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Human cortical dynamics during full-body heading changes.

ABSTRACT: The retrosplenial complex (RSC) plays a crucial role in spatial orientation by computing heading direction and translating between distinct spatial reference frames based on multi-sensory information. While invasive studies allow investigating heading computation in moving animals, established non-invasive analyses of human brain dynamics are restricted to stationary setups. To investigate the role of the RSC in heading computation of actively moving humans, we used a Mobile Brain/Body Imaging approach synchronizing electroencephalography with motion capture and virtual reality. Data from physically rotating participants were contrasted with rotations based only on visual flow. During physical rotation, varying rotation velocities were accompanied by pronounced wide frequency band synchronization in RSC, the parietal and occipital cortices. In contrast, the visual flow rotation condition was associated with pronounced alpha band desynchronization, replicating previous findings in desktop navigation studies, and notably absent during physical rotation. These results suggest an involvement of the human RSC in heading computation based on visual, vestibular, and proprioceptive input and implicate revisiting traditional findings of alpha desynchronization in areas of the navigation network during spatial orientation in movement-restricted participants.

SUBMITTER: Gramann K

PROVIDER: S-EPMC8440696 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Language tasks require the coordinated activation of multiple subnetworks-groups of related cortical interactions involved in specific components of task processing. Although electrocorticography (ECoG) has sufficient temporal and spatial resolution to capture the dynamics of event-related interactions between cortical sites, it is difficult to decompose these complex spatiotemporal patterns into functionally discrete subnetworks without explicit knowledge of each subnetwork's timing. We hypothesized that subnetworks corresponding to distinct components of task-related processing could be identified as groups of interactions with co-varying strengths. In this study, five subjects implanted with ECoG grids over language areas performed word repetition and picture naming. We estimated the interaction strength between each pair of electrodes during each task using a time-varying dynamic Bayesian network (tvDBN) model constructed from the power of high gamma (70-110Hz) activity, a surrogate for population firing rates. We then reduced the dimensionality of this model using principal component analysis (PCA) to identify groups of interactions with co-varying strengths, which we term functional network components (FNCs). This data-driven technique estimates both the weight of each interaction's contribution to a particular subnetwork, and the temporal profile of each subnetwork's activation during the task. We found FNCs with temporal and anatomical features consistent with articulatory preparation in both tasks, and with auditory and visual processing in the word repetition and picture naming tasks, respectively. These FNCs were highly consistent between subjects with similar electrode placement, and were robust enough to be characterized in single trials. Furthermore, the interaction patterns uncovered by FNC analysis correlated well with recent literature suggesting important functional-anatomical distinctions between processing external and self-produced speech. Our results demonstrate that subnetwork decomposition of event-related cortical interactions is a powerful paradigm for interpreting the rich dynamics of large-scale, distributed cortical networks during human cognitive tasks.

Project description:BackgroundLittle is known about the modulation of cortical excitability in the prefrontal cortex during fear processing in humans. Here, we aimed to transiently modulate and test the cortical excitability during fear processing using transcranial magnetic stimulation (TMS) and brain oscillations in theta and alpha frequency bands with electroencephalography (EEG).MethodsWe conducted two separate experiments (no-TMS and TMS). In the no-TMS experiment, EEG recordings were performed during the instructed fear paradigm in which a visual cue (CS+) was paired with an aversive unconditioned stimulus (electric shock), while the other visual cue was unpaired (CS-). In the TMS experiment, in addition the TMS was applied on the right dorsomedial prefrontal cortex (dmPFC). The participants also underwent structural MRI (magnetic resonance imaging) scanning and were assigned pseudo-randomly to both experiments, such that age and gender were matched. The cortical excitability was evaluated by time-frequency analysis and functional connectivity with weighted phase lag index (WPLI). We further linked the excitability patterns with markers of stress coping capability.ResultsAfter visual cue onset, we found increased theta power in the frontal lobe and decreased alpha power in the occipital lobe during CS+ relative to CS- trials. TMS of dmPFC increased theta power in the frontal lobe and reduced alpha power in the occipital lobe during CS+. The TMS pulse increased the information flow from the sensorimotor region to the prefrontal and occipital regions in the theta and alpha bands, respectively during CS+ compared to CS-. Pre-stimulation frontal theta power (0.75-1 s) predicted the magnitude of frontal theta power changes after stimulation (1-1.25 s). Finally, the increased frontal theta power during CS+ compared to CS- was positively correlated with stress coping behavior.ConclusionOur results show that TMS over dmPFC transiently modulated the regional cortical excitability and the fronto-occipital information flows during fear processing, while the pre-stimulation frontal theta power determined the strength of achieved effects. The frontal theta power may serve as a biomarker for fear processing and stress-coping responses in individuals and could be clinically tested in mental disorders.

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Human cortical dynamics during full-body heading changes.

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