title: Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism.
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.
authors.affiliation: Department of Psychological and Brain Sciences, College of Liberal Arts and Sciences, University of Iowa, Iowa City, Iowa 52245, USA.|Department of Neurology, Carver College of Medicine, University of Iowa, Iowa City, Iowa 52245, USA.|Psychology Department, University of California, San Diego, La Jolla, California 92093, USA.
authors.forename: Jan R
authors.initials: JR
authors.lastname: Wessel
authors.affiliation: Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK.|School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham B15 2TT, UK.
authors.forename: Ned
authors.identifier: http://orcid.org/0000-0002-6803-486X
authors.initials: N
authors.lastname: Jenkinson
authors.affiliation: Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK.
authors.forename: John-Stuart
authors.initials: JS
authors.lastname: Brittain
authors.affiliation: Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK.
authors.forename: Sarah H E M
authors.initials: SH
authors.lastname: Voets
authors.affiliation: Nuffield Department of Clinical Neurosurgery, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK.
authors.forename: Tipu Z
authors.initials: TZ
authors.lastname: Aziz
authors.affiliation: Psychology Department, University of California, San Diego, La Jolla, California 92093, USA.
authors.forename: Adam R
authors.initials: AR
authors.lastname: Aron
mesh_terms: D000368:Aged; D001479:Basal Ganglia / Q000502:physiology*; D003071:Cognition / Q000502:physiology*; D004569:Electroencephalography / Q000379:methods; D005071:Evoked Potentials / Q000502:physiology; D005260:Female; D006801:Humans; D008297:Male; D008568:Memory / Q000502:physiology; D008875:Middle Aged; D010300:Parkinson Disease / Q000503:physiopathology*; D010775:Photic Stimulation; D011597:Psychomotor Performance / Q000502:physiology; D011897:Random Allocation; D020531:Subthalamic Nucleus / Q000502:physiology*; D055815:Young Adult