Hazelton Jessica L, Carneiro Fábio, Maito Marcelo, Richter Fabian, Legaz Agustina, Altschuler Florencia, Cubillos-Pinilla Leidy, Chen Yu, Doherty Colin P, Baez Sandra, Ibáñez Agustín
Latin American Brain Health Institute, Universidad Adolfo Ibáñez, Santiago, Chile; Cognitive Neuroscience Center, Universidad de San Andrés, Buenos Aires, Argentina; The University of Sydney, Brain and Mind Centre, School of Psychology, Sydney, Australia.
Laboratory of Neuropsychophysiology, Faculty of Psychology and Education Sciences, University of Porto, Porto, Portugal; Faculty of Medicine, University of Porto, Porto, Portugal; Department of Neurology, Unidade Local de Saúde do Alto Ave, Guimarães, Portugal.
Biol Psychiatry. 2025 Jun 1;97(11):1079-1090. doi: 10.1016/j.biopsych.2024.10.013. Epub 2024 Oct 21.
Simultaneous interoceptive, emotional, and social cognition deficits are observed across neurodegenerative diseases. Indirect evidence suggests shared neurobiological bases underlying these impairments, termed the allostatic-interoceptive network (AIN). However, no study has yet explored the convergence of these deficits in neurodegenerative diseases or examined how structural and functional changes contribute to cross-domain impairments.
A Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) activated likelihood estimate meta-analysis encompassed studies that met the following inclusion criteria: interoception, emotion, or social cognition tasks; neurodegenerative diseases (behavioral variant frontotemporal dementia, primary progressive aphasias, Alzheimer's disease, Parkinson's disease, multiple sclerosis); and neuroimaging (structural: magnetic resonance imaging voxel-based morphometry; functional: magnetic resonance imaging and fluorodeoxyglucose-positron emission tomography).
Of 20,593 studies, 170 met inclusion criteria (58 interoception, 65 emotion, and 47 social cognition) involving 7032 participants (4963 patients and 2069 healthy control participants). In all participants combined, conjunction analyses revealed AIN involvement of the insula, amygdala, orbitofrontal cortex, anterior cingulate, striatum, thalamus, and hippocampus across domains. In behavioral variant frontotemporal dementia, this conjunction was replicated across domains, with further involvement of the temporal pole, temporal fusiform cortex, and angular gyrus. A convergence of interoception and emotion in the striatum, thalamus, and hippocampus in Parkinson's disease and the posterior insula in primary progressive aphasias was also observed. In Alzheimer's disease and multiple sclerosis, disruptions in the AIN were observed during interoception, but no convergence with emotion was identified.
Neurodegeneration induces dysfunctional AIN across atrophy, connectivity, and metabolism, more accentuated in behavioral variant frontotemporal dementia. Findings bolster the predictive coding theories of large-scale AIN, calling for more synergistic approaches to understanding interoception, emotion, and social cognition impairments in neurodegeneration.
在多种神经退行性疾病中均观察到同时存在的内感受、情绪和社会认知缺陷。间接证据表明，这些损伤存在共同的神经生物学基础，即所谓的稳态内感受网络（AIN）。然而，尚无研究探讨神经退行性疾病中这些缺陷的汇聚情况，也未研究结构和功能变化如何导致跨领域损伤。
一项系统评价和荟萃分析的首选报告项目（PRISMA）激活似然估计荟萃分析纳入了符合以下纳入标准的研究：内感受、情绪或社会认知任务；神经退行性疾病（行为变异型额颞叶痴呆、原发性进行性失语症、阿尔茨海默病、帕金森病、多发性硬化症）；以及神经影像学（结构：基于磁共振成像体素的形态测量；功能：磁共振成像和氟脱氧葡萄糖正电子发射断层扫描）。
在20593项研究中，170项符合纳入标准（58项内感受、65项情绪和47项社会认知），涉及7032名参与者（4963名患者和2069名健康对照参与者）。在所有参与者中，联合分析显示，AIN涉及岛叶、杏仁核、眶额皮质、前扣带回、纹状体、丘脑和海马体等跨领域区域。在行为变异型额颞叶痴呆中，这种联合在各领域均得到重复，颞极、颞梭状回皮质和角回也进一步受累。在帕金森病的纹状体、丘脑和海马体以及原发性进行性失语症的后岛叶中也观察到内感受和情绪的汇聚。在阿尔茨海默病和多发性硬化症中，在内感受过程中观察到AIN的破坏，但未发现与情绪的汇聚。
神经退行性变会导致AIN在萎缩、连接性和代谢方面出现功能障碍，在行为变异型额颞叶痴呆中更为明显。研究结果支持了大规模AIN的预测编码理论，呼吁采用更多协同方法来理解神经退行性变中的内感受、情绪和社会认知损伤。
