Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing

The dynamic integration of sensory and bodily signals is central to adaptive behaviour. Although the anterior cingulate cortex (ACC) and the anterior insular cortex (AIC) play key roles in this process, their context-dependent dynamic interactions remain unclear. Here, we studied the spectral features and interplay of these two brain regions using high-fidelity intracranial-EEG recordings from five patients (ACC: 13 contacts, AIC: 14 contacts) acquired during movie viewing with validation analyses performed on an independent resting intracranial-EEG dataset. ACC and AIC both showed a power peak and positive functional connectivity in the gamma (30-35 Hz) frequency while this power peak was absent in the resting data. We then used a neurobiologically informed computational model investigating dynamic effective connectivity asking how it linked to the movie's perceptual (visual, audio) features and the viewer's heart rate variability (HRV). Exteroceptive features related to effective connectivity of ACC highlighting its crucial role in processing ongoing sensory information. AIC connectivity was related to HRV and audio emphasising its core role in dynamically linking sensory and bodily signals. Our findings provide new evidence for complementary, yet dissociable, roles of neural dynamics between the ACC and the AIC in supporting brain-body interactions during an emotional experience. Author Summary Naturalistic stimulus such as movies provide an optimal platform to study time-resolved neural interactions supporting integration of sensory and bodily information. Here, we obtain intracranial recordings from anterior insular cortex and the anterior cingulate cortex while participants (undergoing clinical evaluation for epilepsy) viewed a short movie capable of eliciting robust physiological responses. We first characterise the spectral properties with subsequent model driven approach to probe moment-to-moment neural interactions between the anterior insular cortex and the anterior cingulate cortex. Our findings highlight how this neural system plays a key role in linking the contextual integration of sensory information with that of internal body status.