Head motion during MRI acquisition reduces gray matter volume and thickness estimates

Abstract

Imaging biomarkers derived from magnetic resonance imaging (MRI) data are used to quantify normal development, disease, and the effects of disease-modifying therapies. However, motion during image acquisition introduces image artifacts that, in turn, affect derived markers. A systematic effect can be problematic since factors of interest like age, disease, and treatment are often correlated with both a structural change and the amount of head motion in the scanner, confounding the ability to distinguish biology from artifact. Here we evaluate the effect of head motion during image acquisition on morphometric estimates of structures in the human brain using several popular image analysis software packages (FreeSurfer 5.3, VBM8 SPM, and FSL Siena 5.0.7). Within-session repeated T1-weighted MRIs were collected on 12 healthy volunteers while performing different motion tasks, including two still scans. We show that volume and thickness estimates of the cortical gray matter are biased by head motion with an average apparent volume loss of roughly 0.7%/mm/min of subject motion. Effects vary across regions and remain significant after excluding scans that fail a rigorous quality check. In view of these results, the interpretation of reported morphometric effects of movement disorders or other conditions with increased motion tendency may need to be revisited: effects may be overestimated when not controlling for head motion. Furthermore, drug studies with hypnotic, sedative, tranquilizing, or neuromuscular-blocking substances may contain spurious "effects" of reduced atrophy or brain growth simply because they affect motion distinct from true effects of the disease or therapeutic process.

Keywords: Bias; Cortical gray matter estimates; Head motion; MRI; Quality control; Spurious effect; Thickness; Volume.

Figure 1. Different Motion Levels across Motion Types

Mean RMSpm (RMS displacement per minute) for each motion type with ± standard error. Compared to the still scans, motion increases in nod, shake and free. Significance of the paired Wilcoxon signed rank test is indicated by a red + (p < 0.01) and * (p < 0.001).

Figure 2. Cortical Gray Matter Volume Estimates are explained by Motion

FS and SPM cortical GM volume change is accurately explained by motion in the 12 different subjects via a linear mixed effects model. The slopes are approximately 1% (FS independent, left), 0.7% (FS longitudinal, middle) and 0.7% (SPM, right) volume loss per 1 mm/min RMSpm increase (p < 10⁻¹⁰). Different colors indicate different individuals, sorted with respect to baseline GM volume from smallest (yellow) to largest (red).

Figure 3. VBM GM Volume Estimates Correlate with Motion

Regions of significant VBM GM volume change associated with increased motion. The maps show p-values testing the association (β₂ in Eq. 1) and are FDR thresholded at level 0.05. Red/yellow indicate GM volume loss, blue indicates GM volume gain with increased motion.

Figure 4. Cortical Thickness Estimates Correlate with Motion

Regions of significant cortical thickness change associated with increased motion. Left: FDR thresholded (at level 0.05) p-values testing the association (β₂ in Eq. 1) with increased motion. Red/yellow indicate thickness loss, blue indicates thickness gain with increased motion. Right: Effects as percent thickness change for a 1 mm/min increase in RMSpm motion. Yellow regions of approx. 1.5% thinning correspond to a decrease in thickness of approx. 0.04 mm (per 1 mm/min RMSpm motion increase).

Figure 5. Manual Quality Check Identifies Increased Motion

Different RMSpm motion levels for “pass”, “warn”, and “fail” indicate that the manual quality check correctly identifies cases with motion.

Figure 6. Cortical Gray Matter Volume Estimates after regular QC are explained by Motion

FS and SPM/VBM cortical GM volume change is accurately explained by motion in the 12 different subjects via a linear mixed effects model, even after removing scans that fail QC. The slopes are approximately 1% (FS independent, left), 0.9% (FS longitudinal, middle) and 0.8% (SPM, right) volume loss per 1 mm/min RMSpm increase (p < 10⁻¹⁰). Compare to Figure 2.

Figure 7. VBM GM Volume Estimates Correlate with Motion after regular QC

Regions of significant GM volume change associated with increased motion after removing scans that fail QC. Compare to Fig. 3 and see description for details.

Figure 8. Cortical Thickness Estimates Correlate with Motion after regular QC

Regions of significant cortical thickness change associated with increased motion after removing scans that fail QC. Compare to Fig. 4 and see description for details.

Figure 9. Cortical Thickness Estimates Correlate with Motion after extreme QC

Regions of significant cortical thickness change associated with increased motion after removing scans that fail QC and scans with a warning. The p-value map (left) is not FDR thresholded (effects disappear after FDR). Compare to Figs. 8 and 4 and see description for details.