Top-down and bottom-up alterations of connectivity patterns of the suprachiasmatic nucleus in chronic insomnia disorder

Feb 22, 2023European archives of psychiatry and clinical neuroscience

Changes in Brain Signals to and from the Body’s Internal Clock in Chronic Insomnia

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Abstract

In a study involving 42 patients with chronic insomnia disorder and 37 healthy controls, significant alterations in brain connectivity related to the suprachiasmatic nucleus (SCN) were observed.

Patients with chronic insomnia disorder showed enhanced connectivity between the SCN and the left dorsolateral prefrontal cortex compared to healthy controls.
Reductions in connectivity were noted between the SCN and both medial prefrontal cortices in chronic insomnia patients.
Disrupted functional and causal connectivity between the SCN and the locus coeruleus and raphe nucleus was found in patients with chronic insomnia.
The decreased causal connectivity from the locus coeruleus to the SCN was associated with the duration of the insomnia disorder.
These disruptions may relate to the cognitive and wake-promoting processes linked to the neuropathology of chronic insomnia.

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The importance of the suprachiasmatic nucleus (SCN, also called the master circadian clock) in regulating sleep and wakefulness has been confirmed by multiple animal research. However, human studies of SCN in vivo are still nascent. Recently, the development of resting-state functional magnetic resonance imaging (fMRI) has made it possible to study SCN-related connectivity changes in patients with chronic insomnia disorder (CID). Hence, this study aimed to explore whether sleep-wake circuitry (i.e., communication between the SCN and other brain regions) is disrupted in human insomnia. Forty-two patients with CID and 37 healthy controls (HCs) underwent fMRI scanning. Resting-state functional connectivity (rsFC) and Granger causality analysis (GCA) were performed to find abnormal functional and causal connectivity of the SCN in CID patients. In addition, correlation analyses were conducted to detect associations between features of disrupted connectivity and clinical symptoms. Compared to HCs, CID patients showed enhanced rsFC of the SCN-left dorsolateral prefrontal cortex (DLPFC), as well as reduced rsFC of the SCN-bilateral medial prefrontal cortex (MPFC); these altered cortical regions belong to the "top-down" circuit. Moreover, CID patients exhibited disrupted functional and causal connectivity between the SCN and the locus coeruleus (LC) and the raphe nucleus (RN); these altered subcortical regions constitute the "bottom-up" pathway. Importantly, the decreased causal connectivity from the LC-to-SCN was associated with the duration of disease in CID patients. These findings suggest that the disruption of the SCN-centered "top-down" cognitive process and "bottom-up" wake-promoting pathway may be intimately tied to the neuropathology of CID.

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Top-down and bottom-up alterations of connectivity patterns of the suprachiasmatic nucleus in chronic insomnia disorder

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