Cortical state change by auditory deviants: a mismatch response generation mechanism in unconsciousness

Abstract

Context-dependent sensory processing within the predictive coding framework relies on detecting mismatches between incoming stimuli and internal predictive models. Sensory deviants elicit prediction errors, seen as enhanced neural responses, that update these models and influence attention and behaviour. Although prediction errors have been widely observed across brain regions, the downstream processes remain poorly understood. In this study, we recorded electrocorticography in 5 urethane-anaesthetised rats and identified cortical slow oscillations, characterised by spontaneous transitions between "Up" and "Down" states. Deviant stimuli in an auditory oddball paradigm evoked an initial positive prediction error, followed by a prolonged, all-or-nothing response which spread in a travelling wave across the cortex. Identified as putative evoked cortical Up states, these responses were not evoked by standards, omissions or a many-standards control. Up states following deviants occurred more recently after a previous Up state when compared to spontaneous Up states. In preliminary data from an awake rat, long-latency Up states were not present spontaneously or evoked. In a different rat, anaesthetic depth was key to spontaneous and evoked Up states, with more robust Up/Down states and more reliable triggering of Up states under deeper anaesthesia. These results suggest that sensory deviants may cause shifts in cortical state under anaesthesia, explaining the long-latency MMR under anaesthesia and sleep. HighlightsO_LIWhat is the central question of this study? Whether long-latency deviant-evoked mismatch responses could be produced by deviant stimuli in the oddball paradigm evoking Up states. C_LIO_LIWhat is the main finding and its importance? In anaesthetised rat, responses to unexpected stimuli show two components, an early mismatch negativity followed by an Up state, that may be related to deviant activation of cortical ensembles by unexpected stimuli. C_LI