Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training
Evidence indicates that neurodegenerative diseases spread through distinct brain networks. For Parkinson's disease (PD), somatosensory abnormalities may accompany motor dysfunction in early disease stages when dopaminergic degeneration is limited to the basal ganglia. It remains unclear whether...
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Elsevier
2025-01-01
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| Series: | Neurobiology of Disease |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996124003802 |
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| author | Cheng-Wei Huang Hsin-Yun Tsai Yi-Hsuan Lin Wen-Wei Lin Chin-Hsien Lin Ming-Tsung Tseng |
| author_facet | Cheng-Wei Huang Hsin-Yun Tsai Yi-Hsuan Lin Wen-Wei Lin Chin-Hsien Lin Ming-Tsung Tseng |
| author_sort | Cheng-Wei Huang |
| collection | DOAJ |
| description | Evidence indicates that neurodegenerative diseases spread through distinct brain networks. For Parkinson's disease (PD), somatosensory abnormalities may accompany motor dysfunction in early disease stages when dopaminergic degeneration is limited to the basal ganglia. It remains unclear whether, based on the network-spread account, these abnormalities emanated from aberrant functional connectivity with the basal ganglia, and whether interventions normalizing this connectivity could reverse these abnormalities. Here, we employed functional MRI to record brain responses to tactile stimuli in patients with idiopathic PD and healthy controls before and after three-week rhythmic auditory stimulation-assisted gait (RASg) training. Consistent with the presence of striatal degeneration, patients showed right posterior putamen (pPut) hypoactivation when detecting tactile stimuli of their left leg. They also exhibited reduced functional connectivity from the right pPut to the right parietal somatosensory region (inferior parietal lobule, IPL), whose hypoactivation reflected patients' impaired tactile detectability. Importantly, this dysconnectivity predicted right IPL hypoactivation, indicating that pPut-IPL dysconnectivity underlay patients' impaired tactile detectability. Intriguingly, RASg training normalized patients' tactile detectability, which was mirrored by normalization of right IPL activation and pPut-IPL connectivity. Training-induced changes in pPut-IPL connectivity predicted changes in IPL activation during tactile detection, reinforcing the role of pPut-IPL connectivity in patients' tactile detectability. These findings suggest that somatosensory abnormalities in PD may arise from the spread of striatal pathology to relevant cortical regions. Rhythmic auditory-motor training acts to recover striatal connectivity, improving PD patients' somatosensory deficits. |
| format | Article |
| id | doaj-art-7b37a430fe394b79a220fff9b4fc6dea |
| institution | Kabale University |
| issn | 1095-953X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj-art-7b37a430fe394b79a220fff9b4fc6dea2025-01-07T04:17:10ZengElsevierNeurobiology of Disease1095-953X2025-01-01204106778Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor trainingCheng-Wei Huang0Hsin-Yun Tsai1Yi-Hsuan Lin2Wen-Wei Lin3Chin-Hsien Lin4Ming-Tsung Tseng5Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine, Taipei 10048, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, National Taiwan University and Academia Sinica, Taipei 11574, TaiwanTaiwan International Graduate Program in Interdisciplinary Neuroscience, National Taiwan University and Academia Sinica, Taipei 11574, TaiwanGraduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei 10051, TaiwanDepartment of Neurology, National Taiwan University Hospital, Taipei, Taiwan; Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan; Correspondence to: C.-H. Lin, Department of Neurology, National Taiwan University Hospital, Taipei 100225, Taiwan.Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei 10051, Taiwan; Correspondence to: M.-T. Tseng, No. 1 Jen-Ai Road Section 1, Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei 100233, Taiwan.Evidence indicates that neurodegenerative diseases spread through distinct brain networks. For Parkinson's disease (PD), somatosensory abnormalities may accompany motor dysfunction in early disease stages when dopaminergic degeneration is limited to the basal ganglia. It remains unclear whether, based on the network-spread account, these abnormalities emanated from aberrant functional connectivity with the basal ganglia, and whether interventions normalizing this connectivity could reverse these abnormalities. Here, we employed functional MRI to record brain responses to tactile stimuli in patients with idiopathic PD and healthy controls before and after three-week rhythmic auditory stimulation-assisted gait (RASg) training. Consistent with the presence of striatal degeneration, patients showed right posterior putamen (pPut) hypoactivation when detecting tactile stimuli of their left leg. They also exhibited reduced functional connectivity from the right pPut to the right parietal somatosensory region (inferior parietal lobule, IPL), whose hypoactivation reflected patients' impaired tactile detectability. Importantly, this dysconnectivity predicted right IPL hypoactivation, indicating that pPut-IPL dysconnectivity underlay patients' impaired tactile detectability. Intriguingly, RASg training normalized patients' tactile detectability, which was mirrored by normalization of right IPL activation and pPut-IPL connectivity. Training-induced changes in pPut-IPL connectivity predicted changes in IPL activation during tactile detection, reinforcing the role of pPut-IPL connectivity in patients' tactile detectability. These findings suggest that somatosensory abnormalities in PD may arise from the spread of striatal pathology to relevant cortical regions. Rhythmic auditory-motor training acts to recover striatal connectivity, improving PD patients' somatosensory deficits.http://www.sciencedirect.com/science/article/pii/S0969996124003802Parkinson's diseasefMRITactile detectionMusic-based interventionsAuditorymotor entrainmentInferior parietal lobule |
| spellingShingle | Cheng-Wei Huang Hsin-Yun Tsai Yi-Hsuan Lin Wen-Wei Lin Chin-Hsien Lin Ming-Tsung Tseng Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training Neurobiology of Disease Parkinson's disease fMRI Tactile detection Music-based interventions Auditorymotor entrainment Inferior parietal lobule |
| title | Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training |
| title_full | Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training |
| title_fullStr | Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training |
| title_full_unstemmed | Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training |
| title_short | Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training |
| title_sort | striatal cortical dysconnectivity underlies somatosensory deficits in parkinson s disease insights from rhythmic auditory motor training |
| topic | Parkinson's disease fMRI Tactile detection Music-based interventions Auditorymotor entrainment Inferior parietal lobule |
| url | http://www.sciencedirect.com/science/article/pii/S0969996124003802 |
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