Electrical Source Imaging in Freely Moving Rats: Evaluation of a 12-Electrode Cortical Electroencephalography System
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33568980
PubMed Central
PMC7868391
DOI
10.3389/fninf.2020.589228
Knihovny.cz E-zdroje
- Klíčová slova
- auditory steady-state response experiment, electrical source imaging, electroencephalography, fieldtrip, preclinical models, translational research,
- Publikační typ
- časopisecké články MeSH
This work presents and evaluates a 12-electrode intracranial electroencephalography system developed at the National Institute of Mental Health (Klecany, Czech Republic) in terms of an electrical source imaging (ESI) technique in rats. The electrode system was originally designed for translational research purposes. This study demonstrates that it is also possible to use this well-established system for ESI, and estimates its precision, accuracy, and limitations. Furthermore, this paper sets a methodological basis for future implants. Source localization quality is evaluated using three approaches based on surrogate data, physical phantom measurements, and in vivo experiments. The forward model for source localization is obtained from the FieldTrip-SimBio pipeline using the finite-element method. Rat brain tissue extracted from a magnetic resonance imaging template is approximated by a single-compartment homogeneous tetrahedral head model. Four inverse solvers were tested: standardized low-resolution brain electromagnetic tomography, exact low-resolution brain electromagnetic tomography (eLORETA), linear constrained minimum variance (LCMV), and dynamic imaging of coherent sources. Based on surrogate data, this paper evaluates the accuracy and precision of all solvers within the brain volume using error distance and reliability maps. The mean error distance over the whole brain was found to be the lowest in the eLORETA solution through signal to noise ratios (SNRs) (0.2 mm for 25 dB SNR). The LCMV outperformed eLORETA under higher SNR conditions, and exhibiting higher spatial precision. Both of these inverse solvers provided accurate results in a phantom experiment (1.6 mm mean error distance across shallow and 2.6 mm across subcortical testing dipoles). Utilizing the developed technique in freely moving rats, an auditory steady-state response experiment provided results in line with previously reported findings. The obtained results support the idea of utilizing a 12-electrode system for ESI and using it as a solid basis for the development of future ESI dedicated implants.
Zobrazit více v PubMed
Bae J., Deshmukh A., Song Y., Riera J. (2015). Brain source imaging in preclinical rat models of focal epilepsy using high-resolution EEG recordings. J. Visual. Exp. 100:e52700. 10.3791/52700 PubMed DOI PMC
Bartelle B. B., Barandov A., Jasanoff A. (2016). Molecular fMRI. J. Neurosci. 36, 4139–4148. 10.1523/JNEUROSCI.4050-15.2016 PubMed DOI PMC
Barth Daniel S., Goldberg N., Brett B., Shi D. (1995). The spatiotemporal organization of auditory, visual, and auditory-visual evoked potentials in rat cortex. Brain Res. 678, 177–190. 10.1016/0006-8993(95)00182-P PubMed DOI
Calabrese E., Badea A., Watson C., Johnson G. A. (2013). A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability. Neuroimage 71, 196–206. 10.1016/j.neuroimage.2013.01.017 PubMed DOI PMC
Chang P., Hashemi K. S., Walker M. C. (2011). A novel telemetry system for recording EEG in small animals. J. Neurosci. Methods 201, 106–115. 10.1016/j.jneumeth.2011.07.018 PubMed DOI
Chintaluri H. C., Kowalska M., Średniawa W., Czerwiński M. B., Dzik J. M., Jȩdrzejewska-Szmek J., et al. (2019). kCSD-python, a tool for reliable current source density estimation. bioRxiv [Preprint] 708511. 10.1101/708511 DOI
Choi J. H., Koch K. P., Poppendieck W., Lee M., Shin H.-S. (2010). High resolution electroencephalography in freely moving mice. J. Neurophysiol. 104, 1825–1834. 10.1152/jn.00188.2010 PubMed DOI
Drinkenburg W. H., Ruigt G. S., Ahnaou A. (2015). Pharmaco-EEG studies in animals: an overview of contemporary translational applications. Neuropsychobiology 72, 151–164. 10.1159/000442210 PubMed DOI
Ehlers C. L., Kaneko W. M., Robledo P., Lopez A. L. (1994). Long-latency event-related potentials in rats: effects of task and stimulus parameters. Neuroscience 62, 759–769. 10.1016/0306-4522(94)90474-X PubMed DOI
Ellenbroek B., Youn J. (2016). Rodent models in neuroscience research: is it a rat race? Disease Models Mech. 9, 1079–1087. 10.1242/dmm.026120 PubMed DOI PMC
Febo M. (2011). Technical and conceptual considerations for performing and interpreting functional MRI studies in awake rats. Front. Psychiatry 2:43. 10.3389/fpsyt.2011.00043 PubMed DOI PMC
Franceschini M. A., Nissilä I., Wu W., Diamond S. G., Bonmassar G., Boas D. A. (2008). Coupling between somatosensory evoked potentials and hemodynamic response in the rat. Neuroimage 41, 189–203. 10.1016/j.neuroimage.2008.02.061 PubMed DOI PMC
Fujáková M., Pálenícek T., Brunovský M., Gorman I., Tyls F., Kubesová A., et al. . (2014). The effect of ((-)-2-oxa-4-aminobicyclo[3.1.0]hexane-2,6-dicarboxylic acid (ly379268), an mglu2/3 receptor agonist, on EEG power spectra and coherence in ketamine model of psychosis. Pharmacol. Biochem. Behav. 122, 212–221. 10.1016/j.pbb.2014.03.001 PubMed DOI
Grech R., Cassar T., Muscat J., Camilleri K. P., Fabri S. G., Zervakis M., et al. . (2008). Review on solving the inverse problem in EEG source analysis. J. Neuroeng. Rehabil. 5:25. 10.1186/1743-0003-5-25 PubMed DOI PMC
Groß J., Kujala J., Hämäläinen M., Timmermann L., Schnitzler A., Salmelin R. (2001). Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc. Natl. Acad. Sci. U.S.A. 98, 694–699. 10.1073/pnas.98.2.694 PubMed DOI PMC
Halder T., Talwar S., Jaiswal A. K., Banerjee A. (2019). Quantitative evaluation in estimating sources underlying brain oscillations using current source density methods and beamformer approaches. eNeuro 6, 1–14. 10.1523/ENEURO.0170-19.2019 PubMed DOI PMC
Hallez H., Vanrumste B., Grech R., Muscat J., De Clercq W., Vergult A., et al. . (2007). Review on solving the forward problem in EEG source analysis. J. Neuroeng. Rehabil. 4:46. 10.1186/1743-0003-4-46 PubMed DOI PMC
Hansen P. C. (2010). Discrete Inverse Problems: Insight and Algorithms, Vol. 7. Lyngby: SIAM. 10.1137/1.9780898718836 DOI
Herdman A. T., Lins O., Van Roon P., Stapells D. R., Scherg M., Picton T. W. (2002). Intracerebral sources of human auditory steady-state responses. Brain Topogr. 15, 69–86. 10.1023/A:1021470822922 PubMed DOI
Hurlbut B. J., Lubar J. F., Satterfield S. M. (1987). Auditory elicitation of the p300 event-related evoked potential in the rat. Physiol. Behav. 39, 483–487. 10.1016/0031-9384(87)90377-5 PubMed DOI
Johnson G. A., Badea A., Brandenburg J., Cofer G., Fubara B., Liu S., Nissanov J. (2010). Waxholm space: an image-based reference for coordinating mouse brain research. Neuroimage 53, 365–372. 10.1016/j.neuroimage.2010.06.067 PubMed DOI PMC
Jonmohamadi Y., Poudel G., Innes C., Weiss D., Krueger R., Jones R. (2014). Comparison of beamformers for EEG source signal reconstruction. Biomed. Signal Process. Control 14, 175–188. 10.1016/j.bspc.2014.07.014 DOI
Kim S.-W., Paik S.-H., Song K.-I., Yang S. J., Youn I., Kim B.-M., et al. (2014). Functional connectivity change of the rat brain in response to sensory stimuli using functional near-infrared brain imaging. Biomed. Eng. Lett. 4, 370–377. 10.1007/s13534-014-0166-7 DOI
Kjell J., Olson L. (2016). Rat models of spinal cord injury: from pathology to potential therapies. Disease Models Mech. 9, 1125–1137. 10.1242/dmm.025833 PubMed DOI PMC
Koudelka V., Jiricek S., Piorecka V., Vejmola C., Palenicek T., Raida Z., et al. (2018). Electrical source imaging in rats: Cortical EEG performance and limitations, in 2018 International Workshop on Computing, Electromagnetics, and Machine Intelligence (CEMi) (Stellenbosch: IEEE; ), 45–46.
Lacik J., Koudelka V., Kuratko D., Raida Z., Wojcik D. K., Mikulasek T., et al. (2020). Rat head phantom for testing of electroencephalogram source localization techniques. IEEE Access 8, 106735–106745. 10.1109/ACCESS.2020.3000581 DOI
Lee C., Oostenveld R., Lee S. H., Kim L. H., Sung H., Choi J. H. (2013). Dipole source localization of mouse electroencephalogram using the fieldtrip toolbox. PLoS ONE 8:e79442 10.1371/journal.pone.0079442 PubMed DOI PMC
Leishman E., O'Donnell B. F., Millward J. B., Vohs J. L., Rass O., Krishnan G. P., et al. (2015). Phencyclidine disrupts the auditory steady state response in rats. PLoS ONE 10:e0134979 10.1371/journal.pone.0134979 PubMed DOI PMC
Lundt A., Wormuth C., Siwek M. E., Müller R., Ehninger D., Henseler C., et al. . (2016). EEG radiotelemetry in small laboratory rodents: a powerful state-of-the art approach in neuropsychiatric, neurodegenerative, and epilepsy research. Neural Plastic. 2016. 10.1155/2016/8213878 PubMed DOI PMC
Macé E., Montaldo G., Cohen I., Baulac M., Fink M., Tanter M. (2011). Functional ultrasound imaging of the brain. Nat. Methods 8:662. 10.1038/nmeth.1641 PubMed DOI
Majka P., Kublik E., Furga G., Wójcik D. K. (2012). Common atlas format and 3d brain atlas reconstructor: infrastructure for constructing 3D brain atlases. Neuroinformatics 10, 181–197. 10.1007/s12021-011-9138-6 PubMed DOI PMC
Malmivuo J., Suihko V., Eskola H. (1997). Sensitivity distributions of EEG and MEG measurements. IEEE Trans. Biomed. Eng. 44, 196–208. 10.1109/10.554766 PubMed DOI
Mamach M., Kessler M., Bankstahl J. P., Wilke F., Geworski L., Bengel F. M., et al. . (2018). Visualization of the auditory pathway in rats with 18 F-FDG pet activation studies based on different auditory stimuli and reference conditions including cochlea ablation. PLoS ONE 13:e0205044. 10.1371/journal.pone.0205044 PubMed DOI PMC
Maris E., Oostenveld R. (2007). Nonparametric statistical testing of EEG-and MEG-data. J. Neurosci. Methods 164, 177–190. 10.1016/j.jneumeth.2007.03.024 PubMed DOI
Mathôt S., Schreij D., Theeuwes J. (2012). Opensesame: an open-source, graphical experiment builder for the social sciences. Behav. Res. Methods 44, 314–324. 10.3758/s13428-011-0168-7 PubMed DOI PMC
Medani T., Lautru D., Ren Z. (2012). Study of modeling of current dipoles in the finite element method for EEG forward problem, in Conference NUMELEC 2012 (Marseille: ).
Mégevand P., Quairiaux C., Lascano A. M., Kiss J. Z., Michel C. M. (2008). A mouse model for studying large-scale neuronal networks using EEG mapping techniques. Neuroimage 42, 591–602. 10.1016/j.neuroimage.2008.05.016 PubMed DOI
Oostenveld R., Fries P., Maris E., Schoffelen J.-M. (2011). Fieldtrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011:1. 10.1155/2011/156869 PubMed DOI PMC
Páleníček T., Fujáková M., Brunovskỳ M., Balíková M., Horáček J., Gorman I., et al. . (2011). Electroencephalographic spectral and coherence analysis of ketamine in rats: correlation with behavioral effects and pharmacokinetics. Neuropsychobiology 63, 202–218. 10.1159/000321803 PubMed DOI
Páleníček T., Fujáková M., Brunovskỳ M., Horáček J., Gorman I., Balíková M., et al. . (2013). Behavioral, neurochemical and pharmaco-EEG profiles of the psychedelic drug 4-bromo-2, 5-dimethoxyphenethylamine (2C-B) in rats. Psychopharmacology 225, 75–93. 10.1007/s00213-012-2797-7 PubMed DOI
Pascual-Marqui R. D. (2002). Standardized low-resolution brain electromagnetic tomography (sloreta): technical details. Methods Find Exp. Clin. Pharmacol. 24(Suppl D), 5–12. PubMed
Pascual-Marqui R. D. (2007). Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv preprint arXiv:0710.3341. PubMed
Pascual-Marqui R. D., Lehmann D., Koukkou M., Kochi K., Anderer P., Saletu B., et al. (2011). Assessing interactions in the brain with exact low-resolution electromagnetic tomography. Philos. Trans. Ser. A Math. Phys. Eng. Sci. 369, 3768–3784. 10.1098/rsta.2011.0081 PubMed DOI
Picton T. W., John M. S., Andrew D., David P. (2003). Human auditory steady-state responses. Int. J. Audiol. 42, 177–219. 10.3109/14992020309101316 PubMed DOI
Polich J. (2007). Updating p300: an integrative theory of p3a and p3b. Clin. Neurophysiol. 118, 2128–2148. 10.1016/j.clinph.2007.04.019 PubMed DOI PMC
Quairiaux C., Mégevand P., Kiss J. Z., Michel C. M. (2011). Functional development of large-scale sensorimotor cortical networks in the brain. J. Neurosci. 31, 9574–9584. 10.1523/JNEUROSCI.5995-10.2011 PubMed DOI PMC
Reyes S. A. Lockwood A. H. Salvi R. J. Coad M. L. Wack D. S. and Burkard, R. F. (2005). Mapping the 40-hz auditory steady-state response using current density reconstructions. Hear. Res. 204, 1–15. 10.1016/j.heares.2004.11.016 PubMed DOI
Riera J. J., Ogawa T., Goto T., Sumiyoshi A., Nonaka H., Evans A., et al. . (2012). Pitfalls in the dipolar model for the neocortical EEG sources. J. Neurophysiol. 108, 956–975. 10.1152/jn.00098.2011 PubMed DOI
Sabeti M., Katebi S. D., Rastgar K., Azimifar Z. (2016). A multi-resolution approach to localize neural sources of p300 event-related brain potential. Comput. Methods Prog. Biomed. 133, 155–168. 10.1016/j.cmpb.2016.05.013 PubMed DOI
Sekihara K., Nagarajan S. S., Poeppel D., Marantz A., Miyashita Y. (2001). Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique. IEEE Trans. Biomed. Eng. 48, 760–771. 10.1109/10.930901 PubMed DOI
Shaw N. A. (1991). A possible thalamic component of the auditory evoked potential in the rat. Brain Res. Bull. 27, 133–136. 10.1016/0361-9230(91)90295-U PubMed DOI
Shaw N. A. (1993). Auditory evoked potentials recorded from different skull locations in the rat. Int. J. Neurosci. 70, 277–283. 10.3109/00207459309000582 PubMed DOI
Shuhei Y., Howard G. T. K. R. (1993). P3-like potential in rats. Electroencephalogr. Clin. Neurophysiol. Evoked Potentials 88, 151–154. 10.1016/0168-5597(93)90066-X PubMed DOI
Song J., Davey C., Poulsen C., Luu P., Turovets S., Anderson E., et al. . (2015). EEG source localization: sensor density and head surface coverage. J. Neurosci. Methods 256, 9–21. 10.1016/j.jneumeth.2015.08.015 PubMed DOI
Steinmetz N. A., Aydin C., Lebedeva A., Okun M., Pachitariu M., Bauza M., et al. (2020). Neuropixels 2.0: a miniaturized high-density probe for stable long-term brain recordings. bioRxiv [Preprint]. 10.1101/2020.10.27.358291 PubMed DOI PMC
Sumiyoshi A., Riera J. J., Ogawa T., Kawashima R. (2011). A mini-cap for simultaneous EEG and fMRI recording in rodents. Neuroimage 54, 1951–1965. 10.1016/j.neuroimage.2010.09.056 PubMed DOI
Tarkka I. M., Stokic D. S. (1998). Source localization of p300 from oddball, single stimulus, and omitted-stimulus paradigms. Brain Topogr. 11, 141–151. 10.1023/A:1022258606418 PubMed DOI
Valdés-Hernández P. A., Bae J., Song Y., Sumiyoshi A., Aubert-Vázquez E., Riera J. J. (2019). Validating non-invasive EEG source imaging using optimal electrode configurations on a representative rat head model. Brain Topogr. 32, 599–624. 10.1007/s10548-016-0484-4 PubMed DOI
Van Nieuwenhuyse B., Raedt R., Sprengers M., Dauwe I., Gadeyne S., Carrette E., et al. . (2015). The systemic kainic acid rat model of temporal lobe epilepsy: long-term EEG monitoring. Brain Res. 1627, 1–11. 10.1016/j.brainres.2015.08.016 PubMed DOI
Van Veen B. D., Van Drongelen W., Yuchtman M., Suzuki A. (1997). Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans. Biomed. Eng. 44, 867–880. 10.1109/10.623056 PubMed DOI
Vorwerk J., Oostenveld R., Piastra M. C., Magyari L., Wolters C. H. (2018). The FieldTrip-SimBio pipeline for EEG forward solutions. Biomed. Eng. Online 17:37. 10.1186/s12938-018-0463-y PubMed DOI PMC
Watson C., Paxinos G. (2013). THE RAT BRAIN in Stereotaxic Coordinates, 7th Edn., Vol. 7. New York, NY: Academic Press.
Welniak-Kaminska M., Fiedorowicz M., Orzel J., Bogorodzki P., Modlinska K., Stryjek R., et al. . (2019). Volumes of brain structures in captive wild-type and laboratory rats: 7t magnetic resonance in vivo automatic atlas-based study. PLoS ONE 14:e0215348. 10.1371/journal.pone.0215348 PubMed DOI PMC
White A. M., Williams P. A., Ferraro D. J., Clark S., Kadam S. D., Dudek F. E., et al. . (2006). Efficient unsupervised algorithms for the detection of seizures in continuous EEG recordings from rats after brain injury. J. Neurosci. Methods 152, 255–266. 10.1016/j.jneumeth.2005.09.014 PubMed DOI
Yang H., Jiang H. (2013). Design and evaluation of a miniature probe integrating diffuse optical tomography and electroencephalographic source localization. Appl. Opt. 52, 5036–5041. 10.1364/AO.52.005036 PubMed DOI
Yang H., Zhang T., Zhou J., Carney P. R., Jiang H. (2015). In vivo imaging of epileptic foci in rats using a miniature probe integrating diffuse optical tomography and electroencephalographic source localization. Epilepsia 56, 94–100. 10.1111/epi.12880 PubMed DOI PMC
Zimmer E. R., Parent M. J., Cuello A. C., Gauthier S., Rosa-Neto P. (2014). Micropet imaging and transgenic models: a blueprint for Alzheimer's disease clinical research. Trends Neurosci. 37, 629–641. 10.1016/j.tins.2014.07.002 PubMed DOI