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Research Articles, Behavioral/Cognitive

Subthalamic Nucleus and Sensorimotor Cortex Activity During Speech Production

Anna Chrabaszcz, Wolf-Julian Neumann, Otilia Stretcu, Witold J. Lipski, Alan Bush, Christina A. Dastolfo-Hromack, Dengyu Wang, Donald J. Crammond, Susan Shaiman, Michael W. Dickey, Lori L. Holt, Robert S. Turner, Julie A. Fiez and R. Mark Richardson
Journal of Neuroscience 3 April 2019, 39 (14) 2698-2708; https://doi.org/10.1523/JNEUROSCI.2842-18.2019
Anna Chrabaszcz
1Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15213,
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Wolf-Julian Neumann
2Movement Disorder and Neuromodulation Unit, Department of Neurology, Campus Mitte, Charité, Universitätsmedizin Berlin, Berlin, Germany 10117,
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Otilia Stretcu
3Machine Learning Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213,
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Witold J. Lipski
4Brain Modulation Laboratory, Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
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Alan Bush
4Brain Modulation Laboratory, Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
5Department of Physics, FCEN, University of Buenos Aires and IFIBA-CONICET, Buenos Aires, Argentina 1428,
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Christina A. Dastolfo-Hromack
4Brain Modulation Laboratory, Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
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Dengyu Wang
4Brain Modulation Laboratory, Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
6School of Medicine, Tsinghua University, Beijing, China 100084,
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Donald J. Crammond
4Brain Modulation Laboratory, Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
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Susan Shaiman
7Department of Communication Science and Disorders, University of Pittsburgh, Pittsburgh, Pennsylvania 15213,
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Michael W. Dickey
7Department of Communication Science and Disorders, University of Pittsburgh, Pittsburgh, Pennsylvania 15213,
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Lori L. Holt
8Department of Psychology, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213,
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Robert S. Turner
9Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213, and
10University of Pittsburgh Brain Institute, Pittsburgh, Pennsylvania 15213
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Julie A. Fiez
1Department of Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15213,
7Department of Communication Science and Disorders, University of Pittsburgh, Pittsburgh, Pennsylvania 15213,
10University of Pittsburgh Brain Institute, Pittsburgh, Pennsylvania 15213
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R. Mark Richardson
4Brain Modulation Laboratory, Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213,
9Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15213, and
10University of Pittsburgh Brain Institute, Pittsburgh, Pennsylvania 15213
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    Figure 1.

    Experimental paradigm. ITI, Intertrial interval; ISI, interstimulus interval.

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    Figure 2.

    Location of recording sites in the MNI-defined space. A, Example trajectory of the DBS lead through the left STN shown on the DISTAL atlas by Ewert et al. (2018). B, MNI-defined coordinates (in millimeters) of recording sites in the STN plotted for all subjects in 3D space. C, Reconstructed locations of all ECoG electrodes in the sensorimotor cortex that were included in the study (n = 125), coregistered, and plotted on the cortical surface of the MNI brain space. D, MNI-defined coordinates (in millimeters) of the ECoG contacts on the sensorimotor cortex plotted for all subjects in 3D space. In B and D, each subject's electrodes are mapped with a different color.

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    Figure 3.

    STN and sensorimotor cortex (SMC) show speech-production-related time–frequency modulations. A, B, Grand average of STN (A) and SMC (B) oscillatory activity (average z-scored spectral power) across all recording sites and all trials aligned to vowel onset (time = 0 s, gray dashed vertical line). Significant modulations compared with baseline are marked in red contour (Wilcoxon's signed-rank test, p < 0.05, FDR corrected). Average speech production onsets and offsets are marked with gray dotted vertical lines. Rectangles with gray solid lines mark the time window (±500 ms from vowel onset) for the analysis of speech production-related high-gamma (60–150 Hz) activity. C, D, z-scored high-gamma (60–150 Hz) power averaged for the 1 s time window (±500 ms from vowel onset) plotted in 3D space for each subject's STN (C) and SMC (D) recording site. The location of recoding sites is provided in MNI coordinates.

  • Figure 4.
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    Figure 4.

    Spatial distribution of tongue- and lip-preferred articulatory activity in the MNI-defined STN space and sensorimotor cortex (SMC). A, C, Outcome of a series of t tests comparing z-scored high-gamma power (averaged for a 500-ms-long time window before vowel onset) during articulation of tongue consonants versus lip consonants for each STN (A) and SMC (C) recording site. Opacity of the circles varies with the magnitude of the t-value: negative t-values (in blue shades) suggest a greater response to tongue; positive t-values (in red shades) suggest a greater response to lips (Welch's two-sample t test, p < 0.05). Note that the obtained t-values for the SMC sites differed significantly along the ventral–dorsal and lateral–medial axes (Spearman's rank-order correlation test, p < 0.01), suggesting articulator-discriminative somatotopy. Circles with black outline mark representative sites for tongue and lips, the articulatory activity of which is plotted on the right. B, D, Examples of representative tongue-preferred and lips-preferred sites for STN (B) and SMC (D). A subtraction time–frequency representation is shown for the tongue-preferred site after time–frequency representation for all trials with lip consonants is subtracted from time–frequency representation for all trials with tongue consonants (i) and for the lip-preferred site after time–frequency representation for all trials with tongue consonants is subtracted from time–frequency representation for all trials with lip consonants (iii). Gray-filled contours mark significant time–frequency differences between the two conditions (Wilcoxon's rank-sum test, p < 0.05, FDR corrected). Rectangles with gray solid lines mark the time window (from 500 ms before vowel onset until vowel onset) for the analysis of articulator-specific high-gamma (60–150 Hz) activity. Differences in averaged z-scored high-gamma power elicited by trials with the tongue articulation versus the lip articulation are shown for tongue-specific (ii) and lip-specific (iv) sites (significant differences are marked with asterisks, Welch's two-sample t test, p < 0.05). Gray bands mark the time window (from 500 ms before vowel onset until vowel onset) across which high-gamma power was averaged for the analysis of articulator-specific activity. Throughout i–iv, gray dashed vertical line represents vowel onset (time = 0 s). Dotted vertical lines represent spoken response onsets and offsets for trials with tongue consonants (blue) and trials with lip consonants (red).

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    Figure 5.

    Time course of the articulatory encoding at articulator-discriminative recording sites in the STN and sensorimotor cortex (SMC). A, B, Average high-gamma activity at the STN (A) and SMC (B) articulator-responsive recording sites for trials with word-initial tongue (coronal) and word-initial lip (labial) consonants. C, Number of articulator-responsive electrodes in the STN (a total of 23%) and SMC (a total of 30%) broken down by articulator type. D, Distribution of the effect sizes (Hedges' g) quantifying the difference in average z-scored high-gamma power between trials with word-initial coronal and word-initial labial consonants at each time point of the STN and SMC recordings. Throughout A, B, and D, gray dashed vertical lines represent vowel onset (time = 0 s) and dotted vertical lines represent consonant onset.

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    Table 1.

    Subject demographic and clinical characteristics

    SubjectGenderAgeHandednessEducation, yDuration of disease, yHoehn and Yahr stageUPDRS score (off medication)
    1Male71Not recordedNot recorded6235
    2Male60Right1214253
    3Male69Right149246
    4Male61Right165231
    5Male68Left168250
    6Male57Not recordedNot recorded7244
    7Male82Right168236
    8Male66Right197245
    9Female71Right168224
    10Male77Right1810227
    11Male60Right136239
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    Table 2.

    Subject recording and behavioral performance characteristics

    SubjectCortical recordingNo. of cortical electrode contactsSTN recordingNo. of STN electrode contactsRejected trials, %Mean no. of included trials per sessionSpoken response latency (SD), sSpoken response duration (SD), s
    1Yes6Yes634.2661.60 (0.40)0.59 (0.13)
    2Yes28Not usedNot used20.892.51.70 (0.60)0.77 (0.20)
    3Yes6Yes124.51101.18 (0.50)0.52 (0.09)
    4Yes54Yes64.2110.51.12 (0.38)0.65 (0.14)
    5Yes28Yes64.6103.50.70 (0.12)0.62 (0.17)
    6Yes6Yes65110.51.27 (0.43)0.46 (0.11)
    7Not usedNot usedYes922.359.32.62 (1.83)0.43 (0.08)
    8Yes28Yes122.11140.85 (0.33)0.63 (0.13)
    9Yes6Yes68.691.671.12 (0.49)0.97 (0.36)
    10Not usedNot usedYes412.775.51.21 (0.43)0.54 (0.10)
    11Yes36Yes127.1105.30.99 (0.65)0.43 (0.11)
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The Journal of Neuroscience: 39 (14)
Journal of Neuroscience
Vol. 39, Issue 14
3 Apr 2019
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Subthalamic Nucleus and Sensorimotor Cortex Activity During Speech Production
Anna Chrabaszcz, Wolf-Julian Neumann, Otilia Stretcu, Witold J. Lipski, Alan Bush, Christina A. Dastolfo-Hromack, Dengyu Wang, Donald J. Crammond, Susan Shaiman, Michael W. Dickey, Lori L. Holt, Robert S. Turner, Julie A. Fiez, R. Mark Richardson
Journal of Neuroscience 3 April 2019, 39 (14) 2698-2708; DOI: 10.1523/JNEUROSCI.2842-18.2019

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Subthalamic Nucleus and Sensorimotor Cortex Activity During Speech Production
Anna Chrabaszcz, Wolf-Julian Neumann, Otilia Stretcu, Witold J. Lipski, Alan Bush, Christina A. Dastolfo-Hromack, Dengyu Wang, Donald J. Crammond, Susan Shaiman, Michael W. Dickey, Lori L. Holt, Robert S. Turner, Julie A. Fiez, R. Mark Richardson
Journal of Neuroscience 3 April 2019, 39 (14) 2698-2708; DOI: 10.1523/JNEUROSCI.2842-18.2019
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Keywords

  • deep brain stimulation
  • electrocorticography
  • Parkinson's disease
  • sensorimotor cortex
  • speech
  • subthalamic nucleus

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