Transient topographical dynamics of the electroencephalogram predict brain connectivity and behavioural responsiveness during drowsiness

Abstract

8As we fall sleep, our brain traverses a series of gradual changes at physiological, behavioural and 9 cognitive levels, which are not yet fully understood. The loss of responsiveness is a critical event in 10 the transition from wakefulness to sleep. Here we seek to understand the electrophysiological 11 signatures that reflect the loss of capacity to respond to external stimuli during drowsiness using two 12 complementary methods: spectral connectivity and EEG microstates. Furthermore, we integrate 13 these two methods for the first time by investigating the connectivity patterns captured during 14 individual microstate lifetimes. While participants performed an auditory semantic classification 15 task, we allowed them to become drowsy and unresponsive. As they stopped responding to the 16 stimuli, we report the breakdown of frontoparietal alpha networks and the emergence of 17 frontoparietal theta connectivity. Further, we show that the temporal dynamics of all canonical EEG 18 microstates slow down during unresponsiveness. We identify a specific microstate (D) CC-BY-NC-ND 4.0 International license not peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was . http://dx.doi.org/10.1101/231464 doi: bioRxiv preprint first posted online Dec. 20, 2017; 3 Author summary 28How do we lose responsiveness as we fall asleep? As we become sleepy, our ability to react to 29 external stimuli disappears gradually. Here we sought to understand the rapid fluctuations in brain 30 electrical activity that predict the loss of responsiveness as participants fell asleep while performing 31 a word classification task. We analysed the patterns of connectivity between anterior and posterior 32 brain regions observed during wakefulness in alpha band and showed that this connectivity shifted 33 to slower theta frequencies as participants became unresponsive. We also investigated the dynamics 34 of brain electrical microstates, which represent an alphabet of quasi-stable global brain states with 35 lifetimes of 10-100 milliseconds, and found that the temporal dynamics of microstates slowed down 36 when participants became unresponsive. Using machine learning, we further showed that 37 microstate dynamics prior to a stimulus predict whether subjects will respond to it. We integrated 38 microstates and connectivity for the first time to show that a specific microstate captures 39 connectivity patterns correlated with unresponsiveness during this transition. We conclude that 40 falling asleep is accompanied by a millisecond-level interplay between distinct brain networks, and 41 suggest a renewed focus on fine-grained temporal scales in the study of transitions between levels 42 of consciousness. 43.

Neurophysiological Correlates of a Single Session of Prefrontal tDCS in Patients with Prolonged Disorders of Consciousness: A Pilot Double-Blind Randomized Controlled Study

“…Chennu et al highlighted that the re-emergence of behavioral awareness is correlated with the fronto-parietal alpha band wPLI connectivity. In addition, other studies showed that a decrease in the posterior-anterior alpha band’s wPLI connectivity was associated with the transition into unconsciousness due to sedation or sleep [ 29 , 30 , 31 ]. Based on these previous results, and considering our findings showing that wPLI connectivity in the alpha band was decreased in the sham and increased in the active sessions (which led to a significant increase in fronto-parietal alpha band connectivity), we may argue that anodal tDCS deprived patients of drowsiness in the active session.…”

Decreasing alertness modulates perceptual decision-making

“…Transition of consciousness in the near-awake to light-decrease of alertness is emerging as a model for internally caused interactions (Canales-Johnson et al;Comsa et al, 2019;Noreika et al;Song and Tagliazucchi, 2020;Tagliazucchi and Laufs, 2014) . With lesion and pharmacological challenges, neuropsychology and cognitive neuroscience have tried to define the necessary and sufficient brain networks, areas and dynamics of the brain to implement cognition, revealing compensation, reconfiguration and plasticity (Adolphs, 2016;Valero-Cabré et al, 2017;Yeung et al, 2018) .…”

Longitudinal Bedside Assessments of Brain Networks in Disorders of Consciousness: Case Reports From the Field

“…Nevertheless, the patient's hdEEG network evolved over many months of repeated assessments, and we observed the presence of increased frontoparietal connectivity at the 6th assessment, in keeping with an increased CRS-R score and behavioral evidence of consciousness. Broadly speaking, there is considerable evidence linking the presence of robust frontoparietal alpha networks with conscious awareness, from research into other altered states, including sleep ( 37 ) and sedation ( 19 , 38 ) in particular. That hdEEG metrics derived from alpha connectivity can track fine-grained longitudinal changes in behavioral state of an individual pDOC patient, even after a long intervening period since the original brain injury (7 years in case of Patient 1), is valuable new knowledge that speaks to the clinical utility of repeated hdEEG network assessments of consciousness.…”