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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

EEG analysis schematic.The combined EEG from the WM task and the SST were subjected to ICA. One IC that represented the process underlying successful stopping in the SST was selected per subject. The activity of that component in the WM task was then analysed in three separate ways: by showing that its activity was increased following surprising tones in the WM task, by showing that its activity was correlated with the trial-by-trial effects of surprise on WM accuracy, and by showing that its activity positively mediated between the surprise of the tone and accuracy on the WM probe.
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f2: EEG analysis schematic.The combined EEG from the WM task and the SST were subjected to ICA. One IC that represented the process underlying successful stopping in the SST was selected per subject. The activity of that component in the WM task was then analysed in three separate ways: by showing that its activity was increased following surprising tones in the WM task, by showing that its activity was correlated with the trial-by-trial effects of surprise on WM accuracy, and by showing that its activity positively mediated between the surprise of the tone and accuracy on the WM probe.

Mentions: In this experiment, we specifically used independent component analysis (ICA) to identify the brain source signal component that indexes successful motor stopping in the SST. For present purposes, we call this the ‘motor suppression-independent component' (MS-IC). We then aimed to investigate the activity of this MS-IC in the WM task. To achieve this, we computed an ICA on each participant's combined EEG from both tasks (Fig. 2). ICA decomposes the scalp-EEG mixture into its underlying independent source signal components (ICs), each of which represents an independent neural process that contributes to the scalp-EEG mixture24.


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)

EEG analysis schematic.The combined EEG from the WM task and the SST were subjected to ICA. One IC that represented the process underlying successful stopping in the SST was selected per subject. The activity of that component in the WM task was then analysed in three separate ways: by showing that its activity was increased following surprising tones in the WM task, by showing that its activity was correlated with the trial-by-trial effects of surprise on WM accuracy, and by showing that its activity positively mediated between the surprise of the tone and accuracy on the WM probe.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: EEG analysis schematic.The combined EEG from the WM task and the SST were subjected to ICA. One IC that represented the process underlying successful stopping in the SST was selected per subject. The activity of that component in the WM task was then analysed in three separate ways: by showing that its activity was increased following surprising tones in the WM task, by showing that its activity was correlated with the trial-by-trial effects of surprise on WM accuracy, and by showing that its activity positively mediated between the surprise of the tone and accuracy on the WM probe.
Mentions: In this experiment, we specifically used independent component analysis (ICA) to identify the brain source signal component that indexes successful motor stopping in the SST. For present purposes, we call this the ‘motor suppression-independent component' (MS-IC). We then aimed to investigate the activity of this MS-IC in the WM task. To achieve this, we computed an ICA on each participant's combined EEG from both tasks (Fig. 2). ICA decomposes the scalp-EEG mixture into its underlying independent source signal components (ICs), each of which represents an independent neural process that contributes to the scalp-EEG mixture24.

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