Abstract
Low‐frequency oscillations with a dominant frequency at 0.1 Hz are one of the most influential intrinsic blood‐oxygen‐level‐dependent (BOLD) signals. This raises the question if vascular BOLD oscillations (originating from blood flow in the brain) and intrinsic slow neural activity fluctuations (neural BOLD oscillations) can be differentiated. In this study, we report on two different approaches: first, on computing the phase‐locking value in the frequency band 0.07–0.13 Hz between heart beat‐to‐beat interval (RRI) and BOLD oscillations and second, between multiple BOLD oscillations (functional connectivity) in four resting states in 23 scanner‐naïve, anxious healthy subjects. The first method revealed that vascular 0.1‐Hz BOLD oscillations preceded those in RRI signals by 1.7 ± 0.6 s and neural BOLD oscillations lagged RRI oscillations by 0.8 ± 0.5 s. Together, vascular BOLD oscillations preceded neural BOLD oscillations by ~90° or ~2.5 s. To verify this discrimination, connectivity patterns of neural and vascular 0.1‐Hz BOLD oscillations were compared in 26 regions involved in processing of emotions. Neural BOLD oscillations revealed significant phase‐coupling between amygdala and medial frontal cortex, while vascular BOLD oscillations showed highly significant phase‐coupling between amygdala and multiple regions in the supply areas of the anterior and medial cerebral arteries. This suggests that not only slow neural and vascular BOLD oscillations can be dissociated but also that two strategies may exist to optimize regulation of anxiety, that is increased functional connectivity between amygdala and medial frontal cortex, and increased cerebral blood flow in amygdala and related structures.
Highlights
Neural and hemodynamic oscillations in the slow and ultraslow frequency range between 0.01 and 0.2 Hz are of increasing interest because of their correlation with psychophysical performance and motor behavior (Vanhatalo et al, 2004; Fox et al, 2007; Monto et al, 2008; Palva & Palva, 2012; Pfurtscheller et al, 2017a)
The search for neural and vascular BOLD oscillations was based on calculation of the phase-locking value (PLV) between heart beat-to-beat interval (RRI) and BOLD signals from left MCC in 23 subjects and four resting states
The study yielded two main findings, one referring to intrinsic neural BOLD oscillations at 0.1 Hz and the other to brain connectivity. Both findings are related to each other, because brain connectivity analysis depends on the direction of the time delay between BOLD and RRI oscillations
Summary
Neural and hemodynamic oscillations in the slow and ultraslow frequency range between 0.01 and 0.2 Hz are of increasing interest because of their correlation with psychophysical performance and motor behavior (Vanhatalo et al, 2004; Fox et al, 2007; Monto et al, 2008; Palva & Palva, 2012; Pfurtscheller et al, 2017a). Reviewed by Enrico Glerean, Aalto University, Finland Bin Zhang, Shanghai Mental Health Center, China. All peer review communications can be found with the online version of the article. EEG changes in the slow frequency range are closely associated with slow fluctuations in human psychophysical performance (Monto et al, 2008). Slow BOLD fluctuations (< 0.1 Hz) in the somatomotor cortex are correlated with behavioral fluctuations in motor performance, a finding which was termed the ‘BOLD-behavior effect’ (Fox et al, 2007)
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