Transient and state modulation of beta power in human subthalamic nucleus during speech production and finger movement

Abstract

Signs of Parkinson's disease (PD) are augmented by speech and repetitive motor tasks. The neurophysiological basis for this phenomenon is unknown, but may involve augmentation of β (13-30 Hz) oscillations within the subthalamic nucleus (STN). We hypothesized that speech and motor tasks increase β power in STN and propose a mechanism for clinical observations of worsening motor state during such behaviors. Subjects undergoing deep brain stimulation (DBS) surgery performed tasks while STN local field potential (LFP) data were collected. Power in the β frequency range was analyzed across the entire recording to observe slow shifts related to block design and during time epochs synchronized to behavior to evaluate immediate fluctuations related to task execution. Bilaterally symmetric β event related desynchronization was observed in analysis time-locked to subject motor and speech tasks. We also observed slow shifts of β power associated with blocks of tasks. Repetitive combined speech and motor, and isolated motor blocks were associated with the highest bilateral β power state. Overt speech alone and imagined speech were associated with a low bilateral β power state. Thus, changing behavioral tasks is associated with bilateral switching of β power states. This offers a potential neurophysiologic correlate of worsened PD motor signs experienced during clinical examination with provocative tasks: switching into a high β power state may be responsible for worsening motor states in PD patients when performing unilateral repetitive motor tasks and combined speech and motor tasks. Beta state changes could be chronically measured and potentially used to control closed loop neuromodulatory devices in the future.

Copyright © 2011 IBRO. Published by Elsevier Ltd. All rights reserved.

Figures

Figure 1

Schematic representation of recording electrodes used for LFP recordings. A: Medtronic 3389 DBS lead (reprinted with the permission of Medtronic, Inc © 2008). B: Alpha Omega Neuroprobe microelectrode. Recordings were obtained from the labeled reference contact (reprinted with the permission of Alpha Omega Co. USA © 2011).

Figure 2

Collage demonstrating LFP spectral power changes seen for all overt speech tasks (with and without button press are combined). Upper panel, from recording 1 (see table 2) with paired mER electrode design. A: Power spectral density (PSD) plot for entire recording (All), Speech (1000ms epoch), and pre-Speech baseline (1000ms epoch). Note the depression of PSD in the β band with speech. Also, β power is augmented in the immediate pre-speech period (baseline) relative to the entire recording session. B: Frequency-time representation of PSD for speech onset (left panel, time 0) and speech offset (right panel, time 0). Again, note depression of β band power with speech. C: Averaged β band power over speech trials, synchronized to speech onset (time 0, left panel) and speech offset (time 0, right panel), overlaid on averaged audio track (grey). Red emphasis indicated region that was significant on bootstrap permutation test (BS*). D: Atlas representation demonstrating paired mER recording electrodes (red) in dorsal STN (yellow). Sagittal atlas, lateral 11mm, adopted from Fig 4.31 in (Morel, 2007) with permission. Lower panel, from recording 10 with DBS lead design. E: Similar PSD plot demonstrating β power depression with speech and augmentation of β in the pre-speech baseline period. F: Frequency-Time representation. G: β band power with speech onset and offset. H: Atlas representation demonstrating DBS lead design. Sagittal atlas, lateral 10mm, adopted from Fig 4.30 in (Morel, 2007) with permission. For B, C, F, G, data was baselined to adjust the mean power in 1000ms period before the behavioral cue to zero. For B, F, data was Z-scored and baselined to adjust the mean power in 1000ms period before the behavioral cue to zero; blue and red represent negative and positive relative change, respectively, to baseline.

Figure 3

Power spectral density (PSD) modulation with either speech alone (right panel) or speech plus button press (left panel) from a single subject (recording 10). A, E: Frequency-Time representation for left STN. B, F: Right STN. C, G: averaged patient response activity for audio channel (upper trace) and EMG (lower trace). Note the strong EMG response for button press preceding speech onset for the combined task, but no EMG activity during the speech-only task. D, H: PSD plots for each condition. This demonstrates an increase of pre-speech (1000ms epoch) β power for the speech plus button press tasks (left panel), but no such increase of pre-speech β power for speech-only tasks (right panel), suggesting a unique β state. A, B, C were recorded synchronously, and E, F, G were recorded synchronously. For speech plus button press tasks, 50% of trials were left-handed button press, 50% right handed. For A, B, E, F, data was Z-scored and baselined to adjust the mean power in 1000ms period before the behavioral cue to zero; blue and red represent negative and positive relative change, respectively, to baseline.

Figure 4

Power spectral density (PSD) modulation with button press. A, B: Frequency-Time representation of STN LFP recorded synchronously for left button press. C: β power modulation from left and right STN overlaid on average EMG activity (grey). D, E: Frequency-Time representation of STN LFP recorded synchronously for right button press. F: β power modulation from left and right STN overlaid on average EMG activity (grey). Note the bilateral symmetry in LFP modulation for left and right button press in left and right STN. Data from recording 10. A, B, C were recorded synchronously, and D, E, F were recorded synchronously. Data was baselined to adjust the mean power in 1000ms period before the behavioral cue to zero. For A, B, D, E, blue and red represent negative and positive relative change, respectively, to baseline.

Figure 5

Comparison of β suppression with speech alone versus speech plus button press across recordings. A: For recording 8, β depression with speech alone (orange) and speech plus button press (blue). Overlaid on averaged audio channel data. This composite is formed from appending speech onset and offset matrices (see text and Figure 2). Dotted horizontal red and blue lines indicate the average β power for the final 3000ms of speech, chosen to prevent direct influence of button press-related β rebound on the mean value. Data was baselined to adjust the mean power in 1000ms period before the behavioral cue to zero. B: Mean β suppression for last 3000ms of speech across all recordings and for all recordings combined. For this analysis, the entire length of the recording was z-scored (within-subject) using the overall mean and standard deviation of the log transformed β power. Group difference is significant (−2.8 versus −2.1 log units, p=0.02, 2-tailed t-test). C: Mean β suppression for last 3000ms of speech across all recordings combined. For this analysis, the recording was z-scored within each block of tasks (set of 15 repetitive tasks). This within-subject/within-task normalization reduced the effect size of the added button press on β suppression in the final 3000ms of speech (−3.1 versus −2.9 log units, p=0.60, 2-tailed t-test).

Figure 6

Slow β state changes across blocks of tasks for 30-minute recordings in simultaneous right and left STN recordings for subject 6. These results demonstrate that β power is correlated across bilateral STN and varies with the type of behavioral task. Task blocks of 15 repetitive tasks are color coded. A, B: Plot of smoothed time vector of instantaneous β power (Black, low-pass cutoff frequency 0.04Hz) for left and right STN recordings. The highlighted region is expanded in Figure 7. C: Bar graph representation of average β power within each task group for two subjects with bilateral simultaneous STN recording and silent speech trials (subjects 6 and 7). Average β power for entire task period (cue-to-cue) as well as specifically for pre-cue baseline period (1000ms) are presented. D: Bar graph representation of β power for all subjects for common tasks. The unilateral repetitive motor task produced the greatest β state in bilateral STN. Both the overt speech alone and the silent speech alone tasks yield low β states. Combined tasks created an intermediate β state. There is general agreement between β power in the entire task period (cue-to-cue) and for the pre-cue baseline period with the exception of the combined speech + motor task, which has a high pre-cue baseline average β power but intermediate power for entire task period. ** denotes statistical significant difference from all other tasks (p

Figure 7

Transient and state modulation of β power over three distinct task blocks. Upper panel demonstrates slow, state modulation of β power over a time scale of minutes, shifting from a relatively low β state (speech only, light blue), to a high β state (motor only, green), then to an intermediate β state (speech + motor, dark blue). Each colored block is expanded in a lower panel to demonstrate transient modulation of β on a task-by-task level on the time scale of seconds/milliseconds. Dotted black line represents the mean β power in that panel. Numerical value on the dotted line represents the mean beta power in arbitrary units. The baseline for audio and EMG data serves as a reference marker for the mean β power in the upper panel. The region of data presented here is highlighted in the upper panel of Figure 6.