Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism

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Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism. / Wessel, Jan R.; Jenkinson, Ned; Brittain, John Stuart; Voets, Sarah H. E. M.; Aziz, Tipu Z.; Aron, Adam R.

In: Nature Communications, Vol. 7, 11195, 18.04.2016.

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Wessel, Jan R. ; Jenkinson, Ned ; Brittain, John Stuart ; Voets, Sarah H. E. M. ; Aziz, Tipu Z. ; Aron, Adam R. / Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism. In: Nature Communications. 2016 ; Vol. 7.

Bibtex

@article{2c1e73e3415a47f48cb10f6b7eed7335,
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.",
keywords = "basal ganglia , cognitive neuroscience , working memory",
author = "Wessel, {Jan R.} and Ned Jenkinson and Brittain, {John Stuart} and Voets, {Sarah H. E. M.} and Aziz, {Tipu Z.} and Aron, {Adam R.}",
year = "2016",
month = apr
day = "18",
doi = "10.1038/ncomms11195",
language = "English",
volume = "7",
journal = "Nature Communications",
issn = "2041-1723",
publisher = "Springer",

}

RIS

TY - JOUR

T1 - Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism

AU - Wessel, Jan R.

AU - Jenkinson, Ned

AU - Brittain, John Stuart

AU - Voets, Sarah H. E. M.

AU - Aziz, Tipu Z.

AU - Aron, Adam R.

PY - 2016/4/18

Y1 - 2016/4/18

N2 - 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.

AB - 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.

KW - basal ganglia

KW - cognitive neuroscience

KW - working memory

UR - http://www.scopus.com/inward/record.url?scp=84973177470&partnerID=8YFLogxK

U2 - 10.1038/ncomms11195

DO - 10.1038/ncomms11195

M3 - Article

AN - SCOPUS:84973177470

VL - 7

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 11195

ER -