Subthalamic Beta Activity in Parkinson's Disease May Be Linked to Dorsal Striatum Gray Matter Volume and Prefrontal Cortical Thickness: A Pilot Study

Florencia Sanmartino; Álvaro J Cruz-Gómez; Raúl Rashid-López; Elena Lozano-Soto; Fernando López-Sosa; Amaya Zuazo; Jesús Riqué-Dormido; Raúl Espinosa-Rosso; Javier J González-Rosa

doi:10.3389/fneur.2022.799696

Subthalamic Beta Activity in Parkinson's Disease May Be Linked to Dorsal Striatum Gray Matter Volume and Prefrontal Cortical Thickness: A Pilot Study

Front Neurol. 2022 Mar 23:13:799696. doi: 10.3389/fneur.2022.799696. eCollection 2022.

Authors

Florencia Sanmartino^{1

2}, Álvaro J Cruz-Gómez^{1

2}, Raúl Rashid-López^{2

3}, Elena Lozano-Soto^{1

2}, Fernando López-Sosa², Amaya Zuazo⁴, Jesús Riqué-Dormido⁵, Raúl Espinosa-Rosso^{2

3

6}, Javier J González-Rosa^{1

2}

Affiliations

¹ Department of Psychology, University of Cadiz, Cádiz, Spain.
² Psychophysiology and Neuroimaging Group, Institute of Biomedical Research Cadiz (INiBICA), Cádiz, Spain.
³ Department of Neurology, Puerta del Mar University Hospital, Cádiz, Spain.
⁴ Department of Radiodiagnostic and Medical Imaging, Puerta del Mar University Hospital, Cádiz, Spain.
⁵ Department of Neurosurgery, Puerta del Mar University Hospital, Cádiz, Spain.
⁶ Department of Neurology, Jerez de la Frontera University Hospital, Jerez de la Frontera, Spain.

Abstract

Background: Excessive oscillations at beta frequencies (13-35 Hz) in the subthalamic nucleus (STN) represent a pathophysiological hallmark of Parkinson's disease (PD), which correlates well with parkinsonian symptoms and is reduced in response to standard disease treatments. However, the association of disease-specific regional gray matter (GM) atrophy or cortical thickness (CT) with the presence of STN beta oscillatory activity has been poorly investigated but is of relevance given the potential of these variables for extracting information about PD pathophysiology. This exploratory study investigated the involvement of regional GM volume and CT in the basal ganglia-cortical network and its potential association with the presence of STN beta oscillatory activity in PD.

Methods: We acquired preoperative GM densities on T1-weighted magnetic resonance imaging scans and we carried out regional estimation of GM volume and CT. LFP activities from the STN were recorded post-operatively in 7 cognitively preserved PD patients off dopaminergic medication undergoing deep-brain stimulation surgery. Oscillatory beta power was determined by power spectral density of 4-min resting state STN LFP activity. Spearman partial correlations and regression analysis were used to screen the presence of STN beta power for their relationship with GM volume and CT measurements.

Results: After controlling for the effects of age, educational level, and disease duration, and after correcting for multiple testing, enhanced STN beta power showed significant and negative correlations between, first, volume of the right putamen and left caudate nucleus, and second, smaller CT in frontal regions involving the left rostral middle frontal gyrus (MFG) and left medial orbitofrontal gyrus. A lower volume in the right putamen and a lower CT in the left MFG demonstrated the strongest associations with increased STN beta power.

Conclusions: These tentative results seem to suggest that STN LFP beta frequencies may be mainly linked to different but ongoing parallel neurodegenerative processes, on the one hand, to GM volume reduction in dorsal striatum, and on the other hand, to CT reduction of prefrontal-"associative" regions. These findings could further delineate the brain structural interactions underpinning the exaggerated STN beta activity commonly observed in PD patients.

Keywords: Parkinson's disease; beta oscillations; cortical thickness; gray matter volume; local field potentials; subthalamic nucleus.