Task-Modulated Corticocortical Synchrony in the Cognitive-Motor Network Supporting Handwriting

Abstract

Both motor and cognitive aspects of behavior depend on dynamic, accurately timed neural processes in large-scale brain networks. Here, we studied synchronous interplay between cortical regions during production of cognitive-motor sequences in humans. Specifically, variants of handwriting that differed in motor variability, linguistic content, and memorization of movement cues were contrasted to unveil functional sensitivity of corticocortical connections. Data-driven magnetoencephalography mapping (n = 10) uncovered modulation of mostly left-hemispheric corticocortical interactions, as quantified by relative changes in phase synchronization. At low frequencies (~2-13 Hz), enhanced frontoparietal synchrony was related to regular handwriting, whereas premotor cortical regions synchronized for simple loop production and temporo-occipital areas for a writing task substituting normal script with loop patterns. At the beta-to-gamma band (~13-45 Hz), enhanced synchrony was observed for regular handwriting in the central and frontoparietal regions, including connections between the sensorimotor and supplementary motor cortices and between the parietal and dorsal premotor/precentral cortices. Interpreted within a modular framework, these modulations of synchrony mainly highlighted interactions of the putative pericentral subsystem of hand coordination and the frontoparietal subsystem mediating working memory operations. As part of cortical dynamics, interregional phase synchrony varies depending on task demands in production of cognitive-motor sequences.

Keywords: DICS; MEG; functional connectivity; language production; movement sequence.

Figure 1

Hypothesized cortical system and experimental paradigm. (A) Estimation of the pericentral (green shade), frontoparietal (blue) and perisylvian-occipital (red) divisions of the cortex postulated to support handwriting in the left hemisphere (inset displays the dorsal medial view). Colored dots indicate the reference points derived from neuroimaging literature (as cited in the Methods). Dashed lines indicate the central and intraparietal sulci. dPM; IFC, inferior frontal cortex; IOTC, inferior occipitotemporal cortex; IPL, inferior parietal lobe; IPS, intraparietal sulcus; POper, parietal operculum; SMA; SMC, primary sensorimotor cortex; SPL, superior parietal lobe; STC, superior temporal cortex; vPM. (B) Schematic illustration of the hypothetical network system for handwriting consisting of the pericentral (hand coordination), frontoparietal (core working memory), and perisylvian-occipital (audiovisual language) subsystems. Nodal regions (circles) interact through coherent signaling (bidirectional arrows) within and between the subsystems. The pericentral module forms a control loop with the arm musculature. (C) In a delayed dictation-to-writing/audio cue-to-movement paradigm, the subjects first memorized sentences or auditory pattern cues and, right after, produced corresponding movements. The tasks included RW; LW; PD; and repetitive LD where nonsense scramble stimuli did not offer guidance for the movement. Timeline of a single experimental trial is presented under the task descriptions (WS, warning signal; GO, signal for starting the movement). (An example Finnish sentence [in RW] translates as “The herd seeks shelter”.) The emphasis of task-associated motor and cognitive processes in each task is depicted below.

Figure 2

Arm muscle activity during movement sequences. (A) Example EMG traces (in a single subject) for each variant of the handwriting task. (B) Normalized mean EMG spectra (n = 10) for each variant of handwriting task (recorded from e. carpi arm muscle; high-passed, rectified signals; spectra normalized individually to the maximum value across tasks before averaging across subjects). (C) Individual EMG peak frequencies as a function of grapheme rate per second for letters (RW task) and loops (LD task) in spontaneous production (subset of n = 5).

Figure 3

Coherent neural frequencies. (A) Normalized mean coherence spectra (n = 10) between the arm muscle and the MEG sensors located above the SMC (EMG-MEG; above) and the mean coherence spectra between pairs of left-sided MEG sensors at a minimum distance of 10 cm (MEG-MEG; below). For task abbreviations, see the Introduction. (B) The log-log plot of mean MEG-MEG coherence spectra for each subject (n = 10) averaged across the tasks. The specific frequencies of interest are indicated with Greek lettering.

Figure 4

Mapping of the COIs. (A) Networks comprised of the coherent COI mapped at the low, mid, and high spectral ranges within and between the left and right hemispheres. (B) Robustness of identifying the coherent nodes (exemplified at low frequencies in the left hemisphere) when the clustering parameters of mapping were varied (bundle sizes 2–10; distance criterion 15–25 mm; rendering a total of 99 parameter combinations). The color-coding represents the number of parameter combinations that revealed a specific node. Black dots indicate the nodes selected for the present mapping (with bundle size of 3 and distance criterion 20 mm). (C) The nodes of corticocortical coherence (yellow) at the low spectral range superimposed with the regions (red) showing corticomuscular coherence (at ~ 2–5 Hz).

Figure 5

Task-sensitive corticocortical phase synchronization in the left and right hemispheres (A) and across the hemispheres (B). The cortical surface view illustrates the corticocortical connections (a–q), which showed modulated phase synchrony for the different variants of handwriting task (Fig. 1C). Color-coding refers to the spectral ranges. The bar graphs (below) show SI values (±SEM) for each connection. Task contrast (n = 10; maximum-statistics permutation testing based on t-statistics, 95% threshold) and the frequency band of the effect are indicated. Note the different ranges of y-axis values and the fact that permutation testing can highlight statistical differences that do not fully comply with the apparent differences in mean SI levels (see, e.g., connections p and q).

Figure 6

Assignment of the nodal regions to the postulated cortical subsystems. The plot (3-dimensional MNI data projected to the y-z plane) illustrates the nodes of the task-sensitive connections (larger connected circles) and the reference points (smaller circles) for the postulated subsystems that support handwriting (pericentral in green, frontoparietal in blue, and perisylvian-occipital in red; see Fig. 1A,B), and points representing the “default mode” system (gray). Each connection is labeled (a–i) as in Figure 5.