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Tipping the scales: how clinical assessment shapes the neural correlates of Parkinson’s disease mild cognitive impairment

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Abstract

Mild cognitive impairment in Parkinson’s disease (PD-MCI) is associated with consistent structural and functional brain changes. Whether different approaches for diagnosing PD-MCI are equivalent in their neural correlates is presently unknown. We aimed to profile the neuroimaging changes associated with the two endorsed methods of diagnosing PD-MCI. We recruited 53 consecutive non-demented PD patients and classified them as PD-MCI according to comprehensive neuropsychological examination as operationalized by the Movement Disorders Task Force. Voxel-based morphometry, cortical thickness, functional connectivity and graph theoretical measures were obtained on a 3-Tesla MRI scanner. 18 patients (32%) were classified as PD-MCI with Level-II criteria, 19 (33%) with the Parkinson’s disease Cognitive Rating Scale (PD-CRS) and 32 (60%) with the Montreal Cognitive Assessment (MoCA) scale. Though regions of atrophy differed across classifications, reduced gray matter in the precuneus was found using both Level-II and PD-CRS classifications in PD-MCI patients. Patients diagnosed with the PD-CRS also showed extensive changes in cortical thickness, concurring with the MoCA in regions of the cingulate cortex, and again with Level-II regarding cortical thinning in the precuneus. Functional connectivity analysis found higher coherence within salience network regions of interest, and decreased anticorrelations between salience/central executive and default-mode networks in the PD-CRS classification for PD-MCI patients. Graph theoretical metrics showed a widespread decrease in node degree for the three classifications in PD-MCI, whereas betweenness centrality was increased in select nodes of the default mode network (DMN). Clinical and neuroimaging commonalities between the endorsed methods of cognitive assessment suggest a corresponding set of neural correlates in PD-MCI: loss of structural integrity in DMN structures, mainly the precuneus, and a loss of weighted connections in the salience network that might be counterbalanced by increased centrality in the DMN. Furthermore, the similarity of the results between exhaustive Level-II and screening Level-I tools might have practical implications in the search for neuroimaging biomarkers of cognitive impairment in Parkinson’s disease.

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Funding

The present work has received funding from

- La Marató de TV3, Expedient number 20142910

- FIS Grant PI14/02058, PI 18/01717.

- CIBERNED (Fundación CIEN, Instituto de Salud Carlos III, Spain)

Author information

Author notes

  1. Frederic Sampedro and Juan Marín-Lahoz contributed equally to this work.

Authors and Affiliations

  1. Movement Disorders Unit, Neurology Department, Sant Pau Hospital, Mas Casanovas 90-08041, Barcelona, Spain

    Ignacio Aracil-Bolaños, Juan Marín-Lahoz, Andrea Horta-Barba, Saül Martínez-Horta, Jesús Pérez-Pérez, Helena Bejr-Kasem, Berta Pascual-Sedano, Mariángeles Botí, Antonia Campolongo, Cristina Izquierdo, Alexandre Gironell, Jaime Kulisevsky & Javier Pagonabarraga

  2. Departament de Medicina, Universitat Autònoma de Barcelona (U.A.B.), Barcelona, Spain

    Ignacio Aracil-Bolaños, Juan Marín-Lahoz, Berta Pascual-Sedano, Beatriz Gómez-Ansón, Jaime Kulisevsky & Javier Pagonabarraga

  3. Institut d’Investigacions Biomèdiques- Sant Pau (IIB-Sant Pau), Barcelona, Spain

    Ignacio Aracil-Bolaños, Frederic Sampedro, Juan Marín-Lahoz, Andrea Horta-Barba, Saül Martínez-Horta, Jesús Pérez-Pérez, Helena Bejr-Kasem, Mariángeles Botí, Antonia Campolongo, Cristina Izquierdo, Alexandre Gironell, Beatriz Gómez-Ansón, Jaime Kulisevsky & Javier Pagonabarraga

  4. Centro de Investigación en Red-Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain

    Ignacio Aracil-Bolaños, Frederic Sampedro, Juan Marín-Lahoz, Andrea Horta-Barba, Saül Martínez-Horta, Jesús Pérez-Pérez, Helena Bejr-Kasem, Berta Pascual-Sedano, Mariángeles Botí, Antonia Campolongo, Cristina Izquierdo, Alexandre Gironell, Beatriz Gómez-Ansón, Jaime Kulisevsky & Javier Pagonabarraga

  5. Neurology Department, Sant Pau Hospital, Barcelona, Spain

    José María Gónzalez-de-Echávarri

  6. Neuroradiology Unit, Sant Pau Hospital, Barcelona, Spain

    Beatriz Gómez-Ansón

Authors
  1. Ignacio Aracil-Bolaños
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  2. Frederic Sampedro
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  3. Juan Marín-Lahoz
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  4. Andrea Horta-Barba
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  5. Saül Martínez-Horta
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Contributions

Ignacio Aracil-Bolaños contributed to conception, organization and execution of the research project; designed and executed the imaging and statistical analyses and wrote the first draft.

Frederic Sampedro contributed to execution of the research project, assisted in statistical and imaging analyses and provided review and critique of the manuscript.

Juan Marín-Lahoz contributed to execution of the research project, assisted in statistical analysis and provided review and critique of the manuscript.

Andrea Horta-Barba contributed to conception and execution of the research project and provided review and critique of the manuscript.

Saül Martínez-Horta contributed to conception and execution of the research project and provided review and critique of the manuscript.

José María Gónzalez-de-Echávarri contributed to the execution of the research project and assisted in statistical and imaging analyses.

Mariángeles Botí contributed to conception and execution of the research project and provided review and critique of the manuscript.

Jesús Pérez-Pérez contributed to conception and execution of the research project and provided review and critique of the manuscript.

Helena Bejr-Kasem contributed to conception and execution of the research project and provided review and critique of the manuscript.

Berta Pascual-Sedano contributed to conception and execution of the research project and provided review and critique of the manuscript.

Antonia Campolongo contributed to organization and execution of the research project and provided review and critique of the manuscript.

Cristina Izquierdo contributed to organization and execution of the research project and provided review and critique of the manuscript.

Alexandre Gironell contributed to organization and execution of the research project and provided review and critique of the manuscript.

Beatriz Gómez-Ansón contributed to organization and execution of the research project and provided review and critique of the manuscript.

Jaime Kulisevsky contributed to conception, organization and execution of the research project and provided review and critique of the manuscript.

Javier Pagonabarraga contributed to conception, organization and execution of the research project and provided review and critique of the manuscript.

Corresponding authors

Correspondence to Jaime Kulisevsky or Javier Pagonabarraga.

Ethics declarations

All patients provided written informed consent according to the Declaration of Helsinki. The study was approved by the Ethics Comitee for Clinical Research at the Hospital de la Santa Creu i Sant Pau, Barcelona.

Conflict of interest

The work of Dr. Aracil is supported by the Spanish Neurological Society via the Movement Disorders Study Group Grant, and is employed by Hospital de la Santa Creu i Sant Pau. The work of Dr. Bejr-Kasem is supported by Instituto de Salud Carlos III, Spain and has served on advisory or speakers’ boards, and received honoraria from Zambon. Dr. Javier Pagonabarraga has served on advisory or speakers’ boards, and received honoraria from UCB, Zambon, AbbVie, Italfarmaco, Allergan, Ipsen and Bial, and received grants from CIBERNED & FIS PI14/02058) (Spanish Government grants) and Fundació La Marató de TV3 20,142,910. Dr. Kulisevsky has received research grants from CIBERNED & FIS PI15/00962 (Spanish Government grants), and Fundació La Marató de TV3 20,142,410, and consulting fees or speaker honoraria from Zambon, Roche, Abbvie, Bial, UCB and Teva. Jesus Perez-Perez is employed as a Joan Rodes researcher (Spanish Government contract) and received grants from FIS (PI17/001885). Saul Martinez-Horta, Mariángeles Boti, Andrea Horta-Barba, Frederic Sampedro, Alexandre Gironell, Antonia Campolongo, Cristina Izquierdo, José María Gónzalez-de-Echávarri and Juan Marín-Lahoz are employed by Hospital de la Santa Creu i Sant Pau and report no other conflict of interest or funding.

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Aracil-Bolaños, I., Sampedro, F., Marín-Lahoz, J. et al. Tipping the scales: how clinical assessment shapes the neural correlates of Parkinson’s disease mild cognitive impairment. Brain Imaging and Behavior 16, 761–772 (2022). https://doi.org/10.1007/s11682-021-00543-3

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