Frontal cortex tracks surprise separately for different sensory modalities but engages a common inhibitory control mechanism

Abstract

The brain constantly generates predictions about the environment to guide action. Unexpected events lead to surprise and can necessitate the modification of ongoing behavior. Surprise can occur for any sensory domain, but it is not clear how these separate surprise signals are integrated to affect motor output. By applying a trial-to-trial Bayesian surprise model to human electroencephalography data recorded during a cross-modal oddball task, we tested whether there are separate predictive models for different sensory modalities (visual, auditory), or whether expectations are integrated across modalities such that surprise in one modality decreases surprise for a subsequent unexpected event in the other modality. We found that while surprise was represented in a common frontal signature across sensory modalities (the fronto-central P3 event-related potential), the single-trial amplitudes of this signature more closely conformed to a model with separate surprise terms for each sensory domain. We then investigated whether surprise-related fronto-central P3 activity indexes the rapid inhibitory control of ongoing behavior after surprise, as suggested by recent theories. Confirming this prediction, the fronto-central P3 amplitude after both auditory and visual unexpected events was highly correlated with the fronto-central P3 found after stop-signals (measured in a separate stop-signal task). Moreover, surprise-related and stopping-related activity loaded onto the same component in a cross-task independent components analysis. Together, these findings suggest that medial frontal cortex maintains separate predictive models for different sensory domains, but engages a common mechanism for inhibitory control of behavior regardless of the source of surprise.\n\nAuthor summarySurprise is an elementary cognitive computation that the brain performs to guide behavior. We investigated how the brain tracks surprise across different senses: Do unexpected sounds make subsequent unexpected visual stimuli less surprising? Or does the brain maintain separate expectations of environmental regularities for different senses? We found that the latter is the case. However, even though surprise was separately tracked for auditory and visual events, it elicited a common signature over frontal cortex in both sensory domains. Importantly, we observed the same neural signature when actions had to be stopped after non-surprising stop-signals in a motor inhibition task. This suggests that this signature reflects a rapid interruption of ongoing behavior when our surroundings do not conform to our expectations.