Dataset Information

Effective connectivity of the right anterior insula in schizophrenia: The salience network and task-negative to task-positive transition.

ABSTRACT: Triple network dysfunction theory of schizophrenia postulates that the interaction between the default-mode and the fronto-parietal executive network is disrupted by aberrant salience signals from the right anterior insula (rAI). To date, it is not clear how the proposed resting-state disruption translates to task-processing inefficiency in subjects with schizophrenia. Using a contiguous resting and 2-back task performance fMRI paradigm, we quantified the change in effective connectivity that accompanies rest-to-task state transition in 29 clinically stable patients with schizophrenia and 31 matched healthy controls. We found an aberrant task-evoked increase in the influence of the rAI to both executive (Cohen's d = 1.35, p = 2.8 × 10-6) and default-mode (Cohen's d = 1.22, p = 1.5 × 10-5) network regions occur in patients when compared to controls. In addition, the effective connectivity from middle occipital gyrus (dorsal visual cortex) to insula is also increased in patients as compared with healthy controls. Aberrant insula to executive network influence is pronounced in patients with more severe negative symptom burden. These findings suggest that control signals from rAI are abnormally elevated and directed towards both task-positive and task-negative brain regions, when task-related demands arise in schizophrenia. This aberrant, undiscriminating surge in salience signalling may disrupt contextually appropriate allocation of resources in the neuronal workspace in patients with schizophrenia.

SUBMITTER: Luo Q

PROVIDER: S-EPMC7451428 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Effective connectivity of the right anterior insula in schizophrenia: The salience network and task-negative to task-positive transition.

Luo Qiang Q Pan Baobao B Gu Huaguang H Simmonite Molly M Francis Susan S Liddle Peter F PF Palaniyappan Lena L

NeuroImage. Clinical 20200807

Triple network dysfunction theory of schizophrenia postulates that the interaction between the default-mode and the fronto-parietal executive network is disrupted by aberrant salience signals from the right anterior insula (rAI). To date, it is not clear how the proposed resting-state disruption translates to task-processing inefficiency in subjects with schizophrenia. Using a contiguous resting and 2-back task performance fMRI paradigm, we quantified the change in effective connectivity that ac ...[more]

PMID: 32805679

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Project description:ObjectiveDaytime cognitive impairment is an essential symptom of primary insomnia (PI). However, the underlying neural substrate remains largely unknown. Many studies have shown that the right anterior insula (rAI) as a key node of salience network (SN) plays a critical role in switching between the executive control network (ECN) and the default mode network (DMN) for better performance of cognitively demanding tasks. Aberrant effective connectivity (directional functional connectivity) of rAI with ECN or DMN may be one reason for daytime cognitive impairment in PI patients. Up to now, no effective connectivity study has been conducted on patients with PI during resting state. Our aim is to investigate the effective connectivity between the rAI and the other voxels in the whole brain in PI.Materials and methodsFifty drug-naive patients with PI and forty age- and sex-matched healthy controls were scanned using resting-state functional MRI. Seed-based Granger causality analysis was used to examine effective connectivity between the rAI, including ventral and dorsal part, and the whole brain. The effective connectivity was compared between the two groups and was correlated with clinical characteristics.ResultsCompared with controls, patients showed decreased effective connectivity from the rAI to the bilateral precuneus, the left postcentral gyrus (extending to bilateral precuneus) and the bilateral cerebellum posterior lobe, and decreased effective connectivity from the bilateral orbitofrontal cortex (OFC) to the rAI (single voxel P < 0.001, AlphaSim corrected with P < 0.01). In addition, effective connectivity from the ventral rAI to the left postcentral gyrus and from the left OFC to the ventral rAI were significantly negatively correlated with Insomnia Severity Index scores (r = -0.28/P = 0.046 and r = -0.29/P = 0.038, respectively).ConclusionThe present study is the first to reveal aberrant effective connectivity between the SN hub (rAI) and the posterior DMN hub (precuneus) as well as decision-making region (OFC) and sensori-motor region in PI. These findings suggest an aberrant salience processing system of the rAI in PI patients.

Project description:The emergence of flow is a situation of high salience because externally oriented attention on the task and access to resources for goal-directed behavior are enhanced, while internally oriented or self-related cognition is decreased. The right anterior insula has been reported as a causal out-flow hub of the salience resting-state network, orchestrating the engagement of the central executive network (CEN) and the disengagement of the default-mode network (DMN) during a functional challenge. In the present study, we employed a combined task-based activation and connectivity analysis to investigate the role of the right anterior insula during the emergence of flow. A sample of 41 healthy male subjects was confronted with a functional challenge that permitted the emergence of flow during BOLD-based functional magnetic resonance imaging. Comparing connectivity changes in the right anterior insula during the flow condition against connectivity changes associated with control conditions of boredom and overload, relatively increased couplings were observed with the left and right dorsolateral prefrontal cortex. Activation data for these regions did, however, not show the flow-typical inverted U-shaped (invU) response pattern. Relatively decreased functional couplings encompassed ventral aspects of the striatum, but neither the amygdala nor the medial prefrontal cortex (MPFC). For the ventral striatum, activation data were consistent with the flow-typical U-shaped activation pattern, which supports the notion that under the high salience of autotelic situations, the anterior insula is much less positively coupled with the ventral striatum than under boundary conditions of boredom and overload. Taken together, present functional connectivity results were in alignment with the assumed role of the right anterior insula under conditions of different salience. However, this particular region does not appear to mediate the most typical flow-associated activation patterns.

Dataset Information

Effective connectivity of the right anterior insula in schizophrenia: The salience network and task-negative to task-positive transition.

Publications

Effective connectivity of the right anterior insula in schizophrenia: The salience network and task-negative to task-positive transition.

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