White Matter Microstructural Underpinnings of Mild Behavioral Impairment in Parkinson's Disease

Author:

Monchi Oury1234ORCID,Pinilla‐Monsalve Gabriel D.12ORCID,Almgren Hannes34,Ghahremani Maryam35,Kibreab Mekale34,Maarouf Nadia34,Kathol Iris34,Boré Arnaud6,Rheault François6,Descoteaux Maxime6,Ismail Zahinoor35

Affiliation:

1. Centre de recherche de l'Institut universitaire de gériatrie de Montréal Montreal Quebec Canada

2. Département de radiologie, radio‐oncologie et médicine nucléaire Université de Montréal Montreal Quebec Canada

3. Hotchkiss Brain Institute University of Calgary Calgary Alberta Canada

4. Department of Clinical Neurosciences University of Calgary Calgary Alberta Canada

5. Departments of Psychiatry and Community Health Sciences University of Calgary Calgary Alberta Canada

6. Département d'informatique Université de Sherbrooke Sherbrooke Quebec Canada

Abstract

AbstractBackgroundPatients with Parkinson's disease (PD) experience changes in behavior, personality, and cognition that can manifest even in the initial stages of the disease. Previous studies have suggested that mild behavioral impairment (MBI) should be considered an early marker of cognitive decline. However, the precise neurostructural underpinnings of MBI in early‐ to mid‐stage PD remain poorly understood.ObjectiveThe aim was to explore the changes in white matter microstructure linked to MBI and mild cognitive impairment (MCI) in early‐ to mid‐stage PD using diffusion magnetic resonance imaging (dMRI).MethodsA total of 91 PD patients and 36 healthy participants were recruited and underwent anatomical MRI and dMRI, a comprehensive neuropsychological battery, and the completion of the Mild Behavioral Impairment‐Checklist. Metrics of white matter integrity included tissue fractional anisotropy (FAt) and radial diffusivity (RDt), free water (FW), and fixel‐based apparent fiber density (AFD).ResultsThe connection between the left amygdala and the putamen was disrupted when comparing PD patients with MBI (PD‐MBI) to PD‐non‐MBI, as evidenced by increased RDt (η2 = 0.09, P = 0.004) and both decreased AFD (η2 = 0.05, P = 0.048) and FAt (η2 = 0.12, P = 0.014). Compared to controls, PD patients with both MBI and MCI demonstrated increased FW for the connection between the left orbitofrontal gyrus (OrG) and the hippocampus (η2 = 0.22, P = 0.008), augmented RDt between the right OrG and the amygdala (η2 = 0.14, P = 0.008), and increased RDt (η2 = 0.25, P = 0.028) with decreased AFD (η2 = 0.10, P = 0.046) between the right OrG and the caudate nucleus.ConclusionMBI is associated with abnormal microstructure of connections involving the orbitofrontal cortex, putamen, and amygdala. To our knowledge, this is the first assessment of the white matter microstructure in PD‐MBI using dMRI. © 2024 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Funder

Institute of Neurosciences, Mental Health and Addiction

Université de Montréal

Publisher

Wiley

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