Tackling the challenges of group network inference from intracranial EEG data

. 2022 ; 16 () : 1061867. [epub] 20221201

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36532288

INTRODUCTION: Intracranial EEG (iEEG) data is a powerful way to map brain function, characterized by high temporal and spatial resolution, allowing the study of interactions among neuronal populations that orchestrate cognitive processing. However, the statistical inference and analysis of brain networks using iEEG data faces many challenges related to its sparse brain coverage, and its inhomogeneity across patients. METHODS: We review these challenges and develop a methodological pipeline for estimation of network structure not obtainable from any single patient, illustrated on the inference of the interaction among visual streams using a dataset of 27 human iEEG recordings from a visual experiment employing visual scene stimuli. 100 ms sliding window and multiple band-pass filtered signals are used to provide temporal and spectral resolution. For the connectivity analysis we showcase two connectivity measures reflecting different types of interaction between regions of interest (ROI): Phase Locking Value as a symmetric measure of synchrony, and Directed Transfer Function-asymmetric measure describing causal interaction. For each two channels, initial uncorrected significance testing at p < 0.05 for every time-frequency point is carried out by comparison of the data-derived connectivity to a baseline surrogate-based null distribution, providing a binary time-frequency connectivity map. For each ROI pair, a connectivity density map is obtained by averaging across all pairs of channels spanning them, effectively agglomerating data across relevant channels and subjects. Finally, the difference of the mean map value after and before the stimulation is compared to the same statistic in surrogate data to assess link significance. RESULTS: The analysis confirmed the function of the parieto-medial temporal pathway, mediating visuospatial information between dorsal and ventral visual streams during visual scene analysis. Moreover, we observed the anterior hippocampal connectivity with more posterior areas in the medial temporal lobe, and found the reciprocal information flow between early processing areas and medial place area. DISCUSSION: To summarize, we developed an approach for estimating network connectivity, dealing with the challenge of sparse individual coverage of intracranial EEG electrodes. Its application provided new insights into the interaction between the dorsal and ventral visual streams, one of the iconic dualities in human cognition.

Zobrazit více v PubMed

Aguirre G. K., D'Esposito M. (1999). Topographical disorientation: a synthesis and taxonomy. Brain 122, 1613–1628. 10.1093/brain/122.9.1613 PubMed DOI

Baccalá L., Sameshima K., Baccala L. A., Sameshima K. (2001). Partial directed coherence: a new concept in neural structure determination. Biol. Cybern. 84, 463–474. 10.1007/PL00007990 PubMed DOI

Baccalá L. A., Sameshima K. (2021). Partial directed coherence: twenty years on some history and an appraisal. Biol Cybern. 115, 195–204. 10.1007/s00422-021-00880-y PubMed DOI

Baldassano C., Esteva A., Beck D., Fei-Fei L. (2016). Two distinct scene processing networks connecting vision and memory. J. Vis. 3, 1–16. 10.1523/ENEURO.0178-16.2016 PubMed DOI PMC

Barnett L., Seth A. K. (2014). The mvgc multivariate Granger causality toolbox: a new approach to Granger-causal inference. J. Neurosci. Methods 223, 50–68. 10.1016/j.jneumeth.2013.10.018 PubMed DOI

Bastin J., Deman P., David O., Gueguen M., Benis D., Minotti L., et al. . (2017). Direct recordings from human anterior insula reveal its leading role within the error-monitoring network. Cereb. Cortex 27, 1545–1557. 10.1093/cercor/bhv352 PubMed DOI

Bastin J., Vidal J. R., Bouvier S., Perrone-Bertolotti M., Bénis D., Kahane P., et al. . (2013). Temporal components in the parahippocampal place area revealed by human intracerebral recordings. J. Neurosci. 33, 10123–10131. 10.1523/JNEUROSCI.4646-12.2013 PubMed DOI PMC

Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300. 10.1111/j.2517-6161.1995.tb02031.x DOI

Biswal B. B., Mennes M., Zuo X.-N., Gohel S., Kelly C., Smith S. M., et al. . (2010). Toward discovery science of human brain function. Proc. Natl. Acad. Sci. U.S.A. 107, 4734–4739. 10.1073/pnas.0911855107 PubMed DOI PMC

Blinowska K. J., Malinowski M. (1991). Non-linear and linear forecasting of the EEG time series. Biol. Cybern. 66, 159–165. 10.1007/BF00243291 PubMed DOI

Boccia M., Sulpizio V., Nemmi F., Guariglia C., Galati G. (2017). Direct and indirect parieto-medial temporal pathways for spatial navigation in humans: evidence from resting-state functional connectivity. Brain Struct. Funct. 222, 1945–1957. 10.1007/s00429-016-1318-6 PubMed DOI

Bullmore E., Sporns O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186–198. 10.1038/nrn2575 PubMed DOI

Burke J. F., Sharan A. D., Sperling M. R., Ramayya A. G., Evans J. J., Healey M. K., et al. . (2014). Theta and high-frequency activity mark spontaneous recall of episodic memories. J. Neurosci. 34, 11355–11365. 10.1523/JNEUROSCI.2654-13.2014 PubMed DOI PMC

Burke J. F., Zaghlou K. A., Jacobs J., Williams R. B., Sperling M. R., Sharan A. D., et al. . (2013). Synchronous and asynchronous theta and gamma activity during episodic memory formation. J. Neurosci. 33, 292–304. 10.1523/JNEUROSCI.2057-12.2013 PubMed DOI PMC

Byrne P., Becker S., Burgess N. (2007). Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375. 10.1037/0033-295X.114.2.340 PubMed DOI PMC

Cavanna A. E., Trimble M. R. (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564–583. 10.1093/brain/awl004 PubMed DOI

Cloutman L. L. (2013). Interaction between dorsal and ventral processing streams: where, when and how? Brain Lang. 127, 251–263. 10.1016/j.bandl.2012.08.003 PubMed DOI

Dauwels J., Vialatte F., Musha T., Cichocki A. (2010). A comparative study of synchrony measures for the early diagnosis of Alzheimer's disease based on EEG. Neuroimage 49, 668–693. 10.1016/j.neuroimage.2009.06.056 PubMed DOI

Epstein R., Kanwisher N. (1998). A cortical representation of the local visual environment. Nature 392, 598–601. 10.1038/33402 PubMed DOI

Epstein R. A., Baker C. I. (2019). Scene perception in the human brain. Ann. Rev. 5, 373–397. 10.1146/annurev-vision-091718-014809 PubMed DOI PMC

Friston K. J. (1994). Functional and effective connectivity in neuroimaging: a synthesis. Hum. Brain Mapp. 2, 56–78. 10.1002/hbm.460020107 DOI

Friston K. J., Frith C. D., Liddle P. F., Frackowiak R. S. J. (1993). Functional connectivity-the principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab. 13, 5–14. 10.1038/jcbfm.1993.4 PubMed DOI

Goodale M. A., Milner A. D. (1992). Separate visual pathways for perception and action. Trends Neurosci. 15, 20–25. 10.1016/0166-2236(92)90344-8 PubMed DOI

Hartman D., Hlinka J., Palus M., Mantini D., Corbetta M. (2011). The role of nonlinearity in computing graph-theoretical properties of resting-state functional magnetic resonance imaging brain networks. Chaos 21, 013119. 10.1063/1.3553181 PubMed DOI PMC

Haufe S., Nikulin V. V., Nolte G. (2012). Alleviating the influence of weak data asymmetries on Granger-causal analyses. Lecture Notes Compute. Sci. 7191 LNCS, 25–33. 10.1007/978-3-642-28551-6_4 DOI

Henriksson L., Mur M., Kriegeskorte N. (2019). Rapid invariant encoding of scene layout in human OPA. Neuron 103, 161.e3–171.e3. 10.1016/j.neuron.2019.04.014 PubMed DOI

Hlinka J., Hartman D., Vejmelka M., Runge J., Marwan N., Kurths J., et al. . (2013). Reliability of inference of directed climate networks using conditional mutual information. Entropy 15, 2023–2045. 10.3390/e15062023 DOI

Hlinka J., Paluš M., Vejmelka M., Mantini D., Corbetta M. (2011). Functional connectivity in resting-state fMRI: Is linear correlation sufficient? Neuroimage 54, 2218–2225. 10.1016/j.neuroimage.2010.08.042 PubMed DOI PMC

Hochberg Y. (1988). A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75, 800–802. 10.1093/biomet/75.4.800 DOI

Kalman R. (1960). A new approach to linear filtering and prediction problems. J. Basic Eng. 82, 35–44. 10.1115/1.3662552 PubMed DOI

Kaminski M., Ding M., Truccolo W. A., Bressler S. L. (2001). Evaluating causal relations in neural systems: granger causality, directed transfer function and statistical assessment of significance. Biol. Cybern. 85, 145–157. 10.1007/s004220000235 PubMed DOI

Kaminski M. J., Blinowska K. J. (1991). A new method of the description of the information flow in the brain structures. Biol. Cybern. 65, 203–210. 10.1007/BF00198091 PubMed DOI

Kořenek J., Hlinka J. (2020). Causal network discovery by iterative conditioning: comparison of algorithms. Chaos 30, 013117. 10.1063/1.5115267 PubMed DOI

Korenek J., Hlinka J. (2021). Causality in reversed time series: reversed or conserved? Entropy 23, 1–22. 10.3390/e23081067 PubMed DOI PMC

Kravitz D. J., Saleem K. S., Baker C. I., Mishkin M. (2011). A new neural framework for visuospatial processing. Nat. Rev. Neurosci. 12, 217–230. 10.1038/nrn3008 PubMed DOI PMC

Kristensen S., Garcea F. E., Mahon B. Z., Almeida J. (2016). Temporal frequency tuning reveals interactions between the dorsal and ventral visual streams. J. Cogn. Neurosci. 28, 1295–1302. 10.1162/jocn_a_00969 PubMed DOI PMC

Lachaux J.-,p., Rodriguez E., Martinerie J., Varela F. J. (1999). Measuring phase synchrony in brain signals. Hum. Brain Mapp. 208, 194–208. 10.1002/(SICI)1097-0193(1999)8:4<194::AID-HBM4>3.0.CO;2-C PubMed DOI PMC

Libby L. A., Ekstrom A. D., Ragland J. D., Ranganath C. (2012). Differential connectivity of perirhinal and parahippocampal cortices within human hippocampal subregions revealed by high-resolution functional imaging. J. Neurosci. 32, 6550–6560. 10.1523/JNEUROSCI.3711-11.2012 PubMed DOI PMC

Lütkepohl H. (2005). New Introduction to Multiple Time Series Analysis. Berlin; Heidelberg: Springer-Verlag Berlin Heidelberg.

Mantini D., Hasson U., Betti V., Perrucci M. G., Romani G. L., Corbetta M., et al. . (2012). Interspecies activity correlations reveal functional correspondence between monkey and human brain areas. Nat. Methods 9, 277-U85. 10.1038/nmeth.1868 PubMed DOI PMC

Morgan L. K., MacEvoy S. P., Aguirre G. K., Epstein R. A. (2011). Distances between real-world locations are represented in the human hippocampus. J. Neurosci. 31, 1238–1245. 10.1523/JNEUROSCI.4667-10.2011 PubMed DOI PMC

Namburi P. (2011). Phase Locking Value. Available online at: https://se.mathworks.com/matlabcentral/fileexchange/31600-phase-locking-value.

Neumaier A., Schneider T. (2001). Estimation of parameters and eigenmodes of multivariate autoregressive models. ACM Trans. Math. Softw. 27, 27–57. 10.1145/382043.382304 DOI

Omidvarnia A. (2020). Time-Varying EEG Connectivity: A Time-Frequency Approach. Available online at: https://www.mathworks.com/matlabcentral/fileexchange/33721-time-varying-eeg-connectivity-a-time-frequency-approach.

Omidvarnia A., Mesbah M., O'Toole J., Colditz P., Boashash B. (2011). “Analysis of the time-varying cortical neural connectivity in the newborn EEG: a time-frequency approach,” in 2011 7th International Workshop on Systems, Signal Processing and their Applications (WOSSPA) (Tipaza: ), 179–182.

Poppenk J., Evensmoen H. R., Moscovitch M., Nadel L. (2013). Long-axis specialization of the human hippocampus. Trends Cogn. Sci. 17, 230–240. 10.1016/j.tics.2013.03.005 PubMed DOI

Prichard D., Theiler J. (1994). Generating surrogate data for time series with several simultaneously measured variables. Phys. Rev. Lett. 73, 951–954. 10.1103/PhysRevLett.73.951 PubMed DOI

Pruessner J. C., Köhler S., Crane J., Pruessner M., Lord C., Byrne A., et al. . (2002). Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. Cereb. Cortex 12, 1342–1353. 10.1093/cercor/12.12.1342 PubMed DOI

Sameshima K., Baccalá L. A. (1999). Using partial directed coherence to describe neuronal ensemble interactions. J. Neurosci. Methods 94, 93–103. 10.1016/S0165-0270(99)00128-4 PubMed DOI

Save E., Paz-Villagran V., Alexinsky T., Poucet B. (2005). Functional interaction between the associative parietal cortex and hippocampal place cell firing in the rat. Eur. J. Neurosci. 21, 522–530. 10.1111/j.1460-9568.2005.03882.x PubMed DOI

Seth A. K. (2010). A matlab toolbox for granger causal connectivity analysis. J. Neurosci. Methods 186, 262–273. 10.1016/j.jneumeth.2009.11.020 PubMed DOI

Strange B. A., Witter M. P., Lein E. S., Moser E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 15, 655–669. 10.1038/nrn3785 PubMed DOI

Ungerleider L., Mishkin M. (1982). “Two visual streams,” in Analysis of Visual Behavior, eds D. Ingle, M. Goodale, and R. Mansfield (Cambridge, MA: MIT Press; ), 549–586.

Vlcek K., Fajnerova I., Nekovarova T., Hejtmanek L., Janca R., Jezdik P., et al. . (2020). Mapping the scene and object processing networks by intracranial EEG. Front. Hum. Neurosci. 14, 561399. 10.3389/fnhum.2020.561399 PubMed DOI PMC

Winkler I., Panknin D., Bartz D., Muller K. R., Haufe S. (2016). Validity of time reversal for testing granger causality. IEEE Trans. Signal Process. 64, 2746–2760. 10.1109/TSP.2016.2531628 PubMed DOI

Xia M., Wang J., He Y. (2013). BrainNet viewer: a network visualization tool for human brain connectomics. PLoS ONE 8, e68910. 10.1371/journal.pone.0068910 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...