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Original Investigation |

Resting-State Functional Magnetic Resonance Imaging Activity and Connectivity and Cognitive Outcome in Traumatic Brain Injury

Eva M. Palacios1; Roser Sala-Llonch1,2; Carme Junque, PhD1,2; Teresa Roig, PhD3; Jose M. Tormos, MD, PhD3; Nuria Bargallo, MD, PhD4; Pere Vendrell1,2
[+] Author Affiliations
1August Pi i Sunyer Biomedical Research Institute, Barcelona, Spain
2Department of Psychiatry and Clinical Psychobiology, University of Barcelona, Spain
3Institut Guttmann–Neurorehabilitation Hospital, Badalona, Spain
4Centre de Diagnostic per la Imatge, Hospital Clinic, Barcelona, Spain
JAMA Neurol. 2013;70(7):845-851. doi:10.1001/jamaneurol.2013.38.
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Importance  The study of brain activity and connectivity at rest provides a unique opportunity for the investigation of the brain substrates of cognitive outcome after traumatic axonal injury. This knowledge may contribute to improve clinical management and rehabilitation programs.

Objective  To study functional magnetic resonance imaging abnormalities in signal amplitude and brain connectivity at rest and their relationship to cognitive outcome in patients with chronic and severe traumatic axonal injury.

Design  Observational study.

Setting  University of Barcelona and Hospital Clinic de Barcelona, Barcelona, and Institut Guttmann–Neurorehabilitation Hospital, Badalona, Spain.

Participants  Twenty patients with traumatic brain injury (TBI) were studied, along with 17 matched healthy volunteers.

Interventions  Resting-state functional magnetic resonance imaging and diffusion tensor imaging data were acquired. After exploring group differences in amplitude of low-frequency fluctuations (ALFF), we studied functional connectivity within the default mode network (DMN) by means of independent component analysis, followed by a dual regression approach and seed-based connectivity analyses. Finally, we performed probabilistic tractography between the frontal and posterior nodes of the DMN.

Main Outcomes and Measures  Signal amplitude and functional connectivity during the resting state, tractography related to DMN, and the association between signal amplitudes and cognitive outcome.

Results  Patients had greater ALFF in frontal regions, which was correlated with cognitive performance. Within the DMN, patients showed increased connectivity in the frontal lobes. Seed-based connectivity analyses revealed augmented connectivity within surrounding areas of the frontal and left parietal nodes of the DMN. Fractional anisotropy of the cingulate tract was correlated with increased connectivity of the frontal node of the DMN in patients with TBI.

Conclusions and Relevance  Increased ALFF is related to better cognitive performance in chronic TBI. The loss of structural connectivity produced by damage to the cingulum tract explained the compensatory increases in functional connectivity within the frontal node of the DMN.

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Figures

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Figure 1.
Image processing and analysis methods

(1) Whole-brain analysis of the amplitude of low-frequency fluctuations (ALFF); (2) independent component analysis (ICA) and dual-regression analysis of the default mode network (DMN); (3) connectivity analysis using the predefined DMN regions of interest (ROIs); and (4) diffusion tensor imaging (DTI) tractography analysis of the cingulum tract from the DMN ROIs. (See the Methods section and the eMethods in Supplement for details.) FA indicates fractional anisotropy; fMRI, functional magnetic resonance imaging.

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Figure 2.
Increased amplitude of low-frequency fluctuations during the resting-state in patients with traumatic brain injury

Red-yellow regions represent areas with statistically significant differences between patients and controls (corrected P < .05).

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Figure 3.
Increased connectivity within the default mode network in patients with traumatic brain injury to controls

Red-yellow regions represent areas where the connectivity differed significantly between patients and controls (corrected P < .05).

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Figure 4.
Areas showing increased functional connectivity in traumatic brain injury and locations of the seeds

Areas showing increased functional connectivity in traumatic brain injury (red and yellow) and locations of the seeds (blue). A, Increased connectivity with the medial prefrontal cortex region of interest used as a seed. B, Increased connectivity with the left parietal cortex region of interest used as a seed. Significant at P < .05 (family-wise error corrected).

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Figure 5.
Results of tractography analysis shown as spatial maps of probabilistic tracking

Yellow represents the 2 regions of interest (medial prefrontal cortex and precuneus/posterior cingulate) used as seeds for the fiber-tracking algorithm. Average probabilistic connectivity maps are shown, with the standard anatomical Montreal Neurological Institute template, for controls (in green) and patients with traumatic brain injury (TBI) (in blue).

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