Synchronization of intrinsic 0.1‐Hz blood‐oxygen‐level‐dependent oscillations in amygdala and prefrontal cortex in subjects with increased state anxiety

• Published in: The European journal of neuroscience Vol. 47; no. 5; pp. 417 - 426
• Main Authors: Pfurtscheller, Gert, Schwerdtfeger, Andreas, Seither‐Preisler, Annemarie, Brunner, Clemens, Aigner, Christoph Stefan, Calisto, João, Gens, João, Andrade, Alexandre
• Format: Journal Article
• Language: English
• Published: France Wiley Subscription Services, Inc 01.03.2018; John Wiley and Sons Inc
• Subjects: 0.1‐Hz oscillations; Adult; Amygdala; Amygdala - metabolism; Anxiety; Anxiety Disorders - metabolism; Anxiety Disorders - physiopathology; Blood flow; blood‐oxygen‐level‐dependent signal; Brain Mapping - methods; Cerebral blood flow; Cerebrovascular Circulation - physiology; Cortex (frontal); Female; Functional magnetic resonance imaging; Heart Rate - physiology; heart rate variability; Humans; Information processing; Magnetic Resonance Imaging - methods; Male; Neural networks; Neurosystems; Oscillations; Oxygen - blood; Prefrontal cortex; Prefrontal Cortex - metabolism; state anxiety; Synchronization; state anxiety; blood-oxygen-level-dependent signal; 0.1-Hz oscillations; amygdala; heart rate variability
• ISSN: 0953-816X; 1460-9568; 1460-9568
• DOI: 10.1111/ejn.13845

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. Slow spontaneous BOLD oscillations at 0.1 Hz originate either from neural or vascular fluctuations. A phasor model (based on phase‐coupling between BOLD and heart rate interval signals) shows that vascular BOLD oscillations precede neural BOLD oscillations by ~90° or ~2.5 s. This implies that slow blood pressure waves (vascular BOLD) and central commands (neural activity) modulate the heart rate in a time‐locked manner and also enhance the heart rate variability in the low‐frequency band.