Frequency Dependent Alterations in Regional Homogeneity of Baseline Brain Activity in Schizophrenia

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Abstract

Low frequency oscillations are essential in cognitive function impairment in schizophrenia. While functional connectivity can reveal the synchronization between distant brain regions, the regional abnormalities in task-independent baseline brain activity are less clear, especially in specific frequency bands. Here, we used a regional homogeneity (ReHo) method combined with resting-state functional magnetic resonance imaging to investigate low frequency spontaneous neural activity in the three different frequency bands (slow-5∶0.01–0.027 Hz; slow-4∶0.027–0.08 Hz; and typical band: 0.01–0.08 Hz) in 69 patients with schizophrenia and 62 healthy controls. Compared with controls, schizophrenia patients exhibited decreased ReHo in the precentral gyrus, middle occipital gyrus, and posterior insula, whereas increased ReHo in the medial prefrontal cortex and anterior insula. Significant differences in ReHo between the two bands were found in fusiform gyrus and superior frontal gyrus (slow-4> slow-5), and in basal ganglia, parahippocampus, and dorsal middle prefrontal gyrus (slow-5> slow-4). Importantly, we identified significant interaction between frequency bands and groups in the inferior occipital gyrus and caudate body. This study demonstrates that ReHo changes in schizophrenia are widespread and frequency dependent.

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Most cited references 45

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The positive and negative syndrome scale (PANSS) for schizophrenia.

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The variable results of positive-negative research with schizophrenics underscore the importance of well-characterized, standardized measurement techniques. We report on the development and initial standardization of the Positive and Negative Syndrome Scale (PANSS) for typological and dimensional assessment. Based on two established psychiatric rating systems, the 30-item PANSS was conceived as an operationalized, drug-sensitive instrument that provides balanced representation of positive and negative symptoms and gauges their relationship to one another and to global psychopathology. It thus constitutes four scales measuring positive and negative syndromes, their differential, and general severity of illness. Study of 101 schizophrenics found the four scales to be normally distributed and supported their reliability and stability. Positive and negative scores were inversely correlated once their common association with general psychopathology was extracted, suggesting that they represent mutually exclusive constructs. Review of five studies involving the PANSS provided evidence of its criterion-related validity with antecedent, genealogical, and concurrent measures, its predictive validity, its drug sensitivity, and its utility for both typological and dimensional assessment.

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Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.

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Competition between functional brain networks mediates behavioral variability.

A. M. Clare Kelly, Lucina Q Uddin, Bharat Biswal … (2008)

Increased intraindividual variability (IIV) is a hallmark of disorders of attention. Recent work has linked these disorders to abnormalities in a "default mode" network, comprising brain regions routinely deactivated during goal-directed cognitive tasks. Findings from a study of the neural basis of attentional lapses suggest that a competitive relationship between the "task-negative" default mode network and regions of a "task-positive" attentional network is a potential locus of dysfunction in individuals with increased IIV. Resting state studies have shown that this competitive relationship is intrinsically represented in the brain, in the form of a negative correlation or antiphase relationship between spontaneous activity occurring in the two networks. We quantified the negative correlation between these two networks in 26 subjects, during active (Eriksen flanker task) and resting state scans. We hypothesized that the strength of the negative correlation is an index of the degree of regulation of activity in the default mode and task-positive networks and would be positively related to consistent behavioral performance. We found that the strength of the correlation between the two networks varies across individuals. These individual differences appear to be behaviorally relevant, as interindividual variation in the strength of the correlation was significantly related to individual differences in response time variability: the stronger the negative correlation (i.e., the closer to 180 degrees antiphase), the less variable the behavioral performance. This relationship was moderately consistent across resting and task conditions, suggesting that the measure indexes moderately stable individual differences in the integrity of functional brain networks. We discuss the implications of these findings for our understanding of the behavioral significance of spontaneous brain activity, in both healthy and clinical populations.

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Author and article information

Contributors

Bernhard T. Baune: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 6 March 2013

Volume: 8

Issue: 3

Electronic Location Identifier: e57516

Affiliations

[1 ]Division of the Humanities and Social Sciences, California Institute of Technology, Pasadena, California, United States of America

[2 ]Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan

[3 ]Neurobiology and Cognitive Science Center, National Taiwan University, Taipei, Taiwan

[4 ]Center for Optoelectronic Biomedicine, National Taiwan University College of Medicine, Taipei, Taiwan

[5 ]Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei, Taiwan

[6 ]Department of Medical Imaging, National Taiwan University Hospital, Taipei, Taiwan

University of Adelaide, Australia

Author notes

* E-mail: haigohwu@ 123456ntu.edu.tw (H-GH); wytseng@ 123456ntu.edu.tw (W-YIT)

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: MHH HGH WYIT. Performed the experiments: MHH CML CCL TJH YLC. Analyzed the data: RY HLSW. Contributed reagents/materials/analysis tools: HGH WYIT. Wrote the paper: RY MHH HLSW.

Article

Publisher ID: PONE-D-12-23802

DOI: 10.1371/journal.pone.0057516

PMC ID: 3590274

PubMed ID: 23483911

SO-VID: 9a3eee5f-c2f5-492a-b2f4-4e58affe4c91

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 8 August 2012

Date accepted : 23 January 2013

Page count

Pages: 8

Funding

This study was supported in part by the National Health Research Institute, Taiwan (NHRI-EX101-10145NI), National Science Council, Taiwan (NSC100-3112-B-002-016), and National Taiwan University (97HM00273). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Frequency Dependent Alterations in Regional Homogeneity of Baseline Brain Activity in Schizophrenia

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Most cited references 45

The positive and negative syndrome scale (PANSS) for schizophrenia.

Interoception: the sense of the physiological condition of the body.

Competition between functional brain networks mediates behavioral variability.

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