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Longitudinal brain functional connectivity changes induced by neurosurgical thalamotomy for tremor in Parkinson’s disease: a preliminary study

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Abstract

The hypothesis that the effectiveness of neurosurgical procedures in Parkinson’s disease (PD) would be related to connectivity dysfunctions between the site of the stimulation and other brain regions is growing. This study aimed to assess resting-state functional connectivity between thalamic ventral intermediate nucleus (Vim) and the rest of the brain before and after thalamotomy in PD. A 76-year-old right-handed woman with refractory tremor-dominant PD was selected as a candidate for left Vim radiosurgery thalamotomy. Clinical and motion sensor evaluation and brain resting-state functional MRI (rs-fMRI) were carried out before treatment and 3, 6, and 12 months later. Targeted Vim was selected as region of interest and a seed-based rs-fMRI analysis was performed in the patient and ten age- and sex-matched controls at baseline and over time. Furthermore, a correlation analysis between functional connectivity and tremor data was carried out. Both clinical and motion sensor measurements showed a progressive tremor improvement over time on right side after radiosurgery. In the patient, seed-based analysis showed a significantly increased functional connectivity between targeted Vim and ipsilateral visual areas relative to controls before treatment. Over 1 year, a normalization of aberrant pre-therapeutic functional connectivity between Vim and visual areas was obtained. At correlation analysis, the reduction of tremor metrics over time, assessed by clinical evaluation and wearable motion sensors, was related to the reduction of the left Vim–left visual cortex functional connectivity. Our findings support the evidence that fMRI was able to detect targeted Vim connectivity and its changes over time after thalamotomy.

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Data Availability

The dataset used and analyzed during the current study will be made available by the corresponding author upon request to qualified researchers (i.e., affiliated to a university or research institution/hospital).

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Funding

No funding was received for this research.

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Authors and Affiliations

  1. Neurosurgery and Gamma Knife Radiosurgery Unit, IRCCS Ospedale San Raffaele, Milan, Italy

    Luigi Albano, Roberta Balestrino, Edoardo Pompeo, Lina Raffaella Barzaghi & Pietro Mortini

  2. Neuroimaging Research Unit, Division of Neuroscience, IRCCS Ospedale San Raffaele, Milan, Italy

    Luigi Albano, Silvia Basaia, Massimo Filippi & Federica Agosta

  3. Vita-Salute San Raffaele University, Via Olgettina, 60, 20132, Milan, Italy

    Luigi Albano, Roberta Balestrino, Edoardo Pompeo, Antonella Castellano, Andrea Falini, Pietro Mortini, Massimo Filippi & Federica Agosta

  4. Department of Rehabilitation and Functional Recovery, IRCCS Ospedale San Raffaele, Milan, Italy

    Daniele Emedoli & Sandro Iannaccone

  5. Neurology Unit, IRCCS Ospedale San Raffaele, Milan, Italy

    Roberta Balestrino, Massimo Filippi & Federica Agosta

  6. Neuroradiology Unit, IRCCS Ospedale San Raffaele, Milan, Italy

    Antonella Castellano & Andrea Falini

  7. Neurorehabilitation Unit, IRCCS Ospedale San Raffaele, Milan, Italy

    Massimo Filippi

  8. Neurophysiology Service, IRCCS Ospedale San Raffaele, Milan, Italy

    Massimo Filippi

Authors
  1. Luigi Albano
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  2. Silvia Basaia
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  3. Daniele Emedoli
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  4. Roberta Balestrino
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  5. Edoardo Pompeo
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  6. Lina Raffaella Barzaghi
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  7. Antonella Castellano
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  8. Andrea Falini
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  9. Sandro Iannaccone
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  10. Pietro Mortini
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  11. Massimo Filippi
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  12. Federica Agosta
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Contributions

Design and conceptualization: LA, SB, and FA. Data statistics and analysis: LA, SB, and DE. Acquisition of data: LA, DE, RB, EP, LRB, and AC. Writing of the manuscript: LA, SB, and FA. Supervision: AF, SI, PM, MF, and FA. All authors read and approved the final paper.

Corresponding author

Correspondence to Federica Agosta.

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Conflicts of interests

L. Albano was a recipient of the Lars Leksell Fellowship. S. Basaia, D. Emedoli, R. Balestrino, E. Pompeo, L. R. Barzaghi, S. Iannaccone, and P. Mortini report no disclosures. F. Agosta is Section Editor of neuroimage: Clinical; has received speaker honoraria from Biogen Idec, Roche, Italfarmaco, and Zambon; and receives or has received research supports from the Italian Ministry of Health, Arisla (Fondazione Italiana di Ricerca per la SLA), Fondation Recherche Alzheimer (France), and the European Research Council. M. Filippi is the Editor-in-Chief of the Journal of Neurology, Associate Editor of Human Brain Mapping, Associate Editor of Radiology, and Associate Editor of Neurological Sciences; received compensation for consulting services and/or speaking activities from Alexion, Almirall, Bayer, Biogen, Celgene, Eli Lilly, Genzyme, Merck-Serono, Neopharmed Gentili, Novartis, Roche, Sanofi, Takeda, and Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Merck-Serono, Novartis, Roche, Teva Pharmaceutical Industries, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, and ARiSLA (Fondazione Italiana di Ricerca per la SLA).

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Albano, L., Basaia, S., Emedoli, D. et al. Longitudinal brain functional connectivity changes induced by neurosurgical thalamotomy for tremor in Parkinson’s disease: a preliminary study. J Neurol 270, 3623–3629 (2023). https://doi.org/10.1007/s00415-023-11705-2

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  • DOI: https://doi.org/10.1007/s00415-023-11705-2

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