Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training

Cheng-Wei Huang; Hsin-Yun Tsai; Yi-Hsuan Lin; Wen-Wei Lin; Chin-Hsien Lin; Ming-Tsung Tseng

doi:10.1016/j.nbd.2024.106778

Striatal-cortical dysconnectivity underlies somatosensory deficits in Parkinson's disease: Insights from rhythmic auditory-motor training

Neurobiol Dis. 2024 Dec 22:106778. doi: 10.1016/j.nbd.2024.106778. Online ahead of print.

Authors

Cheng-Wei Huang¹, Hsin-Yun Tsai², Yi-Hsuan Lin², Wen-Wei Lin³, Chin-Hsien Lin⁴, Ming-Tsung Tseng⁵

Affiliations

¹ Graduate Institute of Clinical Medicine, National Taiwan University College of Medicine, Taipei 10048, Taiwan.
² Taiwan International Graduate Program in Interdisciplinary Neuroscience, National Taiwan University and Academia Sinica, Taipei 11574, Taiwan.
³ Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei 10051, Taiwan.
⁴ Department of Neurology, National Taiwan University Hospital, Taipei, Taiwan; Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan. Electronic address: chlin@ntu.edu.tw.
⁵ Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei 10051, Taiwan. Electronic address: mingtsungtseng@ntu.edu.tw.

PMID: 39719198
DOI: 10.1016/j.nbd.2024.106778

Abstract

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.

Keywords: Auditorymotor entrainment; Inferior parietal lobule; Music-based interventions; Parkinson's disease; Tactile detection; fMRI.