Propofol-mediated loss of consciousness disrupts predictive routing and local field phase modulation of neural activity.
Yihan Sophy Xiong, Jacob A Donoghue, Mikael Lundqvist, Meredith Mahnke, Alex James Major, Emery N Brown, Earl K Miller, André M Bastos
Proceedings of the National Academy of Sciences of the United States of America October 15, 2024 DOI: 10.1073/pnas.2315160121 via PubMed
Summary
Predictive coding in the cortex relies on predictions fed back from deep layers via alpha/beta oscillations (8–30 Hz) that inhibit gamma (40–100 Hz) and spiking carrying sensory input forward. Intracranial recordings in macaques during passive auditory oddball tasks showed that in the awake state alpha/beta oscillations inhibited processing of predictable sounds. Propofol-induced loss of consciousness eliminated this alpha/beta modulation in sensory cortex and reduced alpha/beta coherence between sensory and frontal areas. Consequently, oddball stimuli evoked enhanced gamma power, late spiking, and superficial layer sinks in auditory cortex, indicating a disinhibited state. However, differential spiking to oddballs in higher-order cortex was lost, likely due to disrupted spike-field coupling. These findings constrain theories of consciousness.
Study at a glance
| Characteristics | Experimental study Peer reviewed |
|---|---|
| Population | Macaque monkeys |
| Keywords | Anesthesia Consciousness Oscillations Predictive processing |
| Citations | 32 |
| Key finding | Propofol-mediated loss of consciousness eliminates alpha/beta modulation by predictable stimuli in sensory cortex and reduces alpha/beta coherence between sensory and frontal areas, leading to a disinhibited auditory cortex but loss of differential spiking to oddballs in higher-order cortex. |
Abstract
Predictive coding is a fundamental function of the cortex. The predictive routing model proposes a neurophysiological implementation for predictive coding. Predictions are fed back from the deep-layer cortex via alpha/beta (8 to 30 Hz) oscillations. They inhibit the gamma (40 to 100 Hz) and spiking that feed sensory inputs forward. Unpredicted inputs arrive in circuits unprepared by alpha/beta, resulting in enhanced gamma and spiking. To test the predictive routing model and its role in consciousness, we collected data from intracranial recordings of macaque monkeys during passive presentation of auditory oddballs before and after propofol-mediated loss of consciousness (LOC). In line with the predictive routing model, alpha/beta oscillations in the awake state served to inhibit the processing of predictable stimuli. Propofol-mediated LOC eliminated alpha/beta modulation by a predictable stimulus in the sensory cortex and alpha/beta coherence between sensory and frontal areas. As a result, oddball stimuli evoked enhanced gamma power, late period (>200 ms from stimulus onset) spiking, and superficial layer sinks in the sensory cortex. LOC also resulted in diminished decodability of pattern-level prediction error signals in the higher-order cortex. Therefore, the auditory cortex was in a disinhibited state during propofol-mediated LOC. However, despite these enhanced feedforward responses in the auditory cortex, there was a loss of differential spiking to oddballs in the higher-order cortex. This may be a consequence of a loss of within-area and interareal spike-field coupling in the alpha/beta and gamma frequency bands. These results provide strong constraints for current theories of consciousness.