Decreased modulation of segregated SEEKING and selective attention systems in chronic insomnia

Abstract

Sleep-related attentional bias and instinctual craving-sleep status may be associated with value-driven selective attention network and SEEKING system. We hypothesized that the two networks might be important components and underlie etiology of inability to initiate or/and maintain sleep in patients with chronic insomnia (PIs). Our aim is to investigate whether frequency-frequency couplings(temporal and spatial coupling, and differences of a set of imaging parameters) could elevate the sensibility to characterize the two insomnia-related networks in studying their relationships with sleep parameters and post-insomnia emotions. Forty-eight PIs and 48 status-matched good sleepers were requested to complete sleep and emotion-related questionnaires. Receiver operating characteristic curve was used to calculate the discriminatory power of a set of parameters. Granger causality and mediating causality analysis were used to address the causal relationships between the two networks and sleep/emotion-related parameters. Frequency-frequency couplings could characterize the two networks with high discriminatory power (AUC, 0.951; sensitivity, 87.5%; specificity, 95.8%), which suggested that the frequency-frequency couplings could be served as a useful biomarker to address the insomnia-related brain networks. Functional deficits of the SEEKING system played decreased mediator acting in post-insomnia negative emotions (decreased frequency-frequency coupling). Functional hyperarousal of the value-driven attention network played decreased mediator acting in sleep regulation (increased frequency-frequency coupling). Granger causality analysis showed decreased causal effect connectivity between and within the two networks. The between-network causal effect connectivity segregation played decreased mediator acting in sleep regulation (decreased connectivity). These findings suggest that the functional deficits and segregation of the two systems may underlie etiology of PIs.

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Abbreviations

fMRI:

Functional magnetic resonance imaging.

ALFF:

Amplitude of low-frequency fluctuation.

ReHo:

Regional homogeneity.

fALFF:

Fractional ALFF.

GSs:

Good sleepers.

PIs:

Patients with chronic insomnia.

OFC:

Orbitofrontal cortex.

ACC:

Anterior cingulate cortex.

IPS:

Intraparietal sulcus.

GCA:

Granger causality analysis.

PSQI:

Pittsburgh Sleep Quality Index.

HAMD:

Hamilton Depression Rating Scale.

HAMA:

Hamilton Anxiety Rating Scale.

ISI:

Insomnia Severity Index.

SAS:

Self Rating Anxiety Scale.

SDS:

Self-Rating Depression Scale.

DSM-IV:

Statistical Manual of Mental Disorders, version 4.

MNI:

Montreal Neurological Institute.

FD:

Frame-wise displacement.

ROIs:

Regions of interest.

TFCE:

Threshold-Free Cluster Enhancement.

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Acknowledgments

This work was supported by National Natural Science Foundation of China (grant No, 81701678, 81801315 and U1904159), and The Science and Technology Department of Sichuan Province (20YYJC0034).

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Contributions

XJ.D., J. L., and Y. W. conceived and designed the whole experiment; XJ.D., N. W., SZ.A., L. G., W. T., and J. F. take responsibility for the integrity of the data, the accuracy of the data analysis and statistical data analysis; XJ.D. collected the data, wrote the main manuscript text,and under took the critical interpretation of the data. All authors contributed to the final version of the paper and have read, as well as, approved the final manuscript.

Corresponding authors

Correspondence to Jiubao Liu or Yongjun Wang.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Key points/Highlights

1. Chronic insomnia is associated with SEEKING system and value-driven attention network.

2. Frequency-frequency couplings elevate sensibility to characterize insomnia-related networks.

3. Value-driven attention network has decreased mediator acting in sleep regulation.

4. SEEKING system has decreased mediator acting in post-insomnia negative emotion.

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Dai, XJ., Wang, N., Ai, SZ. et al. Decreased modulation of segregated SEEKING and selective attention systems in chronic insomnia. Brain Imaging and Behavior 15, 430–443 (2021). https://doi.org/10.1007/s11682-020-00271-0

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Keywords

  • Insomnia
  • SEEKING system
  • Value-driven attention network
  • Frequency-frequency coupling
  • Visual pathway
  • ML-DA reward system
  • Mediating causality analysis