Quantifying neurovascular coupling through a concurrent assessment of arterial, capillary, and neuronal activation in humans: A multimodal EEG-fNIRS-TCD investigation
Joel S. Burma,
Ibukunoluwa K. Oni,
Andrew P. Lapointe,
Selina Rattana,
Kathryn J. Schneider,
Chantel T. Debert,
Jonathan D. Smirl,
Jeff F. Dunn
Affiliations
Joel S. Burma
Cerebrovascular Concussion Lab, Faculty of Kinesiology, University of Calgary, Alberta, Canada; Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada; Libin Cardiovascular Institute of Alberta, University of Calgary, Alberta, Canada; Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada; Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada; Integrated Concussion Research Program, University of Calgary, Calgary, Alberta, Canada; Corresponding author at: Faculty of Kinesiology, Sports Injury Prevention Research Centre, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada.
Ibukunoluwa K. Oni
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada; Integrated Concussion Research Program, University of Calgary, Calgary, Alberta, Canada; Department of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
Andrew P. Lapointe
Atlas Institute for Veterans and Families, Ottawa, Ontario, Canada
Selina Rattana
Cerebrovascular Concussion Lab, Faculty of Kinesiology, University of Calgary, Alberta, Canada
Kathryn J. Schneider
Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada; Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada; Integrated Concussion Research Program, University of Calgary, Calgary, Alberta, Canada
Chantel T. Debert
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada; Integrated Concussion Research Program, University of Calgary, Calgary, Alberta, Canada; Department of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
Jonathan D. Smirl
Cerebrovascular Concussion Lab, Faculty of Kinesiology, University of Calgary, Alberta, Canada; Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada; Libin Cardiovascular Institute of Alberta, University of Calgary, Alberta, Canada; Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada; Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada; Integrated Concussion Research Program, University of Calgary, Calgary, Alberta, Canada
Jeff F. Dunn
Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada; Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada; Integrated Concussion Research Program, University of Calgary, Calgary, Alberta, Canada; Department of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada; Department of Radiology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
Background: This study explored a novel multimodal neuroimaging approach to assess neurovascular coupling (NVC) in humans using electroencephalography (EEG), functional near-infrared spectroscopy (fNIRS), and transcranial Doppler ultrasound (TCD). Methods: Fifteen participants (nine females; age 19–32) completed concurrent EEG-fNIRS-TCD imaging during motor (finger tapping) and visual (“Where's Waldo?”) tasks, with synchronized monitoring of blood pressure, capnography, and heart rate. fNIRS assessed microvascular oxygenation within the frontal, motor, parietal, and occipital cortices, while the middle and posterior cerebral arteries (MCA/PCA) were insonated using TCD. A 16-channel EEG set-up was placed according to the 10–20 system. Wilcoxon signed-rank tests were used to compare physiological responses between the active and resting phases of the tasks, while cross-correlations with zero legs compared cerebral and systemic hemodynamic responses across both tasks. Results: Time-frequency analysis demonstrated a reduction in alpha and low beta band power in electrodes C3/C4 during finger tapping (p < 0.045) and all electrodes during the Waldo task (all p < 0.001). During Waldo, cross-correlation analysis demonstrated the change in oxygenated hemoglobin and cerebral blood velocity had a moderate-to-strong negative correlation with systemic physiological influences, highlighting the measured change resulted from neuronal input. Deoxygenated hemoglobin displayed the greatest negative cross-correlation with the MCA/PCA within the motor cortices and visual during the motor and visual tasks, respectively (range:0.54, -0.82). Conclusions: This investigation demonstrated the feasibility of the proposed EEG-fNIRS-TCD response to comprehensively assess the NVC response within human, specifically quantifying the real-time temporal synchrony between neuronal activation (EEG), microvascular oxygenation changes (fNIRS), and conduit artery velocity alterations (TCD).
