Angiographic Pulse Wave Coherence in the Human Brain

Abstract

A stroke volume of arterial blood that arrives to the brain housed in the rigid cranium must be matched over the cardiac cycle by an equivalent volume of ejected venous blood. We hypothesize that the brain maintains this equilibrium by organizing coherent arterial and venous pulse waves. To test this hypothesis, we applied wavelet computational methods to diagnostic cerebral angiograms in four human patients, permitting the capture and analysis of cardiac frequency phenomena from fluoroscopic images acquired at faster than cardiac rate. We found that the cardiac frequency reciprocal phase of a small region of interest (ROI) in a named artery predicts venous anatomy pixel-wise and that the predicted pixels reconstitute venous bolus passage timing. Likewise, a small ROI in a named vein predicts arterial anatomy and arterial bolus passage timing. The predicted arterial and venous pixel groups maintain phase complementarity across the bolus travel. We thus establish a novel computational method to analyze vascular pulse waves from minimally invasive cerebral angiograms and provide the first direct evidence of arteriovenous coupling in the intact human brain. This phenomenon of arteriovenous coupling may be a physiologic mechanism for how the brain precisely maintains mechanical equilibrium against volume displacement and kinetic energy transfer resulting from cyclical deformations with each heartbeat. The study also paves the way to study deranged arteriovenous coupling as an underappreciated pathophysiologic disturbance in a myriad of neurological pathologies linked by mechanical disequilibrium.

Keywords: angiography; biomechanics; cerebral circulation; hydrocephalus; pulse waves.

FIGURE 1

Overview of experimental and analytical approach to analyze diagnostic cerebral angiograms by wavelet transformation. (A) Schematic depicting the derivation of wavelet angiograms from raw cerebral angiograms acquired in neurologically unremarkable human patients. In summary, the wavelet transformation permits extraction of contrast intensity signals that oscillate at cardiac frequency from the raw cerebral angiograms. Analysis of the wavelet transformed data from different anatomical components of the cerebrovascular network allowed us to test the hypothesis that the arterial and venous subsystems are coupled. (B) Wavelet transformed right common carotid angiogram during the duration of a single heartbeat demonstrating multiple spatiotemporal phase groupings for subject H1 (frame rate 6.0 Hz). Both anterior-posterior (AP) and lateral (lat) projections are shown.

FIGURE 2

Demonstration of reciprocal coherence between arterial and venous systems of the human brain. Example data for one angiographic projection from subject H1 are shown for panels a–c, data from all other projections are shown in Supplementary Figures S3, S4 Named Vessel ROIs, Right Common Carotid Artery Distribution, Lateral Projection. The top left shows angiographic frames in arterial and venous phases of the bolus travel with named artery and vein ROIs. The bottom left shows time signal curves for the two ROIs. The vertical gray bar indicates the frame selected for mask generation. The right panel shows complex-valued scattergrams for the two ROIs after wavelet transformation for cardiac frequency. Frame rate 6.0 Hz. Subject H1. c) Time Signal Curves From Coherence Masking, Right Common Carotid Artery Distribution, Lateral Projection. The left column shows the arterial, parenchymal, and venous coherence masks as per the named artery and vein ROIs in panel a. The top right shows complex-valued histograms of the wavelet-transformed cardiac frequency data for the masks. The bottom right shows angiographic time intensity curves generated from the masks are given with standard error. d-e) Relative mean arrival times from coherence masking for each subject, AP and lateral projections.

FIGURE 3

Arteriovenous coupling in normal physiology and neurological disorders. Schematic depicting hypotheses regarding arteriovenous coupling in normal cerebrovascular physiology and potential involvement in multiple human neurological disorders.