Effects of thoracic pressure changes on MRI signals in the brain

Abstract

Cerebrovascular stressors, such as breath holding or CO2 inhalation, cause global magnetic resonance imaging (MRI) signal changes. In this study, we show that intrathoracic pressure changes cause rapid MRI signal alterations that have similar spatial patterns to the changes associated with breath holding or CO2 inhalation. Nine subjects performed the Valsalva maneuver during functional MRI data collection. Expiratory pressures ranged from 10 to 40 mm Hg. Breath holds ending on either inhalation or exhalation were also collected. The maximal and minimal functional MRI (fMRI) signal scaled with thoracic pressure load, and the overall amplitude of responses to the Valsalva varied, depending on brain tissue. Additionally, a Valsalva effort as short as 5 seconds yielded signal changes similar in spatial distribution and magnitude to a 20-second breath hold, suggesting potential applications of the Valsalva maneuver for calibrated fMRI experiments.

Trial registration: ClinicalTrials.gov NCT00001360.

Figures

Figure 1

Heart rate changes during the four phases of the Valsalva maneuver. Mean and standard deviation of 4 Valsalva maneuvers across 57 volunteers. The gray-shaded area marks the breath holding period. These data were collected as part of another study, and the figure is adapted from a previously published figure.

Figure 2

Group averaged responses during Valsalva and breath hold challenges. (A–G) Responses when the breath hold duration is always 20 seconds, but intrathoracic pressure is changing. The vertical dashed lines show the onset and offset of the hold, and the inset shows the signals after the breath hold after the exhalation response is subtracted from the other responses. The inset boxes are proportionally scaled from the larger figures. (H–N) Responses when intrathoracic pressure is always 30 mm Hg, but the breath hold duration is changing. The black dashed line is the onset of the breath hold, and the colored dashed lines mark the end of each breath hold duration. In all regions of interest, the magnetic resonance imaging (MRI) responses decreased below baseline (the valley) during the hold, and increased to a peak after the end of the hold. The magnitude of the responses scaled with thoracic pressure. CSF, cerebrospinal fluid.

Figure 3

Peak (A–D) and valley (E–H) magnetic resonance imaging (MRI) signal amplitudes, scaled with Valsalva pressure in all brain tissues. Each colored line represents data from a single subject. The solid black lines show the linear regression fits of these data across subjects. To characterize the effect of hypercapnia versus load pressure, the breath hold ending on exhale response was subtracted from the 10 to 40 mm Hg responses. The dashed lines show the linear regression fits after the breath holds-on-exhalation responses were subtracted. The slope, r2, and P-values for each regression are shown in solid lettering for the original data, and in outline lettering after subtracting the breath hold on exhalation. CSF, cerebrospinal fluid.

Figure 4

Comparison of magnetic resonance imaging (MRI) signal magnitudes during breath holding and Valsalva conditions. The intensity scale of runs from 2% (black) to 98% (white) of the cumulative distribution of the magnitudes. (A) The first EPI volume of each run. (B) The intensity scale is constant across each column. The raw magnitudes change within trial type, but the relative tissue contrast remains similar. (C) The intensity scale is calculated separately for each slice. The maps of peak magnitude, −1*valley magnitude, and the difference between peak and valley magnitudes appears similar across breath hold and Valsalva conditions, even when the Valsalva maneuver duration is only 5 seconds.

Figure 5

Slope of pressure versus (A) peak or (B) valley magnetic resonance imaging (MRI) signal responses. Slopes were calculated for each voxel in the same manner as in Figure 3. The data are thresholded to exclude slopes of less than 0.15%. The anatomic underlay is darkened for voxels with no fMRI data. The slopes were steeper in gray matter than in white matter.

Figure 6

Voxelwise relationships between trials. (A) The relationship between the peak magnitudes for a 20-second breath hold on exhalation (no pressure target) versus a 5-second hold at 30 mm Hg. The subject with the lowest r2 value for this fit is shown. Each point represents a gray-matter voxel. The linear fit to all voxelwise data is shown. (B) For each trial, compared with breath hold on exhalation, the r values from the regressions shown in (A) were Fisher Z-transformed and averaged across subjects. Box plots show the median (circle with dot), 25th and 75th percentiles (solid box), maxima and minima (whiskers) and outliers (hollow circles). Every fit is significant.