Oscillatory Dynamics Track Motor Performance Improvement in Human Cortex

<div><p>Improving performance in motor skill acquisition is proposed to be supported by tuning of neural networks. To address this issue we investigated changes of phase-amplitude cross-frequency coupling (paCFC) in neuronal networks during motor performance improvement. We recorded intracranially from subdural electrodes (electrocorticogram; ECoG) from 6 patients who learned 3 distinct motor tasks requiring coordination of finger movements with an external cue (serial response task, auditory motor coordination task, go/no-go). Performance improved in all subjects and all tasks during the first block and plateaued in subsequent blocks. Performance improvement was paralled by increasing neural changes in the trial-to-trial paCFC between theta (; 4–8 Hz) phase and high gamma (HG; 80–180 Hz) amplitude. Electrodes showing this covariation pattern (Pearson's r ranging up to .45) were located contralateral to the limb performing the task and were observed predominantly in motor brain regions. We observed stable paCFC when task performance asymptoted. Our results indicate that motor performance improvement is accompanied by adjustments in the dynamics and topology of neuronal network interactions in the and HG range. The location of the involved electrodes suggests that oscillatory dynamics in motor cortices support performance improvement with practice.</p></div

Depiction of the results from the ROI-analysis.

<p>A) ROIs with significant performance improvement unrelated TPR/performance correlations. B) ROIs with significant performance improvement related TPR/performance correlations. ROIs with significant correlations (Bonferroni correct for six comparisons) are marked with an asterisk. The 6 ROIs are the anterior and posterior medial frontal gyrus, the anterior and the posterior inferior frontal gyrus, and the superior and posterior sensorimotor cortex. The blue margin shows the grid coverage across all subjects with a square grid implanted.</p

Electrodes with significant trial-by-trial correlations of TPR with performance.

<p>The significance threshold was determined in a permutation procedure (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089576#s4" target="_blank">Methods</a>) A) Learning unrelated correlations of TPR with performance. B) Learning related correlations of TPR with performance. Darker colors indicate stronger correlations. See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089576#s4" target="_blank">Methods</a> for calculations on separating performance and learning related effects. The blue shape in the first and second row show the outline of all superimposed square grids. The black shapes in the third row denotes the grid locations for the participant in the AMCT. Spatial distortions result from the projection onto the cortex (for details see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089576#pone.0089576.s003" target="_blank">Figure S2</a>).</p

Calculation of the trough to peak ratio (TPR).

<p>We quantified paCFC as the ratio between trough (local minima of the time series - red vertical lines) and HG amplitude at the corresponding trough. Around each detected trough we spanned a window (half cycle - gray bars) in which activity (black bold line) and HG amplitude (green line) was averaged.</p

The amplitude of the HG oscillations is phase coupled to the -band (4–8 Hz) oscillations in all subjects across paradigms.

<p>A) Time courses of sine wave functions fitted to the single trial amplitude envelopes of the HG oscillations of one subjects collapsed over electrodes. B) Sine wave functions fitted to the trial-averaged HG oscillation amplitudes envelopes of each subject. Each solid line represents the fit for one subject. Each dot represents the individual trial average of the HG oscillation in one of 20 intervals equally spaced over a cycle. The black dashed line shows the averaged sine waves across subjects. The vertical blue dashed line denotes the averaged phase angle the HG amplitude peaks across subjects. The maximum of the cycle is at phase 0 and the minimum at .</p

Here we depict the separation of the whole experimental session into trial bins.

<p>The experimental session in each patient consisted of 2 blocks separated by a short break. In each block we defined two trial bins each containing 30 trials (blue). We compared the PLV across the four trial bins to assess the evolution of connectivity length of and HG activity during motor performance improvement.</p

Behavioral data.

<p>For SRT (serial reaction time task) and GNG (Go/No-Go) task reaction time is shown (standard deviation) in msec. For AMCT (auditory-motor coordination task) the absolute deviation from precision is shown also in msec. Each trialbin encompasses 30 trials.</p

Covariation of average paCFC with performance over the time course of the experiment.

<p>A) The development of TPR and motor performance during the time course of the experiment. Results are collapsed across all six subjects/three experiments. Data for the first block and second block are shown in the left and second half of the plot. Each point represents the average in one of 100 time bins. Exponential functions fitted to the data z-scored over both blocks indicate a similar time course for performance and TPR. B) Subject averaged motor performance during the first and last sets of 30 trials in the first (early learning) and the second (late learning) experimental block. C) Subject averaged TPR. Data was z-scored within blocks and TPR was averaged over all electrodes.</p

Paradigms employed (details described in Methods).

<p>A) Serial reaction time task: The numbers on the screen indicate the finger to be used for the key press. B) Go/no-go: Green indicates a go and red indicates a no-go trial. C) Auditory motor coordination: Subjects were instructed to press a key in the middle of the interval between two consecutive tones. The interval length was either one second or two seconds and was held fixed for one minute. Each subject carried out two blocks (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089576#s4" target="_blank">Methods</a>).</p