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Effective Connectivity of Cortical Sensorimotor Networks During Finger Movement Tasks: A Simultaneous fNIRS, fMRI, EEG Study

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Abstract

Recently, interest has been growing to understand the underlying dynamic directional relationship between simultaneously activated regions of the brain during motor task performance. Such directionality analysis (or effective connectivity analysis), based on non-invasive electrophysiological (electroencephalography—EEG) and hemodynamic (functional near infrared spectroscopy—fNIRS; and functional magnetic resonance imaging—fMRI) neuroimaging modalities can provide an estimate of the motor task-related information flow from one brain region to another. Since EEG, fNIRS and fMRI modalities achieve different spatial and temporal resolutions of motor-task related activation in the brain, the aim of this study was to determine the effective connectivity of cortico-cortical sensorimotor networks during finger movement tasks measured by each neuroimaging modality. Nine healthy subjects performed right hand finger movement tasks of different complexity (simple finger tapping-FT, simple finger sequence-SFS, and complex finger sequence-CFS). We focused our observations on three cortical regions of interest (ROIs), namely the contralateral sensorimotor cortex (SMC), the contralateral premotor cortex (PMC) and the contralateral dorsolateral prefrontal cortex (DLPFC). We estimated the effective connectivity between these ROIs using conditional Granger causality (GC) analysis determined from the time series signals measured by fMRI (blood oxygenation level-dependent-BOLD), fNIRS (oxygenated-O2Hb and deoxygenated-HHb hemoglobin), and EEG (scalp and source level analysis) neuroimaging modalities. The effective connectivity analysis showed significant bi-directional information flow between the SMC, PMC, and DLPFC as determined by the EEG (scalp and source), fMRI (BOLD) and fNIRS (O2Hb and HHb) modalities for all three motor tasks. However the source level EEG GC values were significantly greater than the other modalities. In addition, only the source level EEG showed a significantly greater forward than backward information flow between the ROIs. This simultaneous fMRI, fNIRS and EEG study has shown through independent GC analysis of the respective time series that a bi-directional effective connectivity occurs within a cortico-cortical sensorimotor network (SMC, PMC and DLPFC) during finger movement tasks.

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Acknowledgments

This work was supported by the German Research Council (SFB 855, projects D2 and D3). Dr. Muthalib is supported by a Labex NUMEV Fellowship (Digital and Hardware Solutions, Environmental and Organic Life Modeling, ANR-10-LABX-20). The funding does not have any involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, and in the decision to submit the article for publication. We would also like to thank Marco Dat for assisting with the experimental setup.

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    Authors and Affiliations

    1. Faculty of Digital Signal Processing and System Theory, University of Kiel, Kiel, Germany

      A. R. Anwar & U. Heute

    2. Biomedical Engineering Department, UET Lahore (KSK), Lahore, Pakistan

      A. R. Anwar

    3. EuroMov, University of Montpellier, Montpellier, France

      M. Muthalib & S. Perrey

    4. Movement Neuroscience, Queensland University of Technology, Brisbane, Australia

      M. Muthalib

    5. Department of Neuropediatrics, University of Kiel, Kiel, Germany

      A. Galka

    6. Department of Neurology, University of Kiel, Kiel, Germany

      O. Granert, G. Deuschl, J. Raethjen & Muthuraman Muthuraman

    7. Department of Neuroradiology, University of Kiel, Kiel, Germany

      S. Wolff

    8. Department of Neurology, Johannes Gutenberg University, Mainz, Germany

      Muthuraman Muthuraman

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    10548_2016_507_MOESM1_ESM.tif

    Supplementary Fig. 1. The preprocessing and conditional granger causality (GC) analysis steps for the fNIRS (red), MRI (blue) and EEG (green) modalities are represented as a flow chart. The GC and the surrogate analysis that are common for all the three modalities are represented in black. Supplementary material 1 (TIFF 2700 kb)

    10548_2016_507_MOESM2_ESM.tif

    Supplementary Fig. 2. The mean group block averaged time course of activation measured by (row 1) fMRI (BOLD), (row 2) fNIRS (O2Hb and HHb), (row 3) EEG-scalp and (row 4) EEG-source from the contralateral sensorimotor cortex (SMC-Blue lines), premotor cortex (PMC-red dashed line) and dorsolateral prefrontal cortex (DLPFC-green dotted line) ROIs during the finger tapping (FT), simple finger sequence (SFS), and complex finger sequence (CFS) tasks of the right hand. The task period starts at 0 s and ends at 30 s. The horizontal black dashed line indicates the significance level in the EEG dynamical coherence plots for the EEG-scalp (row 3) and EEG-source (row 4). Supplementary material 2 (TIFF 3922 kb)

    10548_2016_507_MOESM3_ESM.tif

    Supplementary Fig. 3. A) The mean group time varying directed Granger causality (GC) analysis for the EEG modality during the finger tapping (FT-column 1), simple finger sequence (SFS-column 2) and complex finger sequence (CFS-column 3) tasks of the right hand. Row 1 and Row 3 shows the mean GC values of all forward connections for the EEG-scalp and EEG-source, respectively (PMC → SMC, DLPFC → SMC and DLPFC → SMC). Row 2 and Row 4 shows the mean GC values for the backward connections for the EEG-scalp and EEG-source, respectively (SMC → PMC, SMC → DLPFC and PMC → DLPFC). Supplementary material 3 (TIFF 75 kb)

    10548_2016_507_MOESM4_ESM.tif

    Supplementary Fig. 3 B). The mean group time varying directed Granger causality (GC) analysis for the fNIRS modality during the finger tapping (FT-column 1), simple finger sequence (SFS-column 2) and complex finger sequence (CFS-column 3) tasks. Row 1 and Row 3 shows the mean GC values of all forward connections for the fNIRS-O2Hb and fNIRS-HHb, respectively (PMC → SMC, DLPFC → SMC and DLPFC → SMC). Row 2 and Row 4 shows the mean GC values of all backward connections for the fNIRS-O2Hb and fNIRS-HHb, respectively (SMC → PMC, SMC → DLPFC and PMC → DLPFC).. Supplementary material 4 (TIFF 72 kb)

    10548_2016_507_MOESM5_ESM.tif

    Supplementary Fig. 4. The parcellation of the three ROI’s namely SMC (blue), PMC (red) and DLPFC (green) are shown on the interpolated AAL atlas. The connectivity results for the three tasks are shown on the right side separately for each task.. Supplementary material 5 (TIFF 1147 kb)

    10548_2016_507_MOESM6_ESM.tif

    Supplementary Fig. 5. The results of the band limited analyses at (2-5 Hz) for the three tasks separately A) Finger tapping; B) Simple Finger sequence; C) Complex finger sequence; and their corresponding connectivity results are shown. Supplementary material 6 (TIFF 2700 kb)

    Supplementary material 7 (DOCX 18 kb)

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    Anwar, A.R., Muthalib, M., Perrey, S. et al. Effective Connectivity of Cortical Sensorimotor Networks During Finger Movement Tasks: A Simultaneous fNIRS, fMRI, EEG Study. Brain Topogr 29, 645–660 (2016). https://doi.org/10.1007/s10548-016-0507-1

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