Coherence of BOLD signal and electrical activity in the human brain during deep sevoflurane anesthesia.

Daniel Golkowski,George A Mashour,Joachim Pientka,Philipp Kohl,Rüdiger Ilg,Andreas Ranft,Christine Preibisch,Claus Zimmer,Eberhard F Kochs,Tobias Kiel,Denis Jordan,Guido Rohrer,Valentin Riedl,Sebastian Berger,Gerhard Schneider

doi:10.1002/brb3.679

Abstract

IntroductionChanges in neural activity induce changes in functional magnetic resonance (fMRI) blood oxygenation level dependent (BOLD) signal. Commonly, increases in BOLD signal are ascribed to cellular excitation.ObjectiveThe relationship between electrical activity and BOLD signal in the human brain was probed on the basis of burst suppression EEG. This condition includes two distinct states of high and low electrical activity.MethodsResting‐state simultaneous EEG and BOLD measurements were acquired during deep sevoflurane anesthesia with burst suppression EEG in nineteen healthy volunteers. Afterwards, fMRI volumes were assigned to one of the two states (burst or suppression) as defined by the EEG.ResultsIn the frontal, parietal and temporal lobes as well as in the basal ganglia, BOLD signal increased after burst onset in the EEG and decreased after onset of EEG suppression. In contrast, BOLD signal in the occipital lobe was anticorrelated to electrical activity. This finding was obtained consistently in a general linear model and in raw data.ConclusionsIn human brains exhibiting burst suppression EEG induced by sevoflurane, the positive correlation between BOLD signal and electrical brain activity could be confirmed in most gray matter. The exceptional behavior of the occipital lobe with an anticorrelation of BOLD signal and electrical activity might be due to specific neurovascular coupling mechanisms that are pronounced in the deeply anesthetized brain.

Highlights

Changes in neural activity induce changes in functional magnetic resonance blood oxygenation level dependent (BOLD) signal
Brains of human subjects profoundly anesthetized with sevoflurane exhibited a close coupling of EEG and BOLD signal across the cerebral cortex and subcortical structures
FMRI BOLD depends on the interplay between cerebral blood flow (CBF), cerebral blood volume (CBV), and the cerebral metabolic rate of oxygen (CMRO2) (Kim & Ogawa, 2012; Ogawa, Lee, Kay, & Tank, 1990), which are all related to neuronal activity

Summary

Introduction

Changes in neural activity induce changes in functional magnetic resonance (fMRI) blood oxygenation level dependent (BOLD) signal. Relating BOLD signals to EEG frequency bands yielded a positive correlation with gamma band power following visual stimulation (Goense & Logothetis, 2008; Kayser, Kim, Ugurbil, Kim, & Konig, 2004; Niessing et al, 2005) and during spontaneous activity (Magri, Schridde, Murayama, Panzeri, & Logothetis, 2012; Murayama et al, 2010; Scholvinck, Maier, Ye, Duyn, & Leopold, 2010) This connection was validated in humans performing a cognitive task during simultaneous EEG-fMRI recording where BOLD signal fluctuations were positively correlated with high gamma (60–80 Hz) power and negatively correlated with alpha and beta power (Scheeringa et al, 2011). A strictly data-driven approach to simultaneous EEG-fMRI measurements in human brains revealed distinct electrophysiological signatures of resting state networks, corroborating that the various frequency bands differentially influence BOLD signal (Mantini, Perrucci, Del Gratta, Romani, & Corbetta, 2007)

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Conclusion