Sedation Modulates Frontotemporal Predictive Coding Circuits and the Double Surprise Acceleration Effect

Abstract

Two important theories in cognitive neuroscience are predictive coding (PC) and the global workspace (GW) theory. A key research task is to understand how these two theories relate to one another, and particularly, how the brain transitions from a predictive early state to the eventual engagement of a brain-scale state (the GW). To address this question, we present a source-localization of EEG responses evoked by the local-global task—an experimental paradigm that engages a predictive hierarchy, which encompasses the GW. The results of our source reconstruction suggest three phases of processing. The first phase involves the sensory (here auditory) regions of the superior temporal lobe and predicts sensory regularities over a short timeframe (as per the local effect). The third phase is brain-scale, involving inferior frontal, as well as inferior and superior parietal regions, consistent with a global neuronal workspace (GNW; as per the global effect). Crucially, our analysis suggests that there is an intermediate (second) phase, involving modulatory interactions between inferior frontal and superior temporal regions. Furthermore, sedation with propofol reduces modulatory interactions in the second phase. This selective effect is consistent with a PC explanation of sedation, with propofol acting on descending predictions of the precision of prediction errors; thereby constraining access to the GNW.

Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects

“…Recent non-invasive studies found evidence for interactions between LD and GD effects, suggesting that these two forms of deviance detection are not fully independent modes of auditory novelty processing (Shirazibeheshti et al, 2018;Kompus et al, 2020;Witon et al, 2020). Local-by-global (L × G) interactions can be measured by comparing responses to four stimulus conditions: LSGS, LSGD, LDGS and LDGD.…”

Automatic Sensory Predictions: A Review of Predictive Mechanisms in the Brain and Their Link to Conscious Processing

“…Under standard predictive theories, the influence of PEs depends on their precision ( Auksztulewicz and Friston, 2015 ; Kanai et al, 2015 ), and, as explained previously, this is the effect of attentional selection. This means that ascending PEs with higher precision have more model-updating power than those with lower precision ( Witon et al, 2020 ). Future studies can evaluate whether a similar computational role can be attributed to different states of consciousness and, in particular, according to their arousal and awareness contents.…”

“…The interaction between the local and global effects was significant in a late time window (400–600 ms). The authors found a locally mediated acceleration of global deviance responses ( Witon et al, 2020 ) during sedation and recovery. The second important interaction – the local standard global deviant, representing the pure global deviance effect – was reduced in anesthesia compared to recovery.…”

“…More recent studies have employed the local-global paradigm ( Shirazibeheshti et al, 2018 ; Witon et al, 2020 ) with high-density EEG or iEEG recordings ( Nourski et al, 2018 ) to test this hypothesis directly. Specifically, Shirazibeheshti et al (2018) measured high-density EEG during a local-global paradigm in wakefulness, propofol sedation, and recovery.…”

“…The authors posited that the coincidence of local and global deviance had a facilitatory effect on global deviance responses, which was reduced when individuals were sedated. Witon et al (2020) further examined the neural circuits of this effect and observed effects of sedation on local deviance responses during early (100–150 ms post-stimulus onset) and middle (250–350 ms) time periods, indicative of modulations of evoked power responses early in the processing pathway. The interaction between the local and global effects was significant in a late time window (400–600 ms).…”