Functional connectivity and metabolic brain alterations in sleepwalkers

IF 3.9 2区医学 Q1 CLINICAL NEUROLOGY European Journal of Neurology Pub Date : 2025-01-27 DOI:10.1111/ene.70008

Greta Mainieri, Magali Jane Rochat, Elena Cantoni, Giovanni Sighinolfi, Micaela Mitolo, Giuseppe Loddo, Francesco Mignani, Susanna Mondini, Raffaele Lodi, Federica Provini, Caterina Tonon

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Abstract

Objective

Disorders of arousal (DoA) are characterized by an intermediate state between wakefulness and deep sleep, leading to incomplete awakenings from NREM sleep. Multimodal studies have shown subtle neurophysiologic alterations even during wakefulness in DoA. The aim of this study was to explore the brain functional connectivity in DoA and the metabolic profile of the anterior and posterior cingulate cortex, given its pivotal role in cognitive and emotional processing.

Methods

Fifteen consecutive patients with DoA (9 males, mean age 26.3 ± 7.7) and 15 age- and sex-matched healthy controls (8 males, mean age 25.8 ± 3.6) were enrolled. All participants underwent a protocol including sleep and psychological evaluation scales and multimodal brain MRI with resting-state functional MRI and 1H-MR spectroscopy.

Results

The independent component analysis disclosed an altered resting-state functional connectivity (FC) in the patients' sensory motor network, with a higher connectivity strength in opercular cortex, precuneus, occipital pole, and lingual gyrus. The seed-based analysis revealed a decreased FC between posterior cingulate cortex (PCC) and several cerebral areas. Finally, spectroscopic imaging revealed a reduced content of glutamine in the PCC (p < 0.001).

Interpretation

The increased connectivity in the sensory-motor network of DoA patients could constitute a “facilitatory medium” enhancing motor circuit activation, while the connectivity and metabolic alterations of PCC might represent a trait functional feature, contributing to a dysfunctional arousal process and the difficulty to reach a complete awareness during DoA episodes. In addition, these alterations at rest might be related to daytime impairment reported by patients, requiring new strategies for DoA management.

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梦游者的功能连通性和大脑代谢改变。

目的：觉醒障碍（DoA）是一种介于清醒和深度睡眠之间的中间状态，导致非快速眼动睡眠的不完全觉醒。多模态研究表明，即使在DoA的清醒状态下，神经生理也会发生微妙的变化。考虑到扣带皮层在认知和情绪加工中的关键作用，本研究的目的是探讨DoA脑功能连接和前、后扣带皮层的代谢谱。方法：连续纳入15例DoA患者（男性9例，平均年龄26.3±7.7岁）和15例年龄和性别匹配的健康对照（男性8例，平均年龄25.8±3.6岁）。所有参与者都接受了包括睡眠和心理评估量表和多模态脑MRI与静息状态功能MRI和1H-MR光谱的协议。结果：独立分量分析显示，患者感觉运动网络的静息状态功能连通性（FC）发生改变，其中眼皮层、楔前叶、枕极和舌回的连通性强度较高。基于种子的分析显示，后扣带皮层（PCC）和几个大脑区域之间的FC减少。解释：DoA患者感觉-运动网络连通性的增加可能构成了一种“促进介质”，增强了运动电路的激活，而PCC的连通性和代谢改变可能代表了一种特征功能特征，导致了觉醒过程的功能障碍，并且在DoA发作期间难以达到完全的意识。此外，这些休息时的改变可能与患者报告的日间损伤有关，需要新的DoA管理策略。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

European Journal of Neurology 医学-临床神经学

CiteScore

9.70

自引率

2.00%

发文量

418

审稿时长

1 months

期刊介绍： The European Journal of Neurology is the official journal of the European Academy of Neurology and covers all areas of clinical and basic research in neurology, including pre-clinical research of immediate translational value for new potential treatments. Emphasis is placed on major diseases of large clinical and socio-economic importance (dementia, stroke, epilepsy, headache, multiple sclerosis, movement disorders, and infectious diseases).