Task-related activity in sensorimotor cortex in Parkinson's disease and essential tremor: changes in beta and gamma bands

Abstract

In Parkinson's disease patients in the OFF medication state, basal ganglia local field potentials exhibit changes in beta and gamma oscillations that correlate with reduced voluntary movement, manifested as rigidity and akinesia. However, magnetoencephalography and low-resolution electrocorticography (ECoG) studies in Parkinson's patients suggest that changes in sensorimotor cortical oscillations differ from those of the basal ganglia. To more clearly define the role of sensorimotor cortex oscillatory activity in Parkinson's, we performed intraoperative, high-resolution (4 mm spacing) ECoG recordings in 10 Parkinson's patients (2 females, ages 47-72) undergoing deep brain stimulation (DBS) lead placement in the awake, OFF medication state. We analyzed ECoG potentials during a computer-controlled reaching task designed to separate movement preparation from movement execution and compared findings to similar invasive recordings in eight patients with essential tremor (3 females, ages 59-78), a condition not associated with rigidity or akinesia. We show that (1) cortical beta spectral power at rest does not differ between Parkinson's and essential tremor patients (p = 0.85), (2) early motor preparation in Parkinson's patients in the OFF medication state is associated with a larger beta desynchronization compared to patients with essential tremor (p = 0.0061), and (3) cortical broadband gamma power is elevated in Parkinson's patients compared to essential tremor patients during both rest and task recordings (p = 0.004). Our findings suggest an oscillatory profile in sensorimotor cortex of Parkinson's patients that, in contrast to the basal ganglia, may act to promote movement to oppose the anti-kinetic bias of the dopamine-depleted state.

Keywords: Parkinson's disease; beta frequency; deep brain stimulation; electrocorticography; essential tremor; ipad; oscillations.

Figure 1

Behavioral task, contact localization, examples of raw data recording, and spectral analysis. (A) Schematic of the reaching task. See Materials and Methods for detailed description. (B) Electrode positions relative to the brain anatomy of a single subject. The cortical surface was reconstructed offline using the preoperative MRI (Statistical Parametric Mapping 8, SPM8). Electrode coordinates (in relation to the midpoint of the line adjoining the anterior and posterior commissures) were then determined by co-registering the preoperative MRI and intraoperative CT scan and mapped onto the cortical surface. (C) A 30-s simultaneous recording of ECoG data (from precentral gyrus), accelerometer position, EMG potential, and button tracing from a single Parkinson's subject. The time scale beneath the button recording indicates 5 s. The recordings are shown in relation to the timing of the HOLD, PREPARATION, and MOVE periods during two trials. Accel, accelerometer; m, milli; sec, second; μ, micro; V, volt. (D) Power spectral density for the HOLD, PREPARATION and MOVE periods are superimposed [average of 20 trials, same subject as (C). The PSD curve for the REST period for this subject is nearly indistinguishable from the HOLD PSD curve and is not shown. Gray shaded areas indicate boundaries of the beta (13–30 Hz) and broadband gamma (70–200 Hz) frequency bands. (E) Spectrograms for task transitions, same ECoG data as depicted in (C). Hashed marks indicate the frequency bands (beta: 13–30 Hz and broadband gamma: 70–200 Hz) and intervals (1 s before and after the appearance of the blue filled circle and movement onset for the HOLD-PREP and PREP-MOVE transitions, respectively) over which spectrogram data are shown for comparison.

Figure 2

Beta and gamma spectral power at REST and during different task periods. (A) Comparison of average log₁₀ beta power between Parkinson's disease (n = 10 subjects) and essential tremor (n = 8 subjects) groups for the REST and task periods. Horizontal line within the boxplot indicates median value, lower and upper box limits indicate the interquartile range (25 and 75%, respectively) and whiskers extend to minimum and maximum values of the dataset. Filled dark circles indicate outliers. No differences were found for any period. ET, essential tremor; PD, Parkinson's disease. (B) Comparison of average log₁₀ broadband gamma power between Parkinson's disease (n = 10 subjects) and essential tremor (n = 8 subjects) groups for the REST and task periods. Boxplots constructed as in (A). ^*p_rs < 0.05, ^**p_rs < 0.01, refer to Results section for specific p-values. ET, essential tremor; PD, Parkinson's disease. (C) Cortical topography of the broadband gamma frequency band differences between Parkinson's disease and essential tremor groups, illustrated here for the MOVE period. Boxplots constructed as in (A). Values in parentheses indicate number of patients with contact coverage of a particular cortical region. CenSul, central sulcus; ET, essential tremor; PD, Parkinson's disease; PoCeGy, postcentral gyrus; PoCeSu, postcentral sulcus; PrCeGy, precentral gyrus; PrCeSu, precentral sulcus; SuFrGy, superior frontal gyrus; SuPaLo, Superior parietal lobule; ^*p_rs < 0.05, refer to Results section for specific p-values.

Figure 3

Movement-related transitions in beta and gamma power. (A,B) Average spectrograms during the HOLD-PREP and PREP-MOVE transitions for the Parkinson's disease (n = 10 subjects) and essential tremor (n = 8 subjects) groups. Hashed marks as in Figure 1E. Note that no calculations were performed on the spectrogram data. (C) Cortical topography of the beta band decrease during the early HOLD-PREP transition (i.e., comparison of difference in log PSD values in both groups). Values in parentheses indicate number of patients with contact coverage of a particular cortical region. Boxplot construction is the same as in Figure 2A. CenSul, central sulcus; ET, essential tremor; PD, Parkinson's disease; PoCeGy, postcentral gyrus; PoCeSu, postcentral sulcus; PrCeGy, precentral gyrus; PrCeSu, precentral sulcus; SuFrGy, superior frontal gyrus; SuPaLo, Superior parietal lobule, ^*p_rs < 0.05, refer to Results section for specific p-values.