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

Wessel JR, Jenkinson N, Brittain JS, Voets SH, Aziz TZ, Aron AR - Nat Commun (2016)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychological and Brain Sciences, College of Liberal Arts and Sciences, University of Iowa, Iowa City, Iowa 52245, USA.

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.

No MeSH data available.


Related in: MedlinePlus

STN individual subjects results.(a) Behavioural results (accuracy on the WM probe split by trial type). (b) Individual contrasts of surprising versus standard events, specifically in the gamma band (significant areas at P<0.01 highlighted). (c) Individual single-trial GLM results, specifically in the gamma band (significant areas at P<0.05 highlighted).
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f6: STN individual subjects results.(a) Behavioural results (accuracy on the WM probe split by trial type). (b) Individual contrasts of surprising versus standard events, specifically in the gamma band (significant areas at P<0.01 highlighted). (c) Individual single-trial GLM results, specifically in the gamma band (significant areas at P<0.05 highlighted).

Mentions: ERSPs were computed as for scalp-EEG above (with a broader frequency spectrum of 1–100 Hz), thresholded for significance at P<0.05 on the group level. For the individual subjects data figure (Fig. 6), significance at P<0.01 is displayed. The GLM analysis was also performed as it was for the scalp-EEG (with a broader frequency spectrum of 1–100 Hz), thresholded for significance at P<0.05.


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

Wessel JR, Jenkinson N, Brittain JS, Voets SH, Aziz TZ, Aron AR - Nat Commun (2016)

STN individual subjects results.(a) Behavioural results (accuracy on the WM probe split by trial type). (b) Individual contrasts of surprising versus standard events, specifically in the gamma band (significant areas at P<0.01 highlighted). (c) Individual single-trial GLM results, specifically in the gamma band (significant areas at P<0.05 highlighted).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4837448&req=5

f6: STN individual subjects results.(a) Behavioural results (accuracy on the WM probe split by trial type). (b) Individual contrasts of surprising versus standard events, specifically in the gamma band (significant areas at P<0.01 highlighted). (c) Individual single-trial GLM results, specifically in the gamma band (significant areas at P<0.05 highlighted).
Mentions: ERSPs were computed as for scalp-EEG above (with a broader frequency spectrum of 1–100 Hz), thresholded for significance at P<0.05 on the group level. For the individual subjects data figure (Fig. 6), significance at P<0.01 is displayed. The GLM analysis was also performed as it was for the scalp-EEG (with a broader frequency spectrum of 1–100 Hz), thresholded for significance at P<0.05.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychological and Brain Sciences, College of Liberal Arts and Sciences, University of Iowa, Iowa City, Iowa 52245, USA.

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.

No MeSH data available.


Related in: MedlinePlus