Abstract
Surprising events markedly affect behaviour and cognition, yet the underlying mechanism is unclear. Surprise recruits a brain mechanism that globally suppresses motor activity, ostensibly via the subthalamic nucleus (STN) of the basal ganglia. Here, we tested whether this suppressive mechanism extends beyond skeletomotor suppression and also affects cognition (here, verbal working memory, WM). We recorded scalp-EEG (electrophysiology) in healthy participants and STN local field potentials in Parkinson's patients during a task in which surprise disrupted WM. For scalp-EEG, surprising events engage the same independent neural signal component that indexes action stopping in a stop-signal task. Importantly, the degree of this recruitment mediates surprise-related WM decrements. Intracranially, STN activity is also increased post surprise, especially when WM is interrupted. These results suggest that surprise interrupts cognition via the same fronto-basal ganglia mechanism that interrupts action. This motivates a new neural theory of how cognition is interrupted, and how distraction arises after surprising events.
Highlights
Surprising events markedly affect behaviour and cognition, yet the underlying mechanism is unclear
Based on the model’s surprise values, we found that surprising tones that were followed by erroneous probes were more surprising than those preceding correct WM, with medium-to-large effect size (paired samples t-test, N 1⁄4 20, t(19) 1⁄4 2.14, P 1⁄4 0.045, d 1⁄4 0.77, Fig. 1c), which shows that WM failures in this task were directly related to the degree of surprise
We tested whether a putative fronto-basal ganglia suppressive mechanism involved in motor stopping is recruited to interrupt cognitive activity following surprising events
Summary
Surprising events markedly affect behaviour and cognition, yet the underlying mechanism is unclear. Recent behavioural studies have shown that motor stopping has effects even beyond the motor system, as it affects stimulus value[16] and WM encoding[17] On this basis, we surmise that the impact of surprising events on cognition could relate, at least partially, to the same broad neural suppressive mechanism that is actively recruited to interrupt motor activity (e.g., in the SST). We tested whether the recruitment of the neural suppressive mechanism underlying motor stopping could explain WM failures following surprising events Activity of this neural suppressive mechanism can be assayed using scalp electrophysiology (EEG) and local field potential (LFP) recordings from structures deeper in the brain
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