Cheuk Ni Kan, Mirthe Coenen, Xin Xu, Saima Hilal, Frederik Barkhof, Thomas Benke, Peter Dal-Bianco, Charles DeCarli, Marco Duering, Christian Enzinger, Lieza G Exalto, Evan F Fletcher, Edith Hofer, Huiberdina L Koek, Hugo J Kuijf, Pauline M Maillard, Justine E F Moonen, Janne M Papma, Yolande A L Pijnenburg, Reinhold Schmidt, Rebecca M E Steketee, Esther van den Berg, Wiesje M van der Flier, Narayanaswamy Venketasubramanian, Meike W Vernooij, Frank J Wolters, Geert Jan Biessels, Christopher Li-Hsian Chen, J Matthijs Biesbroek, Chin Hong Tan
{"title":"束特异性白质高信号和神经精神综合征:一项多中心记忆临床研究。","authors":"Cheuk Ni Kan, Mirthe Coenen, Xin Xu, Saima Hilal, Frederik Barkhof, Thomas Benke, Peter Dal-Bianco, Charles DeCarli, Marco Duering, Christian Enzinger, Lieza G Exalto, Evan F Fletcher, Edith Hofer, Huiberdina L Koek, Hugo J Kuijf, Pauline M Maillard, Justine E F Moonen, Janne M Papma, Yolande A L Pijnenburg, Reinhold Schmidt, Rebecca M E Steketee, Esther van den Berg, Wiesje M van der Flier, Narayanaswamy Venketasubramanian, Meike W Vernooij, Frank J Wolters, Geert Jan Biessels, Christopher Li-Hsian Chen, J Matthijs Biesbroek, Chin Hong Tan","doi":"10.1136/jnnp-2024-334264","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>White matter hyperintensities (WMH) have been implicated in the pathogenesis of neuropsychiatric symptoms of dementia but the functional significance of WMH in specific white matter (WM) tracts is unclear. We investigate whether WMH burden within major WM fibre classes and individual WM tracts are differentially associated with different neuropsychiatric syndromes in a large multicentre study.</p><p><strong>Method: </strong>Neuroimaging and neuropsychiatric data of seven memory clinic cohorts through the Meta VCI Map consortium were harmonised. Class-based analyses of major WM fibres (association, commissural and projection) and region-of-interest-based analyses on 11 individual WM tracts were used to evaluate associations of WMH volume with severity of hyperactivity, psychosis, affective and apathy syndromes.</p><p><strong>Results: </strong>Among 2935 patients (50.4% women; mean age=72.2 years; 19.8% subjective cognitive impairment, 39.8% mild cognitive impairment, and 40.4% dementia), larger WMH volume within projection fibres (B=0.24, SE=0.10, p=0.013) was associated with greater apathy. Larger WMH volume within association (B=0.31, SE=0.12, p=0.009), commissural (B=0.47, SE=0.17, p=0.006) and projection (B=0.39, SE=0.16, p=0.016) fibres was associated with greater hyperactivity, driven by the inferior fronto-occipital fasciculus (B=0.50, SE=0.18, p=0.006), forceps major (B=0.48, SE=0.18, p=0.009) and anterior thalamic radiation (B=0.49, SE=0.19, p=0.011), respectively. Larger WMH volume in the uncinate fasciculus (B=1.82, SE=0.67, p=0.005) and forceps minor (B=0.61, SE=0.19, p=0.001) were additionally associated with greater apathy. No associations with affective and psychosis were observed.</p><p><strong>Conclusions: </strong>Tract-syndrome specificity of WMH burden with apathy and hyperactivity suggests that disruption of strategic neuronal pathways may be a potential mechanism through which small vessel disease affects emotional and behavioural regulation in memory clinic patients.</p>","PeriodicalId":16418,"journal":{"name":"Journal of Neurology, Neurosurgery, and Psychiatry","volume":"96 7","pages":"697-704"},"PeriodicalIF":8.7000,"publicationDate":"2025-06-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Tract-specific white matter hyperintensities and neuropsychiatric syndromes: a multicentre memory clinic study.\",\"authors\":\"Cheuk Ni Kan, Mirthe Coenen, Xin Xu, Saima Hilal, Frederik Barkhof, Thomas Benke, Peter Dal-Bianco, Charles DeCarli, Marco Duering, Christian Enzinger, Lieza G Exalto, Evan F Fletcher, Edith Hofer, Huiberdina L Koek, Hugo J Kuijf, Pauline M Maillard, Justine E F Moonen, Janne M Papma, Yolande A L Pijnenburg, Reinhold Schmidt, Rebecca M E Steketee, Esther van den Berg, Wiesje M van der Flier, Narayanaswamy Venketasubramanian, Meike W Vernooij, Frank J Wolters, Geert Jan Biessels, Christopher Li-Hsian Chen, J Matthijs Biesbroek, Chin Hong Tan\",\"doi\":\"10.1136/jnnp-2024-334264\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>White matter hyperintensities (WMH) have been implicated in the pathogenesis of neuropsychiatric symptoms of dementia but the functional significance of WMH in specific white matter (WM) tracts is unclear. We investigate whether WMH burden within major WM fibre classes and individual WM tracts are differentially associated with different neuropsychiatric syndromes in a large multicentre study.</p><p><strong>Method: </strong>Neuroimaging and neuropsychiatric data of seven memory clinic cohorts through the Meta VCI Map consortium were harmonised. Class-based analyses of major WM fibres (association, commissural and projection) and region-of-interest-based analyses on 11 individual WM tracts were used to evaluate associations of WMH volume with severity of hyperactivity, psychosis, affective and apathy syndromes.</p><p><strong>Results: </strong>Among 2935 patients (50.4% women; mean age=72.2 years; 19.8% subjective cognitive impairment, 39.8% mild cognitive impairment, and 40.4% dementia), larger WMH volume within projection fibres (B=0.24, SE=0.10, p=0.013) was associated with greater apathy. Larger WMH volume within association (B=0.31, SE=0.12, p=0.009), commissural (B=0.47, SE=0.17, p=0.006) and projection (B=0.39, SE=0.16, p=0.016) fibres was associated with greater hyperactivity, driven by the inferior fronto-occipital fasciculus (B=0.50, SE=0.18, p=0.006), forceps major (B=0.48, SE=0.18, p=0.009) and anterior thalamic radiation (B=0.49, SE=0.19, p=0.011), respectively. Larger WMH volume in the uncinate fasciculus (B=1.82, SE=0.67, p=0.005) and forceps minor (B=0.61, SE=0.19, p=0.001) were additionally associated with greater apathy. No associations with affective and psychosis were observed.</p><p><strong>Conclusions: </strong>Tract-syndrome specificity of WMH burden with apathy and hyperactivity suggests that disruption of strategic neuronal pathways may be a potential mechanism through which small vessel disease affects emotional and behavioural regulation in memory clinic patients.</p>\",\"PeriodicalId\":16418,\"journal\":{\"name\":\"Journal of Neurology, Neurosurgery, and Psychiatry\",\"volume\":\"96 7\",\"pages\":\"697-704\"},\"PeriodicalIF\":8.7000,\"publicationDate\":\"2025-06-12\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Neurology, Neurosurgery, and Psychiatry\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1136/jnnp-2024-334264\",\"RegionNum\":1,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"CLINICAL NEUROLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neurology, Neurosurgery, and Psychiatry","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1136/jnnp-2024-334264","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
Tract-specific white matter hyperintensities and neuropsychiatric syndromes: a multicentre memory clinic study.
Background: White matter hyperintensities (WMH) have been implicated in the pathogenesis of neuropsychiatric symptoms of dementia but the functional significance of WMH in specific white matter (WM) tracts is unclear. We investigate whether WMH burden within major WM fibre classes and individual WM tracts are differentially associated with different neuropsychiatric syndromes in a large multicentre study.
Method: Neuroimaging and neuropsychiatric data of seven memory clinic cohorts through the Meta VCI Map consortium were harmonised. Class-based analyses of major WM fibres (association, commissural and projection) and region-of-interest-based analyses on 11 individual WM tracts were used to evaluate associations of WMH volume with severity of hyperactivity, psychosis, affective and apathy syndromes.
Results: Among 2935 patients (50.4% women; mean age=72.2 years; 19.8% subjective cognitive impairment, 39.8% mild cognitive impairment, and 40.4% dementia), larger WMH volume within projection fibres (B=0.24, SE=0.10, p=0.013) was associated with greater apathy. Larger WMH volume within association (B=0.31, SE=0.12, p=0.009), commissural (B=0.47, SE=0.17, p=0.006) and projection (B=0.39, SE=0.16, p=0.016) fibres was associated with greater hyperactivity, driven by the inferior fronto-occipital fasciculus (B=0.50, SE=0.18, p=0.006), forceps major (B=0.48, SE=0.18, p=0.009) and anterior thalamic radiation (B=0.49, SE=0.19, p=0.011), respectively. Larger WMH volume in the uncinate fasciculus (B=1.82, SE=0.67, p=0.005) and forceps minor (B=0.61, SE=0.19, p=0.001) were additionally associated with greater apathy. No associations with affective and psychosis were observed.
Conclusions: Tract-syndrome specificity of WMH burden with apathy and hyperactivity suggests that disruption of strategic neuronal pathways may be a potential mechanism through which small vessel disease affects emotional and behavioural regulation in memory clinic patients.
期刊介绍:
The Journal of Neurology, Neurosurgery & Psychiatry (JNNP) aspires to publish groundbreaking and cutting-edge research worldwide. Covering the entire spectrum of neurological sciences, the journal focuses on common disorders like stroke, multiple sclerosis, Parkinson’s disease, epilepsy, peripheral neuropathy, subarachnoid haemorrhage, and neuropsychiatry, while also addressing complex challenges such as ALS. With early online publication, regular podcasts, and an extensive archive collection boasting the longest half-life in clinical neuroscience journals, JNNP aims to be a trailblazer in the field.