Structural basis of the fronto-thalamic dysconnectivity in schizophrenia: A combined DCM-VBM study☆

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Abstract

Several lines of evidence suggest that cognitive control deficits may be regarded as a connecting link between reported impairments in different cognitive domains of schizophrenia. However, the precise interplay within the fronto-cingulo-thalamic network known to be involved in cognitive control processes and its structural correlates has only been sparsely investigated in schizophrenia. The present multimodal study was therefore designed to model cognitive control processes within the fronto-cingulo-thalamic network. A disruption in effective connectivity in patients in association with abnormal white matter (WM) structure in this network was hypothesized. 36 patients with schizophrenia and 36 healthy subjects participated in the present study. Using functional magnetic resonance imaging (fMRI) a Stroop task was applied in an event-related design. For modeling effective connectivity dynamic causal modeling (DCM) was used. Voxel-based morphometry (VBM) was employed to study WM abnormalities. In the fMRI analysis, the patients demonstrated a significantly decreased BOLD signal in the fronto-cingulo-thalamic network. In the DCM analysis, a significantly decreased bilateral endogenous connectivity between the mediodorsal thalamus (MD) and the anterior cingulate cortex (ACC) was detected in patients in comparison to healthy controls, which was negatively correlated with the Stroop interference score. Furthermore, an increased endogenous connectivity between the right DLPFC and the right MD was observed in the patients. WM volume decreases were observed in the patients in the MD and the frontal cortex. The present results provide strong evidence for the notion that an abnormal fronto-cingulo-thalamic effective connectivity may represent the basis of cognitive control deficits in schizophrenia. Moreover, the data indicate that disrupted white matter connectivity in the mediodorsal thalamus and in the fronto-cingulo-thalamic network may constitute the determining cause of fronto-cingulo-thalamic dysconnectivity.

Highlights

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Decreased BOLD signal in the fronto-thalamic network in the Stroop task in patients
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Decreased endogenous connectivity between thalamus and the ACC in patients
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Decreased WM volume in the thalamus and the frontal cortex in patients
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Disrupted WM connectivity as potential cause of the fronto-thalamic dysconnectivity

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Conflict monitoring by the anterior cingulate cortex (ACC) has been posited to signal a need for greater cognitive control, producing neural and behavioral adjustments. However, the very occurrence of behavioral adjustments after conflict has been questioned, along with suggestions that there is no direct evidence of ACC conflict-related activity predicting subsequent neural or behavioral adjustments in control. Using the Stroop color-naming task and controlling for repetition effects, we demonstrate that ACC conflict-related activity predicts both greater prefrontal cortex activity and adjustments in behavior, supporting a role of ACC conflict monitoring in the engagement of cognitive control.

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It has been well established that schizophrenic patients have neurocognitive deficits, but it is not known how these deficits influence the daily lives of patients. The goal of this review was to determine which, if any, neurocognitive deficits restrict the functioning of schizophrenic patients in the outside world. The author reviewed studies that have evaluated neurocognitive measures as predictors and correlates of functional outcome for schizophrenic patients. The review included 1) studies that have prospectively evaluated specific aspects of neurocognition and community (e.g., social and vocational) functioning (six studies), 2) all known studies of neurocognitive correlates of social problem solving (five studies), and 3) all known studies of neurocognitive correlates and predictors of psychosocial skill acquisition (six studies). Despite wide variation among studies in the selection of neurocognitive measures, some consistencies emerged. The most consistent finding was that verbal memory was associated with all types of functional outcome. Vigilance was related to social problem solving and skill acquisition. Card sorting predicted community functioning but not social problem solving. Negative symptoms were associated with social problem solving but not skill acquisition. Notably, psychotic symptoms were not significantly associated with outcome measures in any of the studies reviewed. Verbal memory and vigilance appear to be necessary for adequate functional outcome. Deficiencies in these areas may prevent patients from attaining optimal adaptation and hence act as "neurocognitive rate-limiting factors." On the basis of this review of the literature, a series of hypotheses are offered for follow-up studies.

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Author and article information

Contributors

Gerd Wagner

Journal

Journal ID (nlm-ta): Neuroimage (Amst)

Journal ID (iso-abbrev): Neuroimage (Amst)

Title: NeuroImage : Clinical

Publisher: Elsevier

ISSN (Electronic): 2213-1582

Publication date PMC-release: 3 August 2013

Publication date (Electronic): 3 August 2013

Publication date Collection: 2013

Volume: 3

Pages: 95-105

Affiliations

[a ]Department of Psychiatry and Psychotherapy, University Hospital Jena, Germany

[b ]Medical Physics Group, Institute of Diagnostic and Interventional Radiology I, Jena University Hospital, Germany

[c ]Department of Neuroradiology, Klinikum rechts der Isar, Technische Universität München, Ismaningerstrasse 22, 81675 Munich, Germany

Author notes

[* ]Corresponding author at: Department of Psychiatry and Psychotherapy, Jena University Hospital, Centre for Neuroimaging, Jahnstr. 3, 07740 Jena, Germany. Tel.: + 49 3641934750; fax: + 49 3641934755. wagner.gerd@ 123456uni-jena.de

Article

Publisher ID: S2213-1582(13)00097-1

DOI: 10.1016/j.nicl.2013.07.010

PMC ID: 3791293

PubMed ID: 24179853

SO-VID: b4fe7d7f-b838-49ba-a6f9-8a3820cbfe72

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 10 April 2013

Date revision received : 16 July 2013

Date accepted : 29 July 2013

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