Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism

Jan R. Wessel (), Ned Jenkinson, John-Stuart Brittain, Sarah H. E. M. Voets, Tipu Z. Aziz and Adam R. Aron
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Jan R. Wessel: College of Liberal Arts and Sciences, University of Iowa
Ned Jenkinson: John Radcliffe Hospital, University of Oxford
John-Stuart Brittain: John Radcliffe Hospital, University of Oxford
Sarah H. E. M. Voets: John Radcliffe Hospital, University of Oxford
Tipu Z. Aziz: John Radcliffe Hospital, University of Oxford
Adam R. Aron: University of California

Nature Communications, 2016, vol. 7, issue 1, 1-10

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms11195

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