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

Rowland NC, De Hemptinne C, Swann NC, Qasim S, Miocinovic S, Ostrem JL, Knight RT, Starr PA - Front Hum Neurosci (2015)

Bottom Line: 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.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).

View Article: PubMed Central - PubMed

Affiliation: Department of Neurological Surgery, University of California, San Francisco San Francisco, CA, USA.

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.

No MeSH data available.


Related in: MedlinePlus

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, *prs < 0.05, refer to Results section for specific p-values.
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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, *prs < 0.05, refer to Results section for specific p-values.

Mentions: To study the transition between task periods, cortical beta power (all regions) was averaged 1 s before and 1 s after the appearance of the PREPARATION cue (HOLD-PREP transition) and movement onset (PREP-MOVE) for both groups. In the early movement PREPARATION period (HOLD-PREP transition), the average log beta power difference between the HOLD and PREPARATION periods decreased to a greater extent in the Parkinson's disease (−0.31±0.06) than essential tremor group (−0.071±0.05) (mean ± SE, all units = log10(μV)2/Hz, prs = 0.0061) (spectrogram data only shown in Figure 3A). In examining this transition in specific cortical locations, the stronger early preparation-related beta decrease was found in contacts overlying central sulcus (Parkinson's disease −0.34±0.05, essential tremor −0.031±0.07, prs = 0.022), postcentral sulcus (Parkinson's disease −0.44±0.13, essential tremor −0.043±0.08, prs = 0.032), and superior parietal lobule (Parkinson's disease −0.49±0.16, essential tremor −0.012±0.05, prs = 0.014) (Figure 3C). The average decrease in log beta power during the latter segment of the PREPARATION period was not significantly different between groups, nor were there disease specific differences in beta power at the prep-move transition (spectrogram data only shown in Figure 3B). Thus, the low-dopamine parkinsonian state is associated with a stronger cortical beta decrease during early movement preparation, compared with a non-parkinsonian condition.


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

Rowland NC, De Hemptinne C, Swann NC, Qasim S, Miocinovic S, Ostrem JL, Knight RT, Starr PA - Front Hum Neurosci (2015)

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, *prs < 0.05, refer to Results section for specific p-values.
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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, *prs < 0.05, refer to Results section for specific p-values.
Mentions: To study the transition between task periods, cortical beta power (all regions) was averaged 1 s before and 1 s after the appearance of the PREPARATION cue (HOLD-PREP transition) and movement onset (PREP-MOVE) for both groups. In the early movement PREPARATION period (HOLD-PREP transition), the average log beta power difference between the HOLD and PREPARATION periods decreased to a greater extent in the Parkinson's disease (−0.31±0.06) than essential tremor group (−0.071±0.05) (mean ± SE, all units = log10(μV)2/Hz, prs = 0.0061) (spectrogram data only shown in Figure 3A). In examining this transition in specific cortical locations, the stronger early preparation-related beta decrease was found in contacts overlying central sulcus (Parkinson's disease −0.34±0.05, essential tremor −0.031±0.07, prs = 0.022), postcentral sulcus (Parkinson's disease −0.44±0.13, essential tremor −0.043±0.08, prs = 0.032), and superior parietal lobule (Parkinson's disease −0.49±0.16, essential tremor −0.012±0.05, prs = 0.014) (Figure 3C). The average decrease in log beta power during the latter segment of the PREPARATION period was not significantly different between groups, nor were there disease specific differences in beta power at the prep-move transition (spectrogram data only shown in Figure 3B). Thus, the low-dopamine parkinsonian state is associated with a stronger cortical beta decrease during early movement preparation, compared with a non-parkinsonian condition.

Bottom Line: 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.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).

View Article: PubMed Central - PubMed

Affiliation: Department of Neurological Surgery, University of California, San Francisco San Francisco, CA, USA.

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.

No MeSH data available.


Related in: MedlinePlus