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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

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.
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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.

Mentions: ECoG data were collected with patients quietly resting with their eyes open for 1–2 min (denoted as REST period) in addition to a movement task consisting of a hold period (HOLD), a movement preparation period (PREPARATION) and a movement execution period (MOVE) (schematic in Figure 1A). The task was displayed on a 16-gigabyte iPad device (Apple Inc., Cupertino, CA) secured into a customized flat screen holder facing the patient and attached to the surgical bed. Prior to initiating task recordings, patients practiced several trials of the task. The initial display of the task consisted of a filled red circle present in the center of the screen for 5 s (HOLD). This was followed by the appearance of a filled blue circle either above or below the red dot (PREPARATION). After 3–5 s with both circles on the screen, the red circle became green in color, indicating the MOVE period, during which the patient lifted their forearm from a button resting in their lap and touched the screen at the location of the blue circle. After successful contact with the screen at this location, the blue circle continued to cycle above and below the green circle 6–8 times. The patient was instructed to touch the blue dot at each new location while it was cycling. To end the trial, the red circle again appeared alone on the screen, prompting the patient to return their forearm to the resting position. The number of presentations of the blue dot was chosen so that the duration of the MOVE period would be similar to the duration of the other periods. During a single presentation of the dot in the MOVE period, if no touch was detected after 2–5 s (adjusted individually for the subject based on movement speed), the blue circle would cycle automatically to the other position. The interval between two consecutive appearances of the red circle constituted a single trial. The diameter of the blue circle was adjusted between 1 and 3 cm prior to the beginning of the recording based on patient visual acuity and line of sight. Patients completed up to 20 trials per session.


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)

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.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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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.
Mentions: ECoG data were collected with patients quietly resting with their eyes open for 1–2 min (denoted as REST period) in addition to a movement task consisting of a hold period (HOLD), a movement preparation period (PREPARATION) and a movement execution period (MOVE) (schematic in Figure 1A). The task was displayed on a 16-gigabyte iPad device (Apple Inc., Cupertino, CA) secured into a customized flat screen holder facing the patient and attached to the surgical bed. Prior to initiating task recordings, patients practiced several trials of the task. The initial display of the task consisted of a filled red circle present in the center of the screen for 5 s (HOLD). This was followed by the appearance of a filled blue circle either above or below the red dot (PREPARATION). After 3–5 s with both circles on the screen, the red circle became green in color, indicating the MOVE period, during which the patient lifted their forearm from a button resting in their lap and touched the screen at the location of the blue circle. After successful contact with the screen at this location, the blue circle continued to cycle above and below the green circle 6–8 times. The patient was instructed to touch the blue dot at each new location while it was cycling. To end the trial, the red circle again appeared alone on the screen, prompting the patient to return their forearm to the resting position. The number of presentations of the blue dot was chosen so that the duration of the MOVE period would be similar to the duration of the other periods. During a single presentation of the dot in the MOVE period, if no touch was detected after 2–5 s (adjusted individually for the subject based on movement speed), the blue circle would cycle automatically to the other position. The interval between two consecutive appearances of the red circle constituted a single trial. The diameter of the blue circle was adjusted between 1 and 3 cm prior to the beginning of the recording based on patient visual acuity and line of sight. Patients completed up to 20 trials per session.

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