Altered spatiotemporal brain dynamics of interoception in behavioural-variant frontotemporal dementia.

IF 10.8 1区 医学 Q1 MEDICINE, RESEARCH & EXPERIMENTAL EBioMedicine Pub Date : 2025-03-01 Epub Date: 2025-02-22 DOI:10.1016/j.ebiom.2025.105614
Jessica L Hazelton, Gabriel Della Bella, Pablo Barttfeld, Martin Dottori, Raul Gonzalez-Gomez, Joaquín Migeot, Sebastian Moguilner, Agustina Legaz, Hernan Hernandez, Pavel Prado, Jhosmary Cuadros, Marcelo Maito, Matias Fraile-Vazquez, María Luz González Gadea, Yasir Çatal, Bruce Miller, Olivier Piguet, Georg Northoff, Agustin Ibáñez
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Abstract

Background: Dysfunctional allostatic-interoception, altered processing of bodily signals in response to environmental demands, occurs in behavioural-variant frontotemporal dementia (bvFTD) patients. Previous research has not investigated the dynamic nature of interoception using methods like intrinsic neural timescales. We hypothesised that longer intrinsic neural timescales of interoception would occur in bvFTD patients, evidencing dysfunctional allostatic-interoception.

Methods: One-hundred and twelve participants (31 bvFTD patients, 35 Alzheimer's disease patients, AD and 46 healthy controls) completed a well-validated task measuring cardiac-interoception and exteroception. Simultaneous EEG and ECG were recorded. Intrinsic neural timescales were measured via the autocorrelation window (ACW) of broadband EEG signals from each heartbeat and a time-lagged version of itself. Spatiotemporal clustering analyses identified clusters with significant between-group differences in each condition. Voxel-based morphometry was used to target the allostatic-interoceptive network. Neuropsychological tests of cognition and social cognition were assessed.

Findings: In bvFTD patients, longer interoceptive-ACWs than controls were observed in the bilateral fronto-temporal and parietal regions. In AD patients, longer interoceptive-ACWs than controls were observed in central and occipitoparietal brain regions. No differences were observed during exteroception. In bvFTD patients only, longer interoceptive-ACW was linked to worse sociocognitive performance. Structural neural correlates of interoceptive-ACW in bvFTD involved the anterior cingulate, insula, orbitofrontal cortex, hippocampus, and angular gyrus.

Interpretation: Our findings suggest a core allostatic-interoceptive deficit occurs in people with bvFTD. Further, altered interoceptive intrinsic neural timescales may provide a neurobiological mechanism underpinning the complex behaviours observed in bvFTD patients. Our findings support synergistic models of brain disease and can inform clinical practice.

Funding: All funding sources are reported in the Acknowledgements.

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行为变异额颞叶痴呆中内感受的时空脑动力学改变。
背景:在行为变异性额颞叶痴呆(bvFTD)患者中发生功能失调的异源静态内感受,即身体信号处理因环境要求而改变。以前的研究没有使用内在神经时间尺度等方法来调查内感受的动态性质。我们假设bvFTD患者会出现更长的内感受神经时间尺度,这证明了异源静态内感受功能不正常。方法:112名参与者(31名bvFTD患者,35名阿尔茨海默病患者,AD患者和46名健康对照)完成了一项有效的测量心脏内感受和外感受的任务。同时记录脑电图和心电图。内在神经时间标度是通过每次心跳的宽带脑电图信号的自相关窗口(ACW)和自身的时间滞后版本来测量的。时空聚类分析发现,在每个条件下,组间差异显著。基于体素的形态测量技术被用于定位同种静态内感受网络。进行认知和社会认知的神经心理测试。结果:在bvFTD患者中,双侧额颞区和顶叶区观察到的内感受性acw比对照组更长。在AD患者中,在中枢和枕顶脑区观察到的内感受性acw比对照组更长。在外知觉过程中没有观察到差异。仅在bvFTD患者中,较长的内感受性acw与较差的社会认知表现有关。bvFTD的内感受性acw的结构神经相关涉及前扣带、脑岛、眶额皮质、海马和角回。解释:我们的研究结果表明,bvFTD患者存在核心的适应静态内感受缺陷。此外,改变的内感受性内在神经时间尺度可能为bvFTD患者观察到的复杂行为提供了神经生物学机制。我们的发现支持脑疾病的协同模型,并可以为临床实践提供信息。资金来源:在致谢中报告了所有的资金来源。
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来源期刊
EBioMedicine
EBioMedicine Biochemistry, Genetics and Molecular Biology-General Biochemistry,Genetics and Molecular Biology
CiteScore
17.70
自引率
0.90%
发文量
579
审稿时长
5 weeks
期刊介绍: eBioMedicine is a comprehensive biomedical research journal that covers a wide range of studies that are relevant to human health. Our focus is on original research that explores the fundamental factors influencing human health and disease, including the discovery of new therapeutic targets and treatments, the identification of biomarkers and diagnostic tools, and the investigation and modification of disease pathways and mechanisms. We welcome studies from any biomedical discipline that contribute to our understanding of disease and aim to improve human health.
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