Cerebello-striatal interaction mediates effects of subthalamic nucleus deep brain stimulation in Parkinson's disease

Hanßen, Henrike; Steinhardt, Julia; Münchau, Alexander; Al-Zubaidi, Arkan; Tzvi, Elinor; Heldmann, Marcus; Schramm, Peter; Neumann, Alexander; Rasche, Dirk; Saryyeva, Assel; Voges, Jürgen; Galazky, Imke; Büntjen, Lars; Heinze, Hans‐Jochen; Krauss, Joachim K.; Tronnier, V.; Münte, Thomas F.; Brüggemann, Norbert

doi:10.1016/j.parkreldis.2019.09.003

Cited by 14 publications

(15 citation statements)

References 29 publications

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“…Seven of these studies had a sample size of ≤10 patients, with a mean sample size of 8.3 patients. The remaining thirteen studies had enrolled a mean of 17.4 patients, with only five studies [25,51,54,56,60] enrolling ≥20 participants (the highest number of participants was 32).…”

Section: Sample Sizementioning

confidence: 99%

“…Eleven studies [22, 26-28, 31, 53, 55, 56, 60, 61, 63] used the "UK Parkinson's disease Brain Bank criteria" [65] for the diagnosis of idiopathic PD, four studies [41,43,45,46] adopted the "Hoehn and Yahr scale" [66], and two studies [24,54] used the "Movement Disorder Society criteria" [67]. However, most of the studies (55.8%) did not specify the adopted criteria and only reported that the cases had a neurological history of idiopathic PD.…”

Section: Diagnostic Criteria For Pdmentioning

confidence: 99%

“…Sixteen studies reported a mean UPDRS score in the ON phase (with DBS stimulation) ranging from 9.2 to 37.6, with nine of them (56.2%) reporting a score of ≤20. Four studies [47,50,54,57] did not specify the UPDRS score but only reported an increase or a decrease in the score.…”

Section: Updrs Score After Dbsmentioning

confidence: 99%

“…The remaining nine studies [52, 54, 55, 58-60, 61, 62, 64] also investigated several biomarkers but did not report any potential disease-modifying effect. However, two studies [54,59] examined different biological aspects and reported some interesting findings. One study [54] suggested that the improvements induced by DBS in PD symptoms could be due to an interaction between the cerebellum and the putamen, while the second study [59] suggested that pontine glutamine (Glx) and basal ganglia Glutamate (Glu) levels were potentially significant predictors of the efficacy of DBS, indicating a role of glutamatergic neurotransmission in the therapeutic mechanism of DBS.…”

Section: Neuroimaging Studiesmentioning

confidence: 99%

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A Systematic Review of the Biological Processes Involved in Deep-Brain Stimulation for Parkinson's disease: A Focus on the Potential Disease-Modifying Effects

et al. 2021

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Deep-Brain Stimulation (DBS) is an important treatment option for the management of Parkinson’s disease (PD) and is a common symptomatic treatment. However, an increasing number of studies have examined the biological processes to assess if DBS can also modify the natural history of PD by acting on its pathophysiological mechanisms. Relevant literature published up to November 2020 was systematically searched on databases such as PubMed, ISI Web of Knowledge, Academic Search Index, and Science Citation Index. The following predefined inclusion criteria were applied to the full-text versions of the selected articles: i) recruiting and monitoring of PD subjects that were previously treated with DBS and ii) investigating the electrophysiological, biochemical, epigenetic, or neuroimaging effects of DBS. Studies focusing exclusively on motor and clinical changes were excluded. Reviews, case reports, studies on animal models, and computational studies were also not considered. Out of 2,960 records screened, 43 studies met the inclusion criteria. Only three studies described a potential disease-modifying effect of DBS. However, a wide heterogeneity was observed in the investigated biomarkers, and the design and methodological issues of several studies limited their ability to find potential disease-modifying features. Specifically, 60.4% of the trials followed-up subjects for no more than 1 year from the surgical intervention, and 67.4% observed patients with PD only once after DBS. Moreover, 64.2% of the studies enrolled late-stage PD patients. Most of the studies (88.4%) reported that DBS only had a symptomatic effect, with several of them showing some limitations in the study design and recruitment of patients. Further studies using shared biomarkers are encouraged to assess if and how DBS might affect the progression of PD. Based on the existing preclinical literature, prospective clinical trials examining the course of PD in early-stage patients are needed.

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Section: Sample Sizementioning

confidence: 99%

Section: Diagnostic Criteria For Pdmentioning

confidence: 99%

Section: Updrs Score After Dbsmentioning

confidence: 99%

Section: Neuroimaging Studiesmentioning

confidence: 99%

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A Systematic Review of the Biological Processes Involved in Deep-Brain Stimulation for Parkinson's disease: A Focus on the Potential Disease-Modifying Effects

et al. 2021

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“…Most research focused on motor circuits in PD patients 2,16 . The brain areas mainly involved in these studies are the primary motor cortex (M1), 16,18,19 supplementary motor area (SMA), 15,19 premotor cortex, 20,21 basal ganglia, thalamus, caudal SMA, 19 cerebellum, and putamen 22 . However, the effect of STN‐DBS on brain FC remains poorly understood, and little is known of its impact on the whole brain.…”

Section: Introductionmentioning

confidence: 99%

Effect of deep brain stimulation on brain network and white matter integrity in Parkinson's disease

Huang

Chen²,

Wu³

et al. 2021

CNS Neurosci Ther

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Aims The effects of subthalamic nucleus (STN)‐deep brain stimulation (DBS) on brain topological metrics, functional connectivity (FC), and white matter integrity were studied in levodopa‐treated Parkinson’s disease (PD) patients before and after DBS. Methods Clinical assessment, resting‐state functional MRI (rs‐fMRI), and diffusion tensor imaging (DTI) were performed pre‐ and post‐DBS in 15 PD patients, using a within‐subject design. The rs‐fMRI identified brain network topological metric and FC changes using graph‐theory‐ and seed‐based methods. White matter integrity was determined by DTI and tract‐based spatial statistics. Results Unified Parkinson's Disease Rating Scale III (UPDRS‐ III) scores were significantly improved by 35.3% (p < 0.01) after DBS in PD patients, compared with pre‐DBS patients without medication. Post‐DBS PD patients showed a significant decrease in the graph‐theory‐based degree and cost in the middle temporal gyrus and temporo‐occipital part‐Right. Changes in FC were seen in four brain regions, and a decrease in white matter integrity was seen in the left anterior corona radiata. The topological metrics changes were correlated with Beck Depression Inventory II (BDI‐II) and the FC changes with UPDRS‐III scores. Conclusion STN‐DBS modulated graph‐theoretical metrics, FC, and white matter integrity. Brain connectivity changes observed with multi‐modal imaging were also associated with postoperative clinical improvement. These findings suggest that the effects of STN‐DBS are caused by brain network alterations.

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Basal Ganglia Atrophy as a Marker for Prodromal X‐Linked Dystonia‐Parkinsonism

Hanßen

Diesta

Heldmann

et al. 2023

Annals of Neurology

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In neurodegenerative diseases, the characterization of the prodromal phase is essential for the future application of disease‐modifying therapies. X‐linked dystonia‐parkinsonism is a hereditary neurodegenerative movement disorder characterized by severe adult‐onset dystonia accompanied by parkinsonism. Distinct striatal and pallidal atrophy is present already in early disease stages indicating a long‐lasting presymptomatic degenerative process. To gain insight into the prodromal phase of X‐linked dystonia‐parkinsonism, structural and iron‐sensitive magnetic resonance imaging (MRI) was performed in 10 non‐manifesting carriers and 24 healthy controls in a double‐blind fashion. Seventeen patients with X‐linked dystonia‐parkinsonism were recruited to replicate previous findings of basal ganglia pathology and iron accumulation. Age at onset was estimated in non‐manifesting carriers and patients using the repeat length of the hexanucleotide expansion and 3 single‐nucleotide polymorphisms associated with age at onset. Voxel‐based morphometry and subcortical volumetry showed striatal and pallidal atrophy in non‐manifesting carriers (~10%) and patients (~40%). Substantia nigra volume was similarly reduced in patients (~40%). Caudate volume correlated with time to estimated onset in non‐manifesting carriers. Susceptibility‐weighted imaging confirmed iron deposition in the anteromedial putamen in patients. Non‐manifesting carriers also showed small clusters of iron accumulation in the same area after lowering the statistical threshold. In conclusion, basal ganglia atrophy and iron accumulation precede the clinical onset of X‐linked dystonia‐parkinsonism and can be detected years before the estimated disease manifestation. It thereby highlights the potential of multimodal imaging to identify clinically unaffected mutation carriers with incipient neurodegeneration and to monitor disease progression independent of clinical measures. Longitudinal studies are needed to further elucidate the onset and progression rate of neurodegeneration in prodromal X‐linked dystonia‐parkinsonism. ANN NEUROL 2023;93:999–1011

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Cerebello-striatal interaction mediates effects of subthalamic nucleus deep brain stimulation in Parkinson's disease

Cited by 14 publications

References 29 publications

A Systematic Review of the Biological Processes Involved in Deep-Brain Stimulation for Parkinson's disease: A Focus on the Potential Disease-Modifying Effects

A Systematic Review of the Biological Processes Involved in Deep-Brain Stimulation for Parkinson's disease: A Focus on the Potential Disease-Modifying Effects

Effect of deep brain stimulation on brain network and white matter integrity in Parkinson's disease

Basal Ganglia Atrophy as a Marker for Prodromal X‐Linked Dystonia‐Parkinsonism

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