Thalamic contributions to predictive coding and disconnected consciousness in human volunteers.

Abstract

We can be conscious without awareness of the external world, as when dreaming, a state of disconnected consciousness. The higher-order thalamus is proposed to direct conscious experience to relevant external events through synchronising cortical activity. While disconnected, even surprising external sensory information is ignored. We hypothesise that in wakefulness the cortex synchronises in response to surprise and that this effect is reduced in states of disconnection. An auditory oddball paradigm, with EEG recording, was presented to 18 volunteer subjects while either awake, or disconnected under dexmedetomidine sedation, as confirmed using serial awakening. A computational model of surprise (prediction error) was fit to the auditory tone sequence and cluster-based analysis compared responses across states. Voxel coactivation (synchronisation) was calculated from source-reconstructed data. Surprise was more strongly associated with awake EEG data compared with disconnection. In wakefulness, a significant negative regression coefficient occurred from 33 to 356 ms after the tone over frontal regions (P<0.001), whereas posteriorly a positive coefficient occurred from 37 to 400 ms (P<0.001). This effect was diminished in disconnection. Coactivation of voxels was stronger while awake, and significantly associated with level of surprise. This was perturbed in disconnection (P<0.001), showing reduced synchrony in the disconnected state with no impact of surprise. These findings support the proposal that disconnection emerges from loss of cortical synchronisation in proportion to the salience of sensory stimuli. Impairment of higher-order thalamic synchronisation of cortical activity might underlie sensory disconnection. NCT03284307.