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; Adam R Aron

doi:10.1038/ncomms11195

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Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism

Journal article

Open access

Peer reviewed

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

Nature communications, Vol.7(1), pp.11195-11195

04/18/2016

DOI: 10.1038/ncomms11195

PMCID: PMC4837448

PMID: 27088156

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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.

Humans

Middle Aged

Evoked Potentials - physiology

Male

Random Allocation

Parkinson Disease - physiopathology

Basal Ganglia - physiology

Electroencephalography - methods

Psychomotor Performance - physiology

Young Adult

Subthalamic Nucleus - physiology

Cognition - physiology

Female

Aged

Photic Stimulation

Memory - physiology

Details

Title: Subtitle: Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism
Creators: Jan R Wessel - Psychology Department, University of California, San Diego, La Jolla, California 92093, USA
Ned Jenkinson - School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham B15 2TT, UK
John-Stuart Brittain - Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK
Sarah H E M Voets - Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK
Tipu Z Aziz - Nuffield Department of Clinical Neurosurgery, John Radcliffe Hospital, University of Oxford, Oxford OX1 2JD, UK
Adam R Aron - Psychology Department, University of California, San Diego, La Jolla, California 92093, USA
Resource Type: Journal article
Publication Details: Nature communications, Vol.7(1), pp.11195-11195
DOI: 10.1038/ncomms11195
PMID: 27088156
PMCID: PMC4837448
NLM abbreviation: Nat Commun
ISSN: 2041-1723
eISSN: 2041-1723
Publisher: England
Grant note: R21 NS085543 / NINDS NIH HHS R01 DA026452 / NIDA NIH HHS
Language: English
Date published: 04/18/2016
Academic Unit: Roy J. Carver Department of Biomedical Engineering; Neurology; Psychological and Brain Sciences; Iowa Neuroscience Institute
Record Identifier: 9984002487402771

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