The human brain has evolved for group living [1]. Yet we know so little about how it supports dynamic group interactions that the study of real-world social exchanges has been dubbed the "dark matter of social neuroscience" [2]. Recently, various studies have begun to approach this question by comparing brain responses of multiple individuals during a variety of (semi-naturalistic) tasks [3-15]. These experiments reveal how stimulus properties [13], individual differences [14], and contextual factors [15] may underpin similarities and differences in neural activity across people. However, most studies to date suffer from various limitations: they often lack direct face-to-face interaction between participants, are typically limited to dyads, do not investigate social dynamics across time, and, crucially, they rarely study social behavior under naturalistic circumstances. Here we extend such experimentation drastically, beyond dyads and beyond laboratory walls, to identify neural markers of group engagement during dynamic real-world group interactions. We used portable electroencephalogram (EEG) to simultaneously record brain activity from a class of 12 high school students over the course of a semester (11 classes) during regular classroom activities (Figures 1A-1C; Supplemental Experimental Procedures, section S1). A novel analysis technique to assess group-based neural coherence demonstrates that the extent to which brain activity is synchronized across students predicts both student class engagement and social dynamics. This suggests that brain-to-brain synchrony is a possible neural marker for dynamic social interactions, likely driven by shared attention mechanisms. This study validates a promising new method to investigate the neuroscience of group interactions in ecologically natural settings.

How does the human brain support real-world learning? We used wireless electroencephalography to collect neurophysiological data from a group of 12 senior high school students and their teacher during regular biology lessons. Six scheduled classes over the course of the semester were organized such that class materials were presented using different teaching styles (videos and lectures), and students completed a multiple-choice quiz after each class to measure their retention of that lesson's content. Both students' brain-to-brain synchrony and their content retention were higher for videos than lectures across the six classes. Brain-to-brain synchrony between the teacher and students varied as a function of student engagement as well as teacher likeability: Students who reported greater social closeness to the teacher showed higher brain-to-brain synchrony with the teacher, but this was only the case for lectures-that is, when the teacher is an integral part of the content presentation. Furthermore, students' retention of the class content correlated with student-teacher closeness, but not with brain-to-brain synchrony. These findings expand on existing social neuroscience research by showing that social factors such as perceived closeness are reflected in brain-to-brain synchrony in real-world group settings and can predict cognitive outcomes such as students' academic performance.

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Alpha rhythm (8 to 12 Hz) observed in EEG over human posterior cortex is prominent during eyes‐closed (EC) resting and attenuates during eyes‐open (EO) resting. Research shows that the degree of EC‐to‐EO alpha blocking or alpha desynchronization, termed alpha reactivity here, is a neural marker of cognitive health. We tested the role of acetylcholine in EC‐to‐EO alpha reactivity by applying a multimodal neuroimaging approach to a cohort of young adults and a cohort of older adults. In the young cohort, simultaneous EEG‐fMRI was recorded from twenty‐one young adults during both EO and EC resting. In the older cohort, functional MRI was recorded from forty older adults during EO and EC resting, along with FLAIR and diffusion MRI. For a subset of twenty older adults, EEG was recorded during EO and EC resting in a separate session. In both young and older adults, functional connectivity between the basal nucleus of Meynert (BNM), the major source of cortical acetylcholine, and the visual cortex increased from EC to EO, and this connectivity increase was positively associated with alpha reactivity; namely, the stronger the BNM‐visual cortex functional connectivity increase from EC to EO, the larger the EC‐to‐EO alpha desynchronization. In older adults, lesions of the fiber tracts linking BNM and visual cortex quantified by leukoaraiosis volume, associated with reduced alpha reactivity. These findings support a role of acetylcholine and particularly cholinergic pathways in mediating EC‐to‐EO alpha reactivity and suggest that impaired alpha reactivity could serve as a marker of the integrity of the cholinergic system.

The aim of this study was to explore possible changes in whole brain gray matter volume (GMV) after spinal cord injury (SCI) using voxel-based morphometry (VBM), and to study their associations with the injury duration, severity, and clinical variables. In total, 21 patients with SCI (10 with complete and 11 with incomplete SCI) and 21 age- and sex-matched healthy controls (HCs) were recruited. The 3D high-resolution T1-weighted structural images of all subjects were obtained using a 3.0 Tesla MRI system. Disease duration and American Spinal Injury Association (ASIA) Scale scores were also obtained from each patient. Voxel-based morphometry analysis was carried out to investigate the differences in GMV between patients with SCI and HCs, and between the SCI sub-groups. Associations between GMV and clinical variables were also analyzed. Compared with HCs, patients with SCI showed significant GMV decrease in the dorsal anterior cingulate cortex, bilateral anterior insular cortex, bilateral orbital frontal cortex (OFC), and right superior temporal gyrus. No significant difference in GMV in these areas was found either between the complete and incomplete SCI sub-groups, or between the sub-acute (duration <1 year) and chronic (duration >1 year) sub-groups. Finally, the GMV of the right OFC was correlated with the clinical motor scores of left extremities in not only all SCI patients, but especially the CSCI subgroup. In the sub-acute subgroup, we found a significant positive correlation between the dACC GMV and the total clinical motor scores, and a significant negative correlation between right OFC GMV and the injury duration. These findings indicate that SCI can cause remote atrophy of brain gray matter, especially in the salient network. In general, the duration and severity of SCI may be not associated with the degree of brain atrophy in total SCI patients, but there may be associations between them in subgroups.

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