDs on EEG, and no clinical seizures. Using a high-fidelity driving simulator (miniSim) with simultaneous EEG, a red oval visual stimulus was presented every 5 minutes for baseline testing, and with each GED. Participants were instructed to pull over as quickly and safely as possible with each stimulus. We analyzed driving and EEG signals during GEDs.
Results:
Nine subjects were tested, and five experienced 88 GEDs total with mean duration 2.31 ± 1.89 (SD) seconds. Of these five subjects, three responded appropriately to all stimuli, one failed to respond to 75% of stimuli, and one stopped driving immediately during GEDs. GEDs with no response to stimuli were significantly longer than those with appropriate responses (8.47 ± 3.10 vs 1.85 ± 0.69 seconds, P < .001). Reaction times to stimuli during GEDs were significantly correlated with GED duration (r = 0.30, P = .04). In addition, EEG amplitude was greater for GEDs with no response to stimuli than GEDs with responses, both for overall root mean square voltage amplitude (66.14 μV vs 52.99 μV, P = .02) and for fractional power changes in the frequency range of waves (P < .05) and spikes (P < .001).
Significance:
High-fidelity driving simulation is feasible for investigating driving behavior during GEDs. GEDs with longer duration and greater EEG amplitude showed more driving impairment. Future work with a large sample size may ultimately enable classification of GED EEG features to predict individual driving risk.
Keywords:
EEG; absence seizures; consciousness; driving; epilepsy; spike-wave discharges.
Wiley Periodicals, Inc. © 2019 International League Against Epilepsy.
PubMed Disclaimer
Conflict of interest statement
CONFLICT OF INTEREST
None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
Figures
FIGURE 1
Driving paradigm including electroencephalogram (EEG), video, and behavioral data acquisition. Main components and configuration of the miniSim driving simulator at the DrivSim laboratory are shown. Detection of epileptiform discharge prompts an experienced EEG reviewer to press the Event Detection Button. A red oval stimulus is sent to the screen, and the stimulus time is recorded by the DrivSim computer as well as time-marked as an event on EEG recording. Subject responses including steering wheel, gas, and brake pedal are recorded on the DrivSim computer and analyzed offline. Behavior is also recorded by video cameras in the DrivSim car
FIGURE 2
Examples of generalized epileptiform discharge (GEDs) with spared and impaired responses to stimuli while driving. A, Electroencephalographic (EEG) recordings for GEDs associated with spared and impaired response to red oval stimulus. Insets provide an expanded view of the 3-Hz spike-wave morphology of EEG. Selected EEG channels (of 128 recorded) along the vertical axis comprise the viewing montage used during real-time visual detection of GEDs, as well as subsequent offline review. Cz was used as reference. Scale bar is 500 μV. B, Gas pedal position (green traces) and brake pedal force (orange traces) on same time scale as corresponding GED with spared versus impaired responses to stimulus presentation (red vertical lines). GED onset and offset are indicated by vertical blue lines. In the GED with spared response to the stimulus (left traces), there is a prompt decrease in depression of the gas pedal (downward deflection of green trace) followed by increased brake force (upward deflection of orange trace). In contrast, in the GED with impaired response to the stimulus (right traces), there are no appropriate changes in gas pedal or brakes after the stimulus. Gas pedal units are the ratio of downward displacement distance divided by maximal pedal downward displacement. Brake pedal units are in pounds. All example traces shown here (A and B) are from Patient 3 (Table 1)
FIGURE 3
Responses to stimuli in relation to generalized epileptiform discharges (GEDs) while driving. A, GED durations for the four patients with behavioral data during GEDs. Stimuli (marked in red) and time of response (marked in green) are given relative to the onset of GEDs. All GEDs are aligned by onset time and are arranged in ascending order of duration. GED bars are colored by participant (see key). *GED with no response to the stimulus. B, Relationship between GED duration and the reaction time. The dotted line gives best fit by linear least squares regression. Pearson correlation coefficient r = .30, P = .04. C, Relationship between root mean square voltage (VRMS; normalized to mean within participant) for each GED and reaction time. The dotted line gives best fit by least squares regression. Pearson correlation coefficient r = .20, P = .17. For A, all GEDs with behavioral testing from Patients 1, 3, 7, and 9 are shown (Patient 4 lacked behavioral testing; see text). For B and C, only GEDs where the stimulus was presented during the episode (not afterward, see A for examples of this) and where a response occurred either during or after the episode are included
FIGURE 4
Greater electroencephalographic (EEG) spike amplitude in generalized epileptiform discharge (GED) with impaired responses. A, B, Head maps of 128-channel high-density EEG fractional power change in the 2.5- to 4-Hz frequency range (wave components of spike-wave discharges) for GEDs with spared (A) or impaired (B) response (no response) to stimuli. C, D, Maps of EEG fractional power change in the 10- to 125-Hz frequency range (spike components of spike-wave discharges) for GEDs with spared (C) and impaired (D) responses. Color scale bars represent EEG power during seizures divided by baseline power (fractional power). The top color bar is for A and B, and bottom bar is for C and D. The anterior head region in which fractional power change was compared statistically is outlined in yellow in A. EEG data are from the same patients and GED episodes as in Figure 3A
Similar articles
Driving status of patients with generalized spike-wave on EEG but no clinical seizures.
Antwi P, Atac E, Ryu JH, Arencibia CA, Tomatsu S, Saleem N, Wu J, Crowley MJ, Banz B, Vaca FE, Krestel H, Blumenfeld H.
Antwi P, et al.
Epilepsy Behav. 2019 Mar;92:5-13. doi: 10.1016/j.yebeh.2018.11.031. Epub 2018 Dec 21.
Epilepsy Behav. 2019.
PMID: 30580109
Free PMC article.
Review.
Impaired consciousness in patients with absence seizures investigated by functional MRI, EEG, and behavioural measures: a cross-sectional study.
Guo JN, Kim R, Chen Y, Negishi M, Jhun S, Weiss S, Ryu JH, Bai X, Xiao W, Feeney E, Rodriguez-Fernandez J, Mistry H, Crunelli V, Crowley MJ, Mayes LC, Constable RT, Blumenfeld H.
Guo JN, et al.
Lancet Neurol. 2016 Dec;15(13):1336-1345. doi: 10.1016/S1474-4422(16)30295-2.
Lancet Neurol. 2016.
PMID: 27839650
Free PMC article.
The impact of subclinical epileptiform discharges on complex tasks and cognition: relevance for aircrew and air traffic controllers.
Kasteleijn-Nolst Trenité DG, Vermeiren R.
Kasteleijn-Nolst Trenité DG, et al.
Epilepsy Behav. 2005 Feb;6(1):31-4. doi: 10.1016/j.yebeh.2004.10.005.
Epilepsy Behav. 2005.
PMID: 15652731
Review.
Electroencephalographic findings in patients with circumscribed thalamic lesions.
Tsoures E, Lewerenz J, Pinkhardt E, Ludolph AC, Fauser S.
Tsoures E, et al.
Epilepsy Res. 2017 Sep;135:115-122. doi: 10.1016/j.eplepsyres.2017.06.009. Epub 2017 Jun 15.
Epilepsy Res. 2017.
PMID: 28666153
The influence of subclinical epileptiform EEG discharges on driving behaviour.
Kasteleijn-Nolst Trenité DG, Riemersma JB, Binnie CD, Smit AM, Meinardi H.
Kasteleijn-Nolst Trenité DG, et al.
Electroencephalogr Clin Neurophysiol. 1987 Aug;67(2):167-70. doi: 10.1016/0013-4694(87)90040-x.
Electroencephalogr Clin Neurophysiol. 1987.
PMID: 2439294
Cited by
Timelined multimodal recording of EEG and driving performance using a driving simulator system during a focal impaired awareness seizure.
Ban T, Ishishita Y, Tetsuka M, Uchiyama T, Ohtani K, Kawai K.
Ban T, et al.
Epilepsy Behav Rep. 2020 Jan 7;13:100356. doi: 10.1016/j.ebr.2020.100356. eCollection 2020.
Epilepsy Behav Rep. 2020.
PMID: 32637908
Free PMC article.
A machine-learning approach for predicting impaired consciousness in absence epilepsy.
Springer M, Khalaf A, Vincent P, Ryu JH, Abukhadra Y, Beniczky S, Glauser T, Krestel H, Blumenfeld H.
Springer M, et al.
Ann Clin Transl Neurol. 2022 Oct;9(10):1538-1550. doi: 10.1002/acn3.51647. Epub 2022 Sep 16.
Ann Clin Transl Neurol. 2022.
PMID: 36114696
Free PMC article.
Spatiotemporal dynamics between interictal epileptiform discharges and ripples during associative memory processing.
Henin S, Shankar A, Borges H, Flinker A, Doyle W, Friedman D, Devinsky O, Buzsáki G, Liu A.
Henin S, et al.
Brain. 2021 Jun 22;144(5):1590-1602. doi: 10.1093/brain/awab044.
Brain. 2021.
PMID: 33889945
Free PMC article.
The seizure severity score: a quantitative tool for comparing seizures and their response to therapy.
Pattnaik AR, Ghosn NJ, Ong IZ, Revell AY, Ojemann WKS, Scheid BH, Georgostathi G, Bernabei JM, Conrad EC, Sinha SR, Davis KA, Sinha N, Litt B.
Pattnaik AR, et al.
J Neural Eng. 2023 Aug 10;20(4):10.1088/1741-2552/aceca1. doi: 10.1088/1741-2552/aceca1.
J Neural Eng. 2023.
PMID: 37531949
Free PMC article.
Simulated driving in the epilepsy monitoring unit: Effects of seizure type, consciousness, and motor impairment.
Kumar A, Martin R, Chen W, Bauerschmidt A, Youngblood MW, Cunningham C, Si Y, Ezeani C, Kratochvil Z, Bronen J, Thomson J, Riordan K, Yoo JY, Shirka R, Manganas L, Krestel H, Hirsch LJ, Blumenfeld H.
Kumar A, et al.
Epilepsia. 2022 Jan;63(1):e30-e34. doi: 10.1111/epi.17136. Epub 2021 Nov 24.
Epilepsia. 2022.
PMID: 34816425
Free PMC article.
References
Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512–21.
-
PMC
-
PubMed
Gil-Nagel A, Abou-Khalil B. Electroencephalography and video-electroencephalography. Handb Clin Neurol. 2012;107:323–45.
-
PubMed
Berman R, Negishi M, Vestal M, et al. Simultaneous EEG, fMRI, and behavioral testing in typical childhood absence seizures. Epilepsia. 2010;51(10):2011–22.
-
PMC
-
PubMed
Blumenfeld H. Cellular and network mechanisms of spike-wave seizures. Epilepsia. 2005;46:21–33.
-
PubMed
Avoli M, Biagini G. Thalamocortical synchronization and absence epilepsy In: Schwartzkroin P, editor. Encyclopedia of Basic Epilepsy Research. Cambridge, MA: Academic Press, 2009; p. 28–36.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Europe PubMed Central
Ovid Technologies, Inc.
PubMed Central
Wiley
Medical
MedlinePlus Health Information