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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

Behavioural task details and results.(a) WM task diagram. (b) Stop-signal task diagram. (c) WM task, behavioural data from the behavioural experiment. Left panel: WM accuracy by trial type. WM accuracy is reduced following surprising compared with standard tones (paired samples t-test, N=20, t(19)=3.5, P=0.0026 , d=0.78). Right panel: Bayesian surprise values of surprising trials split by WM accuracy. Surprise is increased for tones that interrupted WM (paired samples t-test, N=20, t(19)=2.14, P=0.045, d=0.77). Error bars denote s.e.m. (d) WM task, behavioural data from the scalp-EEG experiment, description as in c (WM accuracy: paired samples t-test, N=20, t(19)=2.3, P=0.033 , d=0.49; increased surprise for failed WM: paired samples t-test, N=20, t(19)=2.6, P=0.019, d=0.91).
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f1: Behavioural task details and results.(a) WM task diagram. (b) Stop-signal task diagram. (c) WM task, behavioural data from the behavioural experiment. Left panel: WM accuracy by trial type. WM accuracy is reduced following surprising compared with standard tones (paired samples t-test, N=20, t(19)=3.5, P=0.0026 , d=0.78). Right panel: Bayesian surprise values of surprising trials split by WM accuracy. Surprise is increased for tones that interrupted WM (paired samples t-test, N=20, t(19)=2.14, P=0.045, d=0.77). Error bars denote s.e.m. (d) WM task, behavioural data from the scalp-EEG experiment, description as in c (WM accuracy: paired samples t-test, N=20, t(19)=2.3, P=0.033 , d=0.49; increased surprise for failed WM: paired samples t-test, N=20, t(19)=2.6, P=0.019, d=0.91).

Mentions: To test this hypothesis, we developed a task in which WM maintenance was occasionally interrupted by surprising events (Fig. 1a). On each trial, participants encoded a string of consonants into WM, maintained it across a delay, and were then tested with a probe. Importantly, the WM probe was preceded by a sound. On 80% of trials, a standard sine-wave tone was played, with which the participants were familiar from practicing the task before the main experiment. However, in 20% of trials of the main experiment, a surprising birdsong segment was played instead of the standard tone. Behaviourally, we predicted that WM accuracy would be reduced following surprising tones. We further predicted that tones leading to WM failures would be more surprising than tones that were followed by correct WM probes.


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)

Behavioural task details and results.(a) WM task diagram. (b) Stop-signal task diagram. (c) WM task, behavioural data from the behavioural experiment. Left panel: WM accuracy by trial type. WM accuracy is reduced following surprising compared with standard tones (paired samples t-test, N=20, t(19)=3.5, P=0.0026 , d=0.78). Right panel: Bayesian surprise values of surprising trials split by WM accuracy. Surprise is increased for tones that interrupted WM (paired samples t-test, N=20, t(19)=2.14, P=0.045, d=0.77). Error bars denote s.e.m. (d) WM task, behavioural data from the scalp-EEG experiment, description as in c (WM accuracy: paired samples t-test, N=20, t(19)=2.3, P=0.033 , d=0.49; increased surprise for failed WM: paired samples t-test, N=20, t(19)=2.6, P=0.019, d=0.91).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: Behavioural task details and results.(a) WM task diagram. (b) Stop-signal task diagram. (c) WM task, behavioural data from the behavioural experiment. Left panel: WM accuracy by trial type. WM accuracy is reduced following surprising compared with standard tones (paired samples t-test, N=20, t(19)=3.5, P=0.0026 , d=0.78). Right panel: Bayesian surprise values of surprising trials split by WM accuracy. Surprise is increased for tones that interrupted WM (paired samples t-test, N=20, t(19)=2.14, P=0.045, d=0.77). Error bars denote s.e.m. (d) WM task, behavioural data from the scalp-EEG experiment, description as in c (WM accuracy: paired samples t-test, N=20, t(19)=2.3, P=0.033 , d=0.49; increased surprise for failed WM: paired samples t-test, N=20, t(19)=2.6, P=0.019, d=0.91).
Mentions: To test this hypothesis, we developed a task in which WM maintenance was occasionally interrupted by surprising events (Fig. 1a). On each trial, participants encoded a string of consonants into WM, maintained it across a delay, and were then tested with a probe. Importantly, the WM probe was preceded by a sound. On 80% of trials, a standard sine-wave tone was played, with which the participants were familiar from practicing the task before the main experiment. However, in 20% of trials of the main experiment, a surprising birdsong segment was played instead of the standard tone. Behaviourally, we predicted that WM accuracy would be reduced following surprising tones. We further predicted that tones leading to WM failures would be more surprising than tones that were followed by correct WM probes.

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