Frontal theta and beta oscillations during lower-limb movement in Parkinson's disease

Abstract

Objectives: Patients with Parkinson's disease (PD) have deficits in lower-limb functions such as gait, which involves both cognitive and motor dysfunction. In PD, theta and beta brain rhythms are associated with cognitive and motor functions, respectively. We tested the hypothesis that PD patients with lower-limb abnormalities would exhibit abnormal theta and beta rhythms in the mid-frontal cortical region during lower-limb action.

Methods: This study included thirty-nine participants; 13 PD patients with FOG (PDFOG+), 13 without FOG (PDFOG-), and 13 demographically-matched controls. We recorded scalp electroencephalograms (EEG) during a lower-limb pedaling motor task, which required intentional initiation and stopping of a motor movement.

Results: FOG scores were correlated with disease severity and cognition. PDFOG+ patients pedaled with reduced speed and decreased acceleration compared to PDFOG- patients and controls. PDFOG+ patients exhibited attenuated theta-band (4-8 Hz) power and increased beta-band (13-30 Hz) power at mid-frontal electrode Cz during pedaling. Frontal theta- and beta-band oscillations also correlated with motor and cognitive deficits.

Conclusion: Frontal theta and beta oscillations are predictors of lower-limb motor symptoms in PD and could be used to design neuromodulation for PD-related lower-limb abnormalities.

Significance: These data provide insight into mechanisms of lower-limb dysfunction in PD with FOG.

Keywords: Freezing of gait; Frontal region; Lower-limb movement; Oscillations; Parkinson’s disease.

Fig. 1.

Experimental design, accelerometer signals, and relationship between FOG and motor /cognitive characteristics of PD. (A) In this task, a black “warning” cue appeared to alert the subject to pay attention. Within 1000–2000 ms, a green GO cue instructed subject to complete one rotation of the pedals. (B) Accelerometer signals were collected from tri-axial accelerometer and segmented from the GO-cue (−500 to 2500 ms) and averaged to plot the mean trace of X-, Y-, and Z-axes, in control, PDFOG−, and PDFOG+ participants. (C) FOG questionnaire scores as a measurement of lower-extremity impairment showed a significant positive correlation with UPDRS III scores and a significant negative correlation with MOCA scores (left side and middle). Correlation analysis showed a significant correlation between disease duration (DD) and FOG (right side), but not DD and MOCA scores. *p<0.05; **p<0.01. rho = correlation coefficients; FOG: Freezing of Gait; PDFOG−: PD patients without FOG; PDFOG+: PD patients with FOG. UPDRS III: motor Unified Parkinson’s Disease Rating Scale; MOCA: Montreal Cognitive Assessment.

Fig. 2.

Pedaling kinematics. (A) Box plots show that mean pedaling linear speed was the lowest in PDFOG+, and significantly correlated with FOG scores, and UPDRS III scores, but not with MOCA scores. (B) Box plots also show that PDFOG+ patients took the most time to reach maximum acceleration (peak time) during the pedaling task, and a significant correlation was found between peak time and UPDRS III scores only, but not FOG scores and MOCA scores. *p<0.05 vs control subjects; **p<0.01 vs control subjects; **Significance correlation level <0.01. Effect size was symbolized by partial eta-squared (η_p²). rho = correlation coefficients; FOG: Freezing of Gait; UPDRS III: motor Unified Parkinson’s Disease Rating Scale; MOCA: Montreal Cognitive Assessment. PDFOG+: PD patients with FOG; PDFOG−: PD patients without FOG.

Fig. 3.

FOG is associated with attenuated theta-band and amplified beta-band power in PD. (A-B) Time-frequency analysis showed reduced theta and amplified beta power at frontal scalp electrode (vertex or “Cz”) during pedaling task in PDFOG+ patients as compared to PDFOG− patients and control subjects. PDFOG− patients showed low theta power and high beta power compared to control subjects. (C) Box plots displayed the power values from two tf-ROIs (theta and beta power values at 0–400 ms and 0–2000 ms time windows) during pedaling task. (E-F) Topography plots (PDFOG+ patients versus controls and PDFOG+ patients versus PDFOG− patients) indicated reduced theta and increased beta activity at the frontal region in PDFOG+ patients. B: Permutation-corrected p<0.05 outlined in bold lines. *p<0.05 vs control subjects; **p<0.01 vs control subjects; ⁺p<0.05 vs PDFOG−; Effect size was symbolized by partial eta-squared (η_p²); diamonds show significant electrodes in E and F. FOG: Freezing of Gait; PDFOG+: PD patients with FOG; PDFOG−: PD patients without FOG.

Fig. 4.

Correlation analysis between power values of theta and beta-band during motor initiation and motor and cognitive characteristics in PD. (A) A significant correlation was seen between theta power values and FOG scores, a trend was seen between theta power values and MOCA scores, but not between theta power and UPDRS III scores. (B) A significant correlation was observed between beta power values and FOG scores and UPDRS III scores, but not between beta power and MOCA scores. *Significance correlation level =<0.05; **Significance correlation level <0.01. rho = correlation coefficients; FOG: Freezing of Gait; UPDRS III: motor Unified Parkinson’s Disease Rating Scale; MOCA: Montreal Cognitive Assessment. All power within tf-ROIs of 0–400 ms.