Abstract
There are concerns about the effects of subconcussive head impacts in sport, but the effects of subconcussion on brain connectivity are not well understood. We hypothesized that college football players experience changes in brain functional connectivity not found in athletes competing in lower impact sports or healthy controls. These changes may be spatially heterogeneous across participants, requiring analysis methods that go beyond mass-univariate approaches commonly used in functional MRI (fMRI). To test this hypothesis, we analyzed resting-state fMRI data from college football (n = 15), soccer (n = 12), and lacrosse players (n = 16), and controls (n = 29) collected at preseason and postseason time points. Regional homogeneity (ReHo) and degree centrality (DC) were calculated as measures of local and long-range functional connectivity, respectively. Standard voxel-wise analysis and paired support vector machine (SVM) classification studied subconcussion’s effects on local and global functional connectivity. Voxel-wise analyses yielded minimal findings, but SVM classification had high accuracy for college football’s ReHo (87%, p = 0.009) and no other group. The findings suggest subconcussion results in spatially heterogeneous changes in local functional connectivity that may only be detectible with multivariate analyses. To determine if voxel-wise and SVM analyses had similar spatial patterns, region-average t-statistic and SVM weight values were compared using a measure of ranking distance. T-statistic and SVM weight rankings exhibited significantly low ranking distance values for all groups and metrics, demonstrating that the analyses converged on a similar underlying effect. Overall, this research suggests that subconcussion in football may produce local functional connectivity changes similar to concussion.
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Acknowledgements
We thank the athletes, trainers, and coaches of the University of Virginia and football, men’s lacrosse, and men’s soccer teams for their invaluable assistance in collecting this data. Access to the multiband EPI sequence was provided through a research agreement with the University of Minnesota Center for Magnetic Resonance Research and Siemens Healthcare. We thank Donna Broshek, PhD for commentary on early drafts of the manuscript.
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This study was funded by a University of Virginia Health System Research Award, NIH 2 T32 GM 8328-21, and the University of Virginia Department of Radiology and Medical Imaging.
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Dr. Wintermark is a member of the advisory board of the GE NFL project. All other authors declare that they have no conflicts of interest.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.
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Supplementary Table S2
In-scan head movement for the groups. CF=college football, OS=other sports, MC=male controls, Pre=preseason time point, Post=postseason time point, translation is the mean linear head movement during the fMRI scan measured in millimeters, rotation is the mean rotational head movement during the fMRI scan measured in radians. (TIFF 1150 KB)
Supplementary Fig. S1
Mass-univariate analyses increases in regional homogeneity. Significant clusters of increased regional homogeneity for college football players (9 voxels) and male controls (2 voxels). (TIFF 3156 KB)
Supplementary Table S1
Participant demographic information. CF=college football, OS=other sports, MC=male controls, FB=football, LAX=lacrosse, Soc=soccer, LHI=limited head impact, EHM=excessive head movement. (TIFF 2133 KB)
Supplementary Table S3
SVM comparison of regional homogeneity between groups. CF=college football, OS=other sports, MC=male controls, Pre=preseason time point, Post=postseason time point. (TIFF 756 KB)
Supplementary Table S5
Region rankings for college football players’ regional homogeneity. SVM=support vector machine, ΔFC metric is the difference of the postseason and preseason regional homogeneity metrics. (TIFF 5.41 MB)
Supplementary Table S4
SVM comparison of degree centrality between groups. CF=college football, OS=other sports, MC=male controls, Pre=preseason time point, Post=postseason time point. (TIFF 762 KB)
Supplementary Table S6
Region rankings for college football players’ degree centrality. SVM=support vector machine, ΔFC metric is the difference of the postseason and preseason degree centrality metrics. (TIFF 5521 KB)
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Reynolds, B.B., Stanton, A.N., Soldozy, S. et al. Investigating the effects of subconcussion on functional connectivity using mass-univariate and multivariate approaches. Brain Imaging and Behavior 12, 1332–1345 (2018). https://doi.org/10.1007/s11682-017-9790-z
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DOI: https://doi.org/10.1007/s11682-017-9790-z