Multimodal Magnetic Resonance Imaging Data Fusion Reveals Distinct Patterns of Abnormal Brain Structure and Function in Catatonia

Abstract

Catatonia is a nosologically unspecific syndrome, which subsumes a plethora of mostly complex affective, motor, and behavioral phenomena. Although catatonia frequently occurs in schizophrenia spectrum disorders (SSD), specific patterns of abnormal brain structure and function underlying catatonia are unclear at present. Here, we used a multivariate data fusion technique for multimodal magnetic resonance imaging (MRI) data to investigate patterns of aberrant intrinsic neural activity (INA) and gray matter volume (GMV) in SSD patients with and without catatonia. Resting-state functional MRI and structural MRI data were collected from 87 right-handed SSD patients. Catatonic symptoms were examined on the Northoff Catatonia Rating Scale (NCRS). A multivariate analysis approach was used to examine co-altered patterns of INA and GMV. Following a categorical approach, we found predominantly frontothalamic and corticostriatal abnormalities in SSD patients with catatonia (NCRS total score ≥ 3; n = 24) when compared to SSD patients without catatonia (NCRS total score = 0; n = 22) matched for age, gender, education, and medication. Corticostriatal network was associated with NCRS affective scores. Following a dimensional approach, 33 SSD patients with catatonia according to Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision were identified. NCRS behavioral scores were associated with a joint structural and functional system that predominantly included cerebellar and prefrontal/cortical motor regions. NCRS affective scores were associated with frontoparietal INA. This study provides novel neuromechanistic insights into catatonia in SSD suggesting co-altered structure/function-interactions in neural systems subserving coordinated visuospatial functions and motor behavior.

Keywords: MRI; catatonia; mCCA+jICA; motor symptoms; schizophrenia spectrum disorders.

© The Author(s) 2019. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: journals.permissions@oup.com.

Figures

Fig. 1.

Structural and functional networks exhibiting significant differences between catatonic (n = 24) and non-catatonic (n = 22) patients. Bar graphs depict the mean of mixing coefficients for each independent component (IC) in each group. The error bars represent ± 1 standard error of the mean. Analyses of covariance were used to test the effects of group on the mixing coefficients of each IC in structural magnetic resonance imaging (sMRI) and resting-state functional MRI (rs-fMRI) modalities controlled for olanzapine equivalent and Positive and Negative Syndrome Scale total score. The corresponding F and P values for each test are placed above the bar graphs. The regions in both modalities, with a threshold of |z| > 2.5, are shown in sagittal, coronal, and axial planes.

Fig. 2.

Scatter plots depicting the partial correlations (adjusted for olanzapine equivalent and Positive and Negative Syndrome Scale total score) between Northoff Catatonia Rating Scale (NCRS) behavioral and affective scores in schizophrenia spectrum disorders patients with catatonia according to Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision (n = 33) and the mixing coefficients of each independent component in each modality. Corresponding r and P values are placed above each scatter plot. Brain regions in structural magnetic resonance imaging (sMRI) and resting-state functional MRI (rs-fMRI) modalities are shown in sagittal, coronal, and axial slices, with a threshold of |z| > 2.5.