β-Bursts over Frontal Cortex Track the Surprise of Unexpected Events in Auditory, Visual, and Tactile Modalities

Abstract

Abstract One of the fundamental ways in which the brain regulates and monitors behavior is by making predictions about the sensory environment and adjusting behavior when those expectations are violated. As such, surprise is one of the fundamental computations performed by the human brain. In recent years, it has been well established that one key aspect by which behavior is adjusted during surprise is inhibitory control of the motor system. Moreover, because surprise automatically triggers inhibitory control without much proactive influence, it can provide unique insights into largely reactive control processes. Recent years have seen tremendous interest in burst-like β frequency events in the human (and nonhuman) local field potential—especially over (p)FC—as a potential signature of inhibitory control. To date, β-bursts have only been studied in paradigms involving a substantial amount of proactive control (such as the stop-signal task). Here, we used two cross-modal oddball tasks to investigate whether surprise processing is accompanied by increases in scalp-recorded β-bursts. Indeed, we found that unexpected events in all tested sensory domains (haptic, auditory, visual) were followed by low-latency increases in β-bursting over frontal cortex. Across experiments, β-burst rates were positively correlated with estimates of surprise derived from Shannon's information theory, a type of surprise that represents the degree to which a given stimulus violates prior expectations. As such, the current work clearly implicates frontal β-bursts as a signature of surprise processing. We discuss these findings in the context of common frameworks of inhibitory and cognitive control after unexpected events.