Dynamics of respiratory and cardiac CSF motion revealed with real-time simultaneous multi-slice EPI velocity phase contrast imaging

Abstract

Cerebrospinal fluid (CSF) dynamics have been mostly studied with cardiac-gated phase contrast MRI combining signal from many cardiac cycles to create cine-phase sampling of one time-averaged cardiac cycle. The relative effects of cardiac and respiratory changes on CSF movement are not well understood. There is possible respiration-driven movement of CSF in ventricles, cisterns, and subarachnoid spaces which has not been characterized with velocity measurements. To date, commonly used cine-phase contrast techniques of velocity imaging inherently cannot detect respiratory velocity changes since cardiac-gated data acquired over several minutes randomizes respiratory phase contributions. We have developed an extremely fast, real-time, and quantitative MRI technique to image CSF velocity in simultaneous multi-slice (SMS) echo planar imaging (EPI) acquisitions of 3 or 6 slice levels simultaneously over 30s and observe 3D spatial distributions of CSF velocity. Measurements were made in 10 subjects utilizing a respiratory belt to record respiratory phases and visual cues to instruct subjects on breathing rates. A protocol is able to measure velocity within regions of brain and basal cisterns covered with 24 axial slices in 4 minutes, repeated for 3 velocity directions. These measurements were performed throughout the whole brain, rather than in selected line regions so that a global view of CSF dynamics could be visualized. Observations of cardiac and breathing-driven CSF dynamics show bidirectional respiratory motion occurs primarily along the central axis through the basal cisterns and intraventricular passageways and to a lesser extent in the peripheral Sylvian fissure with little CSF motion present in subarachnoid spaces. During inspiration phase, there is upward (inferior to superior) CSF movement into the cranial cavity and lateral ventricles and a reversal of direction in expiration phase.

Keywords: CSF; Cardiac; EPI; Multiband; Phase contrast; Respiratory; Simultaneous multi-slice; Velocity.

Figure 1

Diagram of simultaneous multi-slice (SMS)-EPI velocity pulse sequence. (A) Three simultaneous excitation planes (S¹-S³). Coil array coverage (orange loops) is shown. (B) The pulse sequence acquisition scheme illustration for multiband velocity imaging. The polarity of the velocity phase encoding +/− is determined by the polarity of the bipolar pulse (red/blue vs. blue/red) used in each TR of the encoding scheme. Sequential pairs of time frames encoded with alternating phase polarity are subtracted to create each velocity image. The time series of velocity images can generate the velocity movie. (C) The SMS-EPI velocity pulse sequence diagram. The multiband (MB) excitation pulse is followed by the (velocity encoding) bipolar gradient (red/blue) pulse and the SMS-EPI readout. Radiofrequency (RF), read gradient (Gr), phase encoding gradient (Gp), slice selective gradient (Gs).

Figure 2

Comparison of SMS and single slice velocity encoded images. Magnitude and phase contrast images from 3 slices from an SMS acquisition are shown, with the equivalent phase image from a single slice acquisition. ROI timeseries from the aqueduct are also shown for the SMS and single-slice acquisitions. (Bottom) CSF velocities measured in the aqueduct with SMS-EPI (left) and GRE phase contrast imaging (right). The red plot shows a band-passed timeseries, corresponding to cardiac modulations.

Figure 3

CSF velocities in the aqueduct of a single subject during five different breathing schemes: free breathing, fast breathing, slow breathing and breath-hold after expiration and inspiration. The velocity curve from the aqueduct is shown in the top row: the low-passed data (< 0.5 Hz) is shown (thick blue line), and measurements simultaneously acquired with a respiratory belt (green) are shown. The Fourier transform of the data is shown in the bottom row, with the (red) respiratory (< 0.5 Hz) and (blue) cardiac (~ 1.1 Hz) frequency bands highlighted, respectively, and data from the respiratory belt (green) is plotted.

Figure 4

Velocities measured simultaneously in 2 slices across 7 subjects during cued breathing at two different frequencies. Plotting of the timeseries data has the same color convention as Figure 3. Vertical green lines indicate the start of externally cued inspiration.

Figure 5

Velocities measured in 6 simultaneously acquired slices. Timeseries data is plotted with the same conventions as Figure 2 (raw data in black, low-passed data in blue).

Figure 6

Data from whole brain 24 slice data, showing different measures across 9 subjects. A) Minimum and maximum velocities in the raw data velocity data. SI = red, AP = blue, right-left (RL) = green. B) Minimum and maximum velocities for each ROI in each direction in low-pass (< 0.5 Hz) filtered data. Same plotting convention as A. C) Mean respiratory power (total amplitudes for frequencies < 0.5 Hz). D) Mean cardiac power (frequencies between 0.6 and 1.5 Hz). Same convention as C. E) Peak frequencies for each ROI in the respiratory (blue) and cardiac (red) frequency ranges for the SI direction. ROI abbreviations: Posterior Basal Cistern (PB), Anterior Basal (AB), Foramen of Magendie (FMa), 4^th Ventricle/Aqueduct (4^th/Aq), Aqueduct (Aq), 3^rd Ventricle (3^rd), Foramen of Monroe (FMo), Sylvain Fissure (SF), Calcarine Sulcus (Calc Sulc), Central Sulcus (Cent Culc).