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.
Highlights
Surprise occurs when expectations about the multi-sensory environment are violated
In the cross-modal oddball task, correct trial reaction time (RT) showed the expected pattern as well: There was a main effect of TRIAL TYPE (F(2/108) = 25.3, p = 9.74 10−10, partial-eta^2 = .32), a main effect of BLOCK (F(3/162) = 7.64, p = 8.2567 10−5, p-eta^2 = .12), and a significant INTERACTION (F(6/324) = 9.78, p = 6.51 10−10, p-eta^2 = .15)
Individual comparisons revealed that in Block 1, both visual and auditory unexpected-cue RTs were significantly longer compared to standard-cue RTs (t(54) = 9.41, p = 5.48 10−13, d = .75 for visual and t(54) = 3.14, p = .0028, d = .29 for auditory, respectively)
Summary
Surprise occurs when expectations about the multi-sensory environment are violated. It provides an elementary cognitive and physiological process that forms the backbone of many influential theories of cognitive processing and control [1,2,3,4,5]. Prior imaging work has shown that unexpected events, regardless of their sensory modality, activate similar brain networks [8,9,10,11]. Surprise might result from separate, independent predictions for each sensory domain. In this latter case, the modality-independent surprise response could index a common set of downstream mechanisms triggered by surprise, regardless of sensory domain
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