Standards for data acquisition and software-based analysis of in vivo electroencephalography recordings from animals. A TASK1-WG5 report of the AES/ILAE Translational Task Force of the ILAE
Corresponding Author
Jason T. Moyer
Department of Neurology, Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A
Address correspondence to Jason T. Moyer, University of Pennsylvania, 3320 Smith Walk, 301 Hayden Hall, Philadelphia, Pennsylvania 19104, U.S.A. E-mail: [email protected]
and
Aristea Galanopoulou, Albert Einstein College of Medicine, 1410 Pelham Parkway South, Kennedy Center Rm 306, Bronx, NY 10461, U.S.A. E-mail: [email protected]
Search for more papers by this authorVadym Gnatkovsky
IRCCS Foundation, Epileptology and Experimental Neurophysiology Unit, Carlo Besta Neurological Institute, Milan, Italy
These authors contributed equally to this work.Search for more papers by this authorTomonori Ono
Department of Neurosurgery, National Nagasaki Medical Center, Omura, Nagasaki, Japan
These authors contributed equally to this work.Search for more papers by this authorJakub Otáhal
Institute of Physiology, Czech Academy of Sciences, Prague, Czech Republic
These authors contributed equally to this work.Search for more papers by this authorJoost Wagenaar
Department of Neurology, Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A
Search for more papers by this authorWilliam C. Stacey
Departments of Neurology and Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, U.S.A
Search for more papers by this authorJeffrey Noebels
Department of Neurology, Baylor College of Medicine, Houston, Texas, U.S.A
Search for more papers by this authorAkio Ikeda
Department of Epilepsy, Movement Disorders and Physiology, Graduate School of Medicine, Kyoto University, Kyoto, Japan
Search for more papers by this authorKevin Staley
Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, U.S.A
Search for more papers by this authorMarco de Curtis
IRCCS Foundation, Epileptology and Experimental Neurophysiology Unit, Carlo Besta Neurological Institute, Milan, Italy
Search for more papers by this authorBrian Litt
Departments of Neurology, Neurosurgery, and Bioengineering, Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A
Search for more papers by this authorCorresponding Author
Aristea S. Galanopoulou
Laboratory of Developmental Epilepsy, Saul R. Korey Department of Neurology, Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York, U.S.A
Address correspondence to Jason T. Moyer, University of Pennsylvania, 3320 Smith Walk, 301 Hayden Hall, Philadelphia, Pennsylvania 19104, U.S.A. E-mail: [email protected]
and
Aristea Galanopoulou, Albert Einstein College of Medicine, 1410 Pelham Parkway South, Kennedy Center Rm 306, Bronx, NY 10461, U.S.A. E-mail: [email protected]
Search for more papers by this authorCorresponding Author
Jason T. Moyer
Department of Neurology, Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A
Address correspondence to Jason T. Moyer, University of Pennsylvania, 3320 Smith Walk, 301 Hayden Hall, Philadelphia, Pennsylvania 19104, U.S.A. E-mail: [email protected]
and
Aristea Galanopoulou, Albert Einstein College of Medicine, 1410 Pelham Parkway South, Kennedy Center Rm 306, Bronx, NY 10461, U.S.A. E-mail: [email protected]
Search for more papers by this authorVadym Gnatkovsky
IRCCS Foundation, Epileptology and Experimental Neurophysiology Unit, Carlo Besta Neurological Institute, Milan, Italy
These authors contributed equally to this work.Search for more papers by this authorTomonori Ono
Department of Neurosurgery, National Nagasaki Medical Center, Omura, Nagasaki, Japan
These authors contributed equally to this work.Search for more papers by this authorJakub Otáhal
Institute of Physiology, Czech Academy of Sciences, Prague, Czech Republic
These authors contributed equally to this work.Search for more papers by this authorJoost Wagenaar
Department of Neurology, Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A
Search for more papers by this authorWilliam C. Stacey
Departments of Neurology and Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, U.S.A
Search for more papers by this authorJeffrey Noebels
Department of Neurology, Baylor College of Medicine, Houston, Texas, U.S.A
Search for more papers by this authorAkio Ikeda
Department of Epilepsy, Movement Disorders and Physiology, Graduate School of Medicine, Kyoto University, Kyoto, Japan
Search for more papers by this authorKevin Staley
Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, U.S.A
Search for more papers by this authorMarco de Curtis
IRCCS Foundation, Epileptology and Experimental Neurophysiology Unit, Carlo Besta Neurological Institute, Milan, Italy
Search for more papers by this authorBrian Litt
Departments of Neurology, Neurosurgery, and Bioengineering, Center for Neuroengineering and Therapeutics, University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A
Search for more papers by this authorCorresponding Author
Aristea S. Galanopoulou
Laboratory of Developmental Epilepsy, Saul R. Korey Department of Neurology, Dominick P. Purpura Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York, U.S.A
Address correspondence to Jason T. Moyer, University of Pennsylvania, 3320 Smith Walk, 301 Hayden Hall, Philadelphia, Pennsylvania 19104, U.S.A. E-mail: [email protected]
and
Aristea Galanopoulou, Albert Einstein College of Medicine, 1410 Pelham Parkway South, Kennedy Center Rm 306, Bronx, NY 10461, U.S.A. E-mail: [email protected]
Search for more papers by this authorSummary
Electroencephalography (EEG)—the direct recording of the electrical activity of populations of neurons—is a tremendously important tool for diagnosing, treating, and researching epilepsy. Although standard procedures for recording and analyzing human EEG exist and are broadly accepted, there are no such standards for research in animal models of seizures and epilepsy—recording montages, acquisition systems, and processing algorithms may differ substantially among investigators and laboratories. The lack of standard procedures for acquiring and analyzing EEG from animal models of epilepsy hinders the interpretation of experimental results and reduces the ability of the scientific community to efficiently translate new experimental findings into clinical practice. Accordingly, the intention of this report is twofold: (1) to review current techniques for the collection and software-based analysis of neural field recordings in animal models of epilepsy, and (2) to offer pertinent standards and reporting guidelines for this research. Specifically, we review current techniques for signal acquisition, signal conditioning, signal processing, data storage, and data sharing, and include applicable recommendations to standardize collection and reporting. We close with a discussion of challenges and future opportunities, and include a supplemental report of currently available acquisition systems and analysis tools. This work represents a collaboration on behalf of the American Epilepsy Society/International League Against Epilepsy (AES/ILAE) Translational Task Force (TASK1-Workgroup 5), and is part of a larger effort to harmonize video-EEG interpretation and analysis methods across studies using in vivo and in vitro seizure and epilepsy models.
Supporting Information
| Filename | Description |
|---|---|
| epi13909-sup-0001-TableS1.docxWord document, 125.6 KB |
Table S1. Acquisition systems. Table S2. Analysis software. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1Niedermeyer E. Historical aspects. In E Niedermeyer, F Lopes da Silva (Eds) Electroencephalography: basic principles, clinical applications, and related fields. Philadelphia: Lippincott Williams and Wilkins, 2005: 1–16.
- 2Westbrook G. Seizures and epilepsy. In E Kandel, T Schwartz, T Jessell, et al. (Eds) Principles of neural science. New York: McGraw Hill Professional, 2013: 1116–1139.
- 3 American Clinical Neurophysiology Society. Guideline 6: a proposal for standard montages to be used in clinical eeg. J Clin Neurophysiol 2006; 23: 111–117.
- 4Hirsch LJ, LaRoche SM, Gaspard N, et al. American clinical neurophysiology society's standardized critical care eeg terminology: 2012 version. J Clin Neurophysiol 2013; 30: 1–27.
- 5Noachtar S, Binnie C, Ebersole J, et al. A glossary of terms most commonly used by clinical electroencephalographers and proposal for the report form for the eeg findings. The international federation of clinical neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999; 52: 21–41.
- 6 International Electrotechnical Commission. IEC 60601-1:2015. Medical Electrical Equipment - Part 1: General requirements for basic safety and essential performance. Geneva, Switzerland. See https://www.iso.org/standard/65529.html. Accessed October 12, 2017.
- 7Sherman-Gold R. The axon guide for electrophysiology and biophysics: laboratory techniques. Foster City, CA: Axon Instruments, Inc. 1993.
- 8Isley MR, Krauss GL, Levin KH, et al. Electromyography/electroencephalography. Redmond, WA: SpaceLabs Medical; 1993.
- 9Nagel JH. Biopotential amplifiers. In JD Bronzino, DR Peterson (Eds) The biomedical engineering handbook, Vol. 4: medical devices and engineering. Boca Raton, FL: CRC Press, LLC, 2014: 9–16.
- 10Olson WH. Electrical safety. In JG Webster (Ed) Medical instrumentation: application and design. New York: John Wiley & Sons; 2010: 638–675.
- 11Mathew G. Medical Devices Isolation: How Safe is Safe Enough, 2002. Available at: https://www.wipro.com/documents/whitepaper/Whitepaper-Medical Devices Isolation-%C3%B4How safe is safe enough%C3%B6.pdf. Accessed July 31, 2016.
- 12Prutchi D, Norris M. Design and development of medical electronic instrumentation: a practical perspective of the design, construction, and test of medical devices. New York: John Wiley & Sons; 2005.
- 13Webster JG. Amplifiers and signal processing. In JG Webster (Ed) Medical instrumentation: application and design. New York: John Wiley & Sons; 2010: 91–125.
- 14Reilly EL. Eeg recording and operation of the apparatus. In E Niedermeyer, F Lopes da Silva (Eds) Electroencephalography: basic principles, clinical applications, and related fields. Philadelphia: Lippincott Williams and Wilkins; 2005: 139–159.
- 15Bertram EH. Monitoring for seizures in rodents. In A Pitkanen, PA Schwartzkroin, SL Moshe (Eds) Models of seizures and epilepsy. Burlington, MA, USA: Elsevier Academic Press; 2006: 569–582.
- 16Rensing NR, Guo D, Wong M. Video-eeg monitoring methods for characterizing rodent models of tuberous sclerosis and epilepsy. In T Weichhart (Ed) Mtor: methods and protocols. New York: Humana Press; 2012: 373–391.
10.1007/978-1-61779-430-8_24 Google Scholar
- 17Galanopoulou AS, Kokaia M, Loeb JA, et al. Epilepsy therapy development: technical and methodologic issues in studies with animal models. Epilepsia 2013; 54(Suppl. 4): 13–23.
- 18Smith SW. The scientist and engineer's guide to digital signal processing. San Diego, CA: California Technical Publishers; 1997.
- 19Krauss GL, Webber WRS. Digital eeg. In E Niedermeyer, F Lopes da Silva (Eds) Electroencephalography: basic principles, clinical applications, and related fields. Philadelphia: Lippincott Williams and Wilkins; 2005: 797–813.
- 20Lesser RP, Webber WRS. Principles of computerized epilepsy monitoring. In E Niedermeyer, F Lopes da Silva (Eds) Electroencephalography: basic principles, clinical applications, and related fields. Philadelphia: Lippincott Williams and Wilkins, 2005: 791–796.
- 21Shannon CE. Communication in the presence of noise. Proc Inst Radio Eng 1949; 37: 10–21.
- 22Nyquist H. Certain topics in telegraph transmission theory. Trans Am Inst Electric Eng 1928; 47: 617–644.
10.1109/T-AIEE.1928.5055024 Google Scholar
- 23Mainardi LT, Bianchi AM, Cerutti S. Digital biomedical signal acquisition and processing. In JD Bronzino, DR Peterson (Eds) The biomedical engineering handbook, vol. 3: biomedical signals, imaging, and informatics. New York: CRC Press LLC, 2014: 1–24.
- 24van Drongelen W. Signal processing for neuroscientists: an introduction to the analysis of physiological signals. Burlington, MA: Academic Press; 2006.
- 25Widmann A, Schroger E, Maess B. Digital filter design for electrophysiological data–a practical approach. J Neurosci Methods 2015; 250: 34–46.
- 26Ifeachor E, Jervis B. Digital signal processing: a practical approach. Upper Saddle River, NJ: Prentice Hall, 2002.
- 27Gliske SV, Irwin ZT, Chestek C, et al. Effect of sampling rate and filter settings on high frequency oscillation detections. Clin Neurophysiol 2016; 127: 3042–3050.
- 28 Practical Introduction to Digital Filter Design. Available at: http://www.mathworks.com/help/signal/examples/practical-introduction-to-digital-filter-design.html?requestedDomain=www.mathworks.com. Accessed July 31, 2016.
- 29Wesson KD, Ochshorn RM, Land BR. Low-cost, high-fidelity, adaptive cancellation of periodic 60 hz noise. J Neurosci Methods 2009; 185: 50–55.
- 30Northrop RB. Signals and systems analysis in biomedical engineering. Boca Raton, FL: CRC Press, Taylor & Francis Group; 2010.
- 31Qian S, Chen D. Joint time-frequency analysis: methods and applications. Upper Saddle River, NJ: PTR Prentice Hall; 1996.
- 32Walker JS. A primer on wavelets and their scientific applications. New York: Chapman and Hall/CRC; 2008.
10.1201/9781584887461 Google Scholar
- 33Castellanos NP, Makarov VA. Recovering eeg brain signals: artifact suppression with wavelet enhanced independent component analysis. J Neurosci Methods 2006; 158: 300–312.
- 34Wilson SB, Emerson R. Spike detection: a review and comparison of algorithms. Clin Neurophysiol 2002; 113: 1873–1881.
- 35Latka M, Was Z, Kozik A, et al. Wavelet analysis of epileptic spikes. Phys Rev E Stat Nonlin Soft Matter Phys 2003; 67: 052902.
- 36Kadam SD, D'Ambrosio R, Duveau S, et al. Methodological standards and interpretation of video-EEG in adult control rodents. A TASK1-WG1 report of the AES/ILAE Translational Task Force of the ILAE. Epilepsia 2017; 58(Suppl. 4): 10–27.
- 37del Campo CM, Velazquez JL, Freire MA. Eeg recording in rodents, with a focus on epilepsy. Curr Protoc Neurosci 2009; Chapter 6:Unit 6 24.
- 38Nolan H, Whelan R, Reilly RB. Faster: fully automated statistical thresholding for eeg artifact rejection. J Neurosci Methods 2010; 192: 152–162.
- 39Kelleher D, Temko A, Orregan S, et al. Parallel artefact rejection for epileptiform activity detection in routine eeg. Conf Proc IEEE Eng Med Biol Soc 2011; 2011: 7953–7956.
- 40LeVan P, Urrestarazu E, Gotman J. A system for automatic artifact removal in ictal scalp eeg based on independent component analysis and bayesian classification. Clin Neurophysiol 2006; 117: 912–927.
- 41Chaumon M, Bishop DV, Busch NA. A practical guide to the selection of independent components of the electroencephalogram for artifact correction. J Neurosci Methods 2015; 250: 47–63.
- 42Delorme A, Sejnowski T, Makeig S. Enhanced detection of artifacts in eeg data using higher-order statistics and independent component analysis. NeuroImage 2007; 34: 1443–1449.
- 43Hamaneh MB, Chitravas N, Kaiboriboon K, et al. Automated removal of ekg artifact from eeg data using independent component analysis and continuous wavelet transformation. IEEE Trans Biomed Eng 2014; 61: 1634–1641.
- 44Lopes da Silva F. Eeg analysis: theory and practice. In E Niedermeyer, F Lopes da Silva (Eds) Electroencephalography: basic principles, clinical applications, and related fields. Philadelphia, PA, USA: Lippincott Williams and Wilkins; 2005: 1199–1231.
- 45Brinkmann BH, Bower MR, Stengel KA, et al. Multiscale electrophysiology format: an open-source electrophysiology format using data compression, encryption, and cyclic redundancy check. Conf Proc IEEE Eng Med Biol Soc 2009; 2009: 7083–7086.
- 46Brinkmann BH, Bower MR, Stengel KA, et al. Large-scale electrophysiology: acquisition, compression, encryption, and storage of big data. J Neurosci Methods 2009; 180: 185–192.
- 47Stead M, Halford JJ. A proposal for a standard format for neurophysiology data recording and exchange. J Clin Neurophysiol 2016; 33: 403–413.
- 48Teeters JL, Godfrey K, Young R, et al. Neurodata without borders: creating a common data format for neurophysiology. Neuron 2015; 88: 629–634.
- 49Kemp B, Varri A, Rosa AC, et al. A simple format for exchange of digitized polygraphic recordings. Electroencephalogr Clin Neurophysiol 1992; 82: 391–393.
- 50Kemp B, Olivan J. European data format ‘plus’ (edf+), an edf alike standard format for the exchange of physiological data. Clin Neurophysiol 2003; 114: 1755–1761.
- 51Wagenaar JB, Worrell GA, Ives Z, et al. Collaborating and sharing data in epilepsy research. J Clin Neurophysiol 2015; 32: 235–239.
- 52Liang SF, Shaw FZ, Young CP, et al. A closed-loop brain computer interface for real-time seizure detection and control. Conf Proc IEEE Eng Med Biol Soc 2010; 2010: 4950–4953.
- 53Nelson TS, Suhr CL, Freestone DR, et al. Closed-loop seizure control with very high frequency electrical stimulation at seizure onset in the gaers model of absence epilepsy. Int J Neural Syst 2011; 21: 163–173.
- 54Zayachkivsky A, Lehmkuhle MJ, Dudek FE. Long-term continuous eeg monitoring in small rodent models of human disease using the epoch wireless transmitter system. J Vis Exp 2015; 101: e52554.
- 55Kuzum D, Takano H, Shim E, et al. Transparent and flexible low noise graphene electrodes for simultaneous electrophysiology and neuroimaging. Nat Commun 2014; 5: 5259.
- 56Baldassano SN, Brinkmann BH, Ung H, et al. Crowdsourcing seizure detection: algorithm development and validation on human implanted device recordings. Brain 2017; 140:1680–1691.
- 57Vanhatalo S, Palva JM, Andersson S, et al. Slow endogenous activity transients and developmental expression of k+-cl- cotransporter 2 in the immature human cortex. Eur J Neurosci 2005; 22: 2799–2804.
- 58Myers KA, Bello-Espinosa LE, Wei XC, et al. Infraslow eeg changes in infantile spasms. J Clin Neurophysiol 2014; 31: 600–605.
- 59Thordstein M, Lofgren N, Flisberg A, et al. Infraslow eeg activity in burst periods from post asphyctic full term neonates. Clin Neurophysiol 2005; 116: 1501–1506.
- 60Vanhatalo S, Holmes MD, Tallgren P, et al. Very slow eeg responses lateralize temporal lobe seizures: an evaluation of non-invasive dc-eeg. Neurology 2003; 60: 1098–1104.
- 61Bragin A, Engel J Jr, Staba RJ. High-frequency oscillations in epileptic brain. Curr Opin Neurol 2010; 23: 151–156.
- 62 Open, Industry-Standard File Format for Neurophysiological Data, 2000. Available at: http://neuroshare.sourceforge.net/API-Documentation/sfn00meeting_agenda.pdf. Accessed July 31, 2016.
