Schizophrenia induces abnormal frequency-dependent patterns of dynamic brain network reconfiguration during an auditory oddball task

Abstract

Abstract Objective. Schizophrenia is a psychiatric disorder that has been shown to disturb the dynamic top-down processing of sensory information. Various imaging techniques have revealed abnormalities in brain activity associated with this disorder, both locally and between cerebral regions. However, there is increasing interest in investigating dynamic network response to novel and relevant events at the network level during an attention-demanding task with high-temporal-resolution techniques. The aim of the work was: (i) to test the capacity of a novel algorithm to detect recurrent brain meta-states from auditory oddball task recordings; and (ii) to evaluate how the dynamic activation and behavior of the aforementioned meta-states were altered in schizophrenia, since it has been shown to impair top-down processing of sensory information. Approach. A novel unsupervised method for the detection of brain meta-states based on recurrence plots and community detection algorithms, previously tested on resting-state data, was used on auditory oddball task recordings. Brain meta-states and several properties related to their activation during target trials in the task were extracted from electroencephalography data from patients with schizophrenia and cognitively healthy controls. Main results. The methodology successfully detected meta-states during an auditory oddball task, and they appeared to show both frequency-dependent time-locked and non-time-locked activity with respect to the stimulus onset. Moreover, patients with schizophrenia displayed higher network diversity, and showed more sluggish meta-state transitions, reflected in increased dwell times, less complex meta-state sequences, decreased meta-state space speed, and abnormal ratio of negative meta-state correlations. Significance. Abnormal cognition in schizophrenia is also reflected in decreased brain flexibility at the dynamic network level, which may hamper top-down processing, possibly indicating impaired decision-making linked to dysfunctional predictive coding. Moreover, the results showed the ability of the methodology to find meaningful and task-relevant changes in dynamic connectivity and pathology-related group differences.