Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2

ABSTRACT Objective Spinocerebellar ataxia type 2 (SCA2) is a hereditary cerebellar degenerative disorder, with motor and cognitive symptoms. The constellation of cognitive symptoms due to cerebellar degeneration is named cerebellar cognitive affective syndrome (CCAS), which has increasingly been rec...

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Main Authors: Ami Kumar, Ruo‐Yah Lai, Zena Fadel, Yicheng Lin, Pia Parekh, Rachel Griep, Ming‐Kai Pan, Sheng‐Han Kuo
Format: Article
Language:English
Published: Wiley 2025-06-01
Series:Annals of Clinical and Translational Neurology
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Online Access:https://doi.org/10.1002/acn3.70028
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author Ami Kumar
Ruo‐Yah Lai
Zena Fadel
Yicheng Lin
Pia Parekh
Rachel Griep
Ming‐Kai Pan
Sheng‐Han Kuo
author_facet Ami Kumar
Ruo‐Yah Lai
Zena Fadel
Yicheng Lin
Pia Parekh
Rachel Griep
Ming‐Kai Pan
Sheng‐Han Kuo
author_sort Ami Kumar
collection DOAJ
description ABSTRACT Objective Spinocerebellar ataxia type 2 (SCA2) is a hereditary cerebellar degenerative disorder, with motor and cognitive symptoms. The constellation of cognitive symptoms due to cerebellar degeneration is named cerebellar cognitive affective syndrome (CCAS), which has increasingly been recognized to profoundly impact patients' quality of life; however, the brain circuits underlying these cognitive dysfunctions remain elusive. Methods We utilized a novel technique, cerebello‐cortical electroencephalogram (EEG), to investigate the resting‐state functional connectivity in different frequency domains in 12 SCA2 patients and 24 age‐matched controls. Given that the prefrontal cortex is strongly connected to the cerebellum, we studied the EEG connectivity between the cerebellum and the prefrontal cortex. We also conducted correlation analyses to explore the association between this connectivity and the severity of cognitive dysfunction, determined by CCAS scores. Results Source‐space spectral analysis differences between SCA2 patients and controls were observed in the cerebellum at the delta, theta, and beta frequencies. Functional connectivity between the posterior cerebellum and the prefrontal cortex revealed decreased theta and increased beta connectivity in SCA2 patients, with no differences in delta connectivity. Increased beta connectivity was unique to the prefrontal regions, not seen in the connectivity to the primary motor cortex or mid‐temporal lobe. Interestingly, this beta connectivity correlated with CCAS scores in SCA2 patients. Conclusion Our findings demonstrated that SCA2 patients have an increase in beta cerebello‐prefrontal connectivity that correlates with cognitive performance. These findings suggest cerebello‐cortical EEG could track circuit dysfunction underlying cognitive symptoms in SCA2, paving the way for developing targeted neuromodulation therapeutics.
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spelling doaj-art-3d2e418b5d444684ab6a18054d5b997f2025-08-20T03:45:40ZengWileyAnnals of Clinical and Translational Neurology2328-95032025-06-011261109111710.1002/acn3.70028Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2Ami Kumar0Ruo‐Yah Lai1Zena Fadel2Yicheng Lin3Pia Parekh4Rachel Griep5Ming‐Kai Pan6Sheng‐Han Kuo7Department of Neurology, College of Physicians and Surgeons Columbia University New York New York USADepartment of Neurology, College of Physicians and Surgeons Columbia University New York New York USAInitiative for Columbia Ataxia and Tremor Columbia University New York New York USADepartment of Neurology, College of Physicians and Surgeons Columbia University New York New York USADepartment of Neurology, College of Physicians and Surgeons Columbia University New York New York USADepartment of Neurology, College of Physicians and Surgeons Columbia University New York New York USACerebellar Research Center National Taiwan University Hospital, Yun‐Lin Branch Yun‐Lin TaiwanDepartment of Neurology, College of Physicians and Surgeons Columbia University New York New York USAABSTRACT Objective Spinocerebellar ataxia type 2 (SCA2) is a hereditary cerebellar degenerative disorder, with motor and cognitive symptoms. The constellation of cognitive symptoms due to cerebellar degeneration is named cerebellar cognitive affective syndrome (CCAS), which has increasingly been recognized to profoundly impact patients' quality of life; however, the brain circuits underlying these cognitive dysfunctions remain elusive. Methods We utilized a novel technique, cerebello‐cortical electroencephalogram (EEG), to investigate the resting‐state functional connectivity in different frequency domains in 12 SCA2 patients and 24 age‐matched controls. Given that the prefrontal cortex is strongly connected to the cerebellum, we studied the EEG connectivity between the cerebellum and the prefrontal cortex. We also conducted correlation analyses to explore the association between this connectivity and the severity of cognitive dysfunction, determined by CCAS scores. Results Source‐space spectral analysis differences between SCA2 patients and controls were observed in the cerebellum at the delta, theta, and beta frequencies. Functional connectivity between the posterior cerebellum and the prefrontal cortex revealed decreased theta and increased beta connectivity in SCA2 patients, with no differences in delta connectivity. Increased beta connectivity was unique to the prefrontal regions, not seen in the connectivity to the primary motor cortex or mid‐temporal lobe. Interestingly, this beta connectivity correlated with CCAS scores in SCA2 patients. Conclusion Our findings demonstrated that SCA2 patients have an increase in beta cerebello‐prefrontal connectivity that correlates with cognitive performance. These findings suggest cerebello‐cortical EEG could track circuit dysfunction underlying cognitive symptoms in SCA2, paving the way for developing targeted neuromodulation therapeutics.https://doi.org/10.1002/acn3.70028cerebellumcognitionelectroencephalogram (EEG)functional connectivityspinocerebellar ataxia type 2 (SCA2)
spellingShingle Ami Kumar
Ruo‐Yah Lai
Zena Fadel
Yicheng Lin
Pia Parekh
Rachel Griep
Ming‐Kai Pan
Sheng‐Han Kuo
Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2
Annals of Clinical and Translational Neurology
cerebellum
cognition
electroencephalogram (EEG)
functional connectivity
spinocerebellar ataxia type 2 (SCA2)
title Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2
title_full Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2
title_fullStr Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2
title_full_unstemmed Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2
title_short Cerebello‐Prefrontal Connectivity Underlying Cognitive Dysfunction in Spinocerebellar Ataxia Type 2
title_sort cerebello prefrontal connectivity underlying cognitive dysfunction in spinocerebellar ataxia type 2
topic cerebellum
cognition
electroencephalogram (EEG)
functional connectivity
spinocerebellar ataxia type 2 (SCA2)
url https://doi.org/10.1002/acn3.70028
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