Elsevier

NeuroImage

Volume 59, Issue 1, 2 January 2012, Pages 431-438
NeuroImage

The influence of head motion on intrinsic functional connectivity MRI

https://doi.org/10.1016/j.neuroimage.2011.07.044Get rights and content

Abstract

Functional connectivity MRI (fcMRI) has been widely applied to explore group and individual differences. A confounding factor is head motion. Children move more than adults, older adults more than younger adults, and patients more than controls. Head motion varies considerably among individuals within the same population. Here we explored the influence of head motion on fcMRI estimates. Mean head displacement, maximum head displacement, the number of micro movements (> 0.1 mm), and head rotation were estimated in 1000 healthy, young adult subjects each scanned for two resting-state runs on matched 3T scanners. The majority of fcMRI variation across subjects was not linked to head motion. However, head motion had significant, systematic effects on fcMRI network measures. Head motion was associated with decreased functional coupling in the default and frontoparietal control networks — two networks characterized by coupling among distributed regions of association cortex. Other network measures increased with motion including estimates of local functional coupling and coupling between left and right motor regions — a region pair sometimes used as a control in studies to establish specificity. Comparisons between groups of individuals with subtly different levels of head motion yielded difference maps that could be mistaken for neuronal effects in other contexts. These effects are important to consider when interpreting variation between groups and across individuals.

Highlights

► We explored the influence of head motion on functional connectivity MRI estimates. ► Head motion had significant, systematic effects on several network measures. ► Majority of network variance across subjects was not related to motion. ► Head motion was associated with both decreased and increased metrics. ► These differences in another context could be mistaken for neuronal effects.

Introduction

Resting-state functional connectivity MRI (fcMRI) is widely used to explore the architecture of brain systems. Studies of differences across the lifespan, between individuals with clinical diagnoses, and across varied personality traits have become common (for recent reviews, see Fornito and Bullmore, 2010, Fox and Greicius, 2010, Vogel et al., 2010, Zhang and Raichle, 2010). The technique is robust and yields reliable measures within individuals (e.g., Honey et al., 2009, Meindl et al., 2010, Shehzad et al., 2009, Van Dijk et al., 2010, Zuo et al., 2010). Recent family and twin studies suggest functional connectivity estimates are heritable and thus may offer insight into how genetic variation affects brain function (Fornito et al., 2011, Glahn et al., 2010). However, there is general awareness that resting state fcMRI is sensitive to confounding factors including head motion even after common data preprocessing steps (Buckner, 2010, Cole et al., 2010). Head motion has long been known to be a confound in task-based functional MRI studies, but has become a particularly challenging problem in recent studies using fcMRI. Effects of interest are often between groups of subjects where differences in motion are expected such as between children and young adults, between young and old adults, and between patients and controls. The present paper explores how head motion affects measures of functional connectivity.

Section snippets

Overview

The primary focus of the paper is to explore how between-subject differences in head motion affect MRI measures of intrinsic functional connectivity. A large sample of data from typical, healthy control subjects ages 18 to 30 were selected (n = 1110). All subjects were imaged on matched MRI scanners using the same MRI sequence. Subjects with artifacts or abnormally low temporal signal-to-noise (tSNR) were eliminated but otherwise the sample represents a typical convenience sample of good to

Estimates of head motion

We explored the distribution of head motion across all 1088 usable subjects by plotting the frequency histogram of Mean Motion (the mean displacement of each brain volume as compared to the previous volume). A few observations are notable (Fig. 1A). First, there is substantial inter-subject variability. Second, a minority of subjects displayed disproportionately high levels of Mean Motion. Although this skewed distribution is expected from a distance measure it is worth noting that 8.5% of the

Discussion

The present study examined the influence of head motion on functional connectivity MRI. The primary result is that head motion has systematic effects on functional connectivity estimates that could easily be misinterpreted as neuronal effects. High levels of head motion were associated with reduced functional connectivity in large-scale distributed networks (e.g., the default network and the frontoparietal control network; Figs. 3A and B) and increased local functional connectivity (Figs. 3C

Conclusions

Head motion significantly affects measures of functional connectivity MRI even within the range of motion exhibited by typical, healthy young adults. The effects are dependent on the specific measure and include decreased functional coupling for distributed networks and increased functional coupling for local networks. Since motion was found to be a stable property within subjects – behaving as a trait – studies of genetic associations, heritability, and relations to behavior and personality

Acknowledgments

We thank the Harvard Center for Brain Science Neuroimaging Core, the Athinoula A. Martinos Center for imaging support, and the Harvard Neuroinformatics Research Group (Gabriele Fariello, Timothy O'Keefe, and Victor Petrov). The data analyzed were collected as part of the Genomics Superstruct Project. We thank Marisa Hollinshead, Elizabeth Hemphill, Leah Bakst, Angela Castellanos, and Sara Rubenstein for assistance in collecting the data. Avram Holmes and Jorge Sepulcre assisted in constructing

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