Alice Tisserand, Frédéric Blanc, Candice Muller, Hélène Durand, Catherine Demuynck, Alix Ravier, Léa Sanna, Paulo Loureiro de Sousa, Anne Botzung, Mary Mondino, Nathalie Philippi
{"title":"路易体痴呆症患者自传体记忆的神经成像:脑岛的故事。","authors":"Alice Tisserand, Frédéric Blanc, Candice Muller, Hélène Durand, Catherine Demuynck, Alix Ravier, Léa Sanna, Paulo Loureiro de Sousa, Anne Botzung, Mary Mondino, Nathalie Philippi","doi":"10.1093/braincomms/fcae272","DOIUrl":null,"url":null,"abstract":"<p><p>Although deficits in learning and retrieving new information are well characterized in dementia with Lewy bodies, autobiographical memory has never been explored in this disease. Yet, autobiographical memory impairments are a pervasive feature of dementia, well characterized in other neurodegenerative diseases. Moreover, autobiographical memory corresponds to an extension over time of the self, which we hypothesize is altered in dementia with Lewy bodies and impairment of which could be linked to the insular atrophy occurring from an early stage of the disease. In this study, we sought to characterize autobiographical memory impairments and explore their neural correlates in dementia with Lewy bodies, on the assumption that insular damage could impact the self, including its most elaborate components, such as autobiographical memory. Twenty patients with prodromal to mild dementia with Lewy bodies were selected to participate in this exploratory study along with 20 healthy control subjects. The Autobiographical Interview was used to assess autobiographical memory. Performances were compared between patients and control subjects, and an analysis across life periods and recall conditions was performed. 3D magnetic resonance images were acquired for all participants, and correlational analyses were performed in the patient group using voxel-based morphometry. The behavioural results of the Autobiographical Interview showed that autobiographical memory performances were significantly impaired in dementia with Lewy body patients compared to control subjects in a temporally ungraded manner, for both the free recall and the specific probe conditions (<i>P</i> < 0.0001), though with greater improvement after probing in the patient group. Furthermore, autobiographical memory impairments were correlated with grey matter volume within right insular cortex, temporoparietal junction, precuneus, putamen, left temporal cortex, bilateral parahippocampus and cerebellum, using a threshold of <i>P</i> = 0.005 uncorrected. The behavioural results confirm the existence of temporally ungraded autobiographical memory impairments in dementia with Lewy bodies, from the early stage of the disease. As we expected, neuroimaging analysis revealed a role for the insula and the precuneus in autobiographical memory retrieval, two regions associated with elementary aspects of the self, among other brain regions classically associated with autobiographical memory, such as medial temporal lobe and temporoparietal junction. Our findings provide important insights regarding the involvement of the insula in the self and suggest that insular damage could lead to a global collapse of the self, including its more elaborated components, such as autobiographical memory.</p>","PeriodicalId":93915,"journal":{"name":"Brain communications","volume":null,"pages":null},"PeriodicalIF":4.1000,"publicationDate":"2024-08-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11358644/pdf/","citationCount":"0","resultStr":"{\"title\":\"Neuroimaging of autobiographical memory in dementia with Lewy bodies: a story of insula.\",\"authors\":\"Alice Tisserand, Frédéric Blanc, Candice Muller, Hélène Durand, Catherine Demuynck, Alix Ravier, Léa Sanna, Paulo Loureiro de Sousa, Anne Botzung, Mary Mondino, Nathalie Philippi\",\"doi\":\"10.1093/braincomms/fcae272\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Although deficits in learning and retrieving new information are well characterized in dementia with Lewy bodies, autobiographical memory has never been explored in this disease. Yet, autobiographical memory impairments are a pervasive feature of dementia, well characterized in other neurodegenerative diseases. Moreover, autobiographical memory corresponds to an extension over time of the self, which we hypothesize is altered in dementia with Lewy bodies and impairment of which could be linked to the insular atrophy occurring from an early stage of the disease. In this study, we sought to characterize autobiographical memory impairments and explore their neural correlates in dementia with Lewy bodies, on the assumption that insular damage could impact the self, including its most elaborate components, such as autobiographical memory. Twenty patients with prodromal to mild dementia with Lewy bodies were selected to participate in this exploratory study along with 20 healthy control subjects. The Autobiographical Interview was used to assess autobiographical memory. Performances were compared between patients and control subjects, and an analysis across life periods and recall conditions was performed. 3D magnetic resonance images were acquired for all participants, and correlational analyses were performed in the patient group using voxel-based morphometry. The behavioural results of the Autobiographical Interview showed that autobiographical memory performances were significantly impaired in dementia with Lewy body patients compared to control subjects in a temporally ungraded manner, for both the free recall and the specific probe conditions (<i>P</i> < 0.0001), though with greater improvement after probing in the patient group. Furthermore, autobiographical memory impairments were correlated with grey matter volume within right insular cortex, temporoparietal junction, precuneus, putamen, left temporal cortex, bilateral parahippocampus and cerebellum, using a threshold of <i>P</i> = 0.005 uncorrected. The behavioural results confirm the existence of temporally ungraded autobiographical memory impairments in dementia with Lewy bodies, from the early stage of the disease. As we expected, neuroimaging analysis revealed a role for the insula and the precuneus in autobiographical memory retrieval, two regions associated with elementary aspects of the self, among other brain regions classically associated with autobiographical memory, such as medial temporal lobe and temporoparietal junction. 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引用次数: 0
摘要
尽管路易体痴呆症患者在学习和检索新信息方面存在缺陷,但对这种疾病的自传体记忆却从未进行过研究。然而,自传体记忆障碍是痴呆症的一个普遍特征,也是其他神经退行性疾病的显著特征。此外,自传体记忆与自我的时间延伸相对应,我们推测路易体痴呆症患者的自传体记忆会发生改变,而自传体记忆的损伤可能与疾病早期出现的岛叶萎缩有关。在这项研究中,我们试图描述路易体痴呆症患者自传体记忆损伤的特征,并探索其神经相关性,假设岛叶损伤会影响自我,包括其最复杂的组成部分,如自传体记忆。这项探索性研究选取了 20 名路易体痴呆前驱期至轻度患者和 20 名健康对照组受试者。自传体访谈被用来评估自传体记忆。对患者和对照组受试者的表现进行了比较,并对不同生活时期和回忆条件进行了分析。研究人员为所有参与者采集了三维磁共振图像,并使用体素形态测量法对患者组进行了相关分析。自传体访谈的行为结果显示,与对照组相比,路易体痴呆症患者的自传体记忆能力在自由回忆和特定探查条件下均明显受损(P < 0.0001),但患者组在探查后改善程度更大。此外,自传体记忆障碍与右侧岛叶皮层、颞顶交界处、楔前区、普鲁门、左侧颞叶皮层、双侧海马旁和小脑的灰质体积相关,未校正阈值为 P = 0.005。行为学结果证实,路易体痴呆症患者从疾病早期开始就存在时间上未分级的自传体记忆障碍。正如我们所预期的那样,神经影像学分析表明,岛叶和楔前叶在自传体记忆检索中发挥作用,这两个区域与自我的基本方面有关,其他脑区通常与自传体记忆有关,如内侧颞叶和颞顶交界处。我们的研究结果提供了有关岛叶参与自我的重要见解,并表明岛叶损伤可能导致自我的全面崩溃,包括其更精细的组成部分,如自传体记忆。
Neuroimaging of autobiographical memory in dementia with Lewy bodies: a story of insula.
Although deficits in learning and retrieving new information are well characterized in dementia with Lewy bodies, autobiographical memory has never been explored in this disease. Yet, autobiographical memory impairments are a pervasive feature of dementia, well characterized in other neurodegenerative diseases. Moreover, autobiographical memory corresponds to an extension over time of the self, which we hypothesize is altered in dementia with Lewy bodies and impairment of which could be linked to the insular atrophy occurring from an early stage of the disease. In this study, we sought to characterize autobiographical memory impairments and explore their neural correlates in dementia with Lewy bodies, on the assumption that insular damage could impact the self, including its most elaborate components, such as autobiographical memory. Twenty patients with prodromal to mild dementia with Lewy bodies were selected to participate in this exploratory study along with 20 healthy control subjects. The Autobiographical Interview was used to assess autobiographical memory. Performances were compared between patients and control subjects, and an analysis across life periods and recall conditions was performed. 3D magnetic resonance images were acquired for all participants, and correlational analyses were performed in the patient group using voxel-based morphometry. The behavioural results of the Autobiographical Interview showed that autobiographical memory performances were significantly impaired in dementia with Lewy body patients compared to control subjects in a temporally ungraded manner, for both the free recall and the specific probe conditions (P < 0.0001), though with greater improvement after probing in the patient group. Furthermore, autobiographical memory impairments were correlated with grey matter volume within right insular cortex, temporoparietal junction, precuneus, putamen, left temporal cortex, bilateral parahippocampus and cerebellum, using a threshold of P = 0.005 uncorrected. The behavioural results confirm the existence of temporally ungraded autobiographical memory impairments in dementia with Lewy bodies, from the early stage of the disease. As we expected, neuroimaging analysis revealed a role for the insula and the precuneus in autobiographical memory retrieval, two regions associated with elementary aspects of the self, among other brain regions classically associated with autobiographical memory, such as medial temporal lobe and temporoparietal junction. Our findings provide important insights regarding the involvement of the insula in the self and suggest that insular damage could lead to a global collapse of the self, including its more elaborated components, such as autobiographical memory.