Temporal and Spatial Dynamics of Somatosensory Cortex Network in Typically Developing Children

Research Background

Touch plays a crucial role in our interaction with external objects and the fine control of hand movements. Despite substantial research on the mechanisms of sensory information processing in human skin, it remains unclear how brain regions involved in this process dynamically interact. Existing studies have reported inconsistent results regarding the temporal dynamics of sensory information flow. Therefore, this study aims to explore the temporal and spatial dynamics of sensory processing in typically developing children through magnetoencephalography (MEG) and dynamic analysis of cortex-cortex coupling.

Paper Source

This paper was co-authored by Yanlong Song, Sadra Shahdadian, and other authors, who are affiliated with the Neuroscience Research Center at the Jane and John Justin Institute for Mind Health, Cook Children’s Health Care System in Fort Worth, the Department of Bioengineering at the University of Texas at Arlington, and the Departments of Physical Medicine and Rehabilitation and Radiology at the University of Texas Southwestern Medical Center. The paper was published in Cerebral Cortex on June 4, 2024.

Research Process

Participants and Grouping

The study included 35 typically developing children (TD children) with no known neurological impairments or diseases and normal cognitive function. Participants signed informed consent before any data collection. Five participants who did not complete MEG recordings or whose data contained artifacts were excluded from the study, leaving data from 29 children for analysis.

MRI Acquisition

All participants underwent T1-weighted structural MRI scans using a Siemens Skyra 3T MR Scanner with a 10-channel head coil.

MEG Data Acquisition

Participants sat in a magnetically shielded room, and MEG signals were recorded using the Neuromag® Triux 306-sensor system. During the recording, researchers digitized the positions of the head position indicator (HPI) coils, head landmarks, and additional scalp points to coregister MEG sensor locations with the participants’ structural MRI. Each middle finger was subjected to 400 air-puff stimulations, and data were recorded at a sampling rate of 20 Hz.

Data Processing and Analysis

Initial MEG data were filtered using Temporal Extension of Signal-Space Separation to reduce environmental noise and compensate for head movement. Raw data were preprocessed, and heartbeat and blink artifacts were removed using Independent Component Analysis (ICA). Raw data for each somatic evoked field (SEF) were segmented into event-locked 700ms trials. Dynamic Statistical Parametric Mapping (dSPM) generated individual standard surfaces based on participants’ structural brain MRIs, and MEG signals were coregistered with the standard surface.

Spatiotemporal Cortical Activation Analysis

Reconstructed source SEFs were analyzed at the individual and group levels. The MATLAB function envelop determined the upper and lower envelopes of source SEFs for each cortical vertex, and peak and valley values in individual source SEFs were detected using findpeaks. At the group level, paired-sample permutation t-tests and partial coupling analyses were used for statistical analysis.

Granger Causality Analysis

Significantly activated cortical areas were selected for Granger causality analysis. Source waveform estimates for these areas were used in the Granger causality analyses.

Research Results

Cortical Activation and Source Localization

At the individual level, source localization data showed consistent activation predominantly in the contralateral primary somatosensory area (BA3) within 60 milliseconds of tactile stimulation. This finding aligns with previous research, indicating the stability of contralateral cortical activation in typically developing children. However, subsequent SEF peaks/valleys showed significant individual differences in number, latency, and location.

At the group level, significant and consistent cortical activation was found in the contralateral primary (S1) and secondary somatosensory areas (S2) within a 0-400 millisecond window following stimulation of the left and right middle fingers. Additionally, significant activation was observed in the contralateral primary motor cortex (M1), the parieto-temporal-occipital junction (PTO), and the supplementary motor area (SMA) post-stimulation. Ipsilateral primary somatosensory area (IS1) activation was weaker and less consistent, with significant results observed in only a few participants.

Developmental Changes

Regarding developmental changes, participants’ age showed a significant positive correlation with the first peak activation amplitude of individual source SEFs, suggesting that primary somatosensory area development is not fully mature in children aged 5 to 18. No significant correlation was found between age and the latency of the second and third peaks. However, the maximum activation amplitude of the third peak showed a significant positive correlation with age only in right-hand stimulation, linked to further maturation of somatosensory information processing.

GS Gene Analysis Validates Early Serial Somatosensory Processing Model

GS analysis results indicated that, within 0 to 60 milliseconds after pneumatic stimulation, the primary information flow sequentially proceeded from the contralateral primary somatosensory area (CS1) to the contralateral parietal operculum (CSG), contralateral primary motor area (CM1), and contralateral secondary somatosensory area (CS2). These results support the early serial somatosensory processing model, which posits that thalamic somatosensory inputs first reach CS1 before being forwarded to CS2. These results are consistent with previous studies based on intracranial recordings in humans and non-human primates (e.g., Allison et al., 1991).

Research Conclusion

This study revealed the temporal and spatial cortical activation induced by unilateral pneumatic stimulation in typically developing children through MEG. Significant and consistent activation was observed in contralateral primary somatosensory area S1, secondary somatosensory area S2, primary motor cortex M1, and parietal operculum SG. Ipsilateral cortical activation was relatively weak and inconsistent. GS analysis revealed initial serial information flow, followed by dynamic parallel information flow between consistently activated contralateral cortical areas. These findings provide references for designing brain stimulation studies and applications for children with somatosensory disorders in the future.

This study not only provides valuable insights into the mechanisms of somatosensory information processing in typically developing children but also offers new evidence to explain the critical role of the contralateral cortex in early somatosensory processing. Future research can further explore the clinical application potential of this mechanism.