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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 group results.(a) ERSP following surprising versus standard tones in the WM task. The plot shows increased MS-IC activity for surprising tones in the WM task. Significant areas highlighted. (b) Single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted.
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f5: STN group results.(a) ERSP following surprising versus standard tones in the WM task. The plot shows increased MS-IC activity for surprising tones in the WM task. Significant areas highlighted. (b) Single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted.

Mentions: We then analysed the LFP response in STN in the same way as the event-related spectral perturbation (ERSP) response of the MS-ICs in the scalp-EEG experiment, but with a broader frequency range (1–100 Hz), which included gamma activity. In line with our scalp-EEG results and our hypothesis, STN activity was increased following surprising events, notably in the delta (1–4 Hz), beta (13–30 Hz) and gamma (>30 Hz) frequency bands (Fig. 4a). The same single-subject GLM analysis as in the scalp-EEG experiment further showed that gamma-band activity was significantly related to the SURPRISE × WM interaction, just like the scalp MS-IC activity in the scalp-EEG experiment. Furthermore, single-subject plots (Fig. 5) show that each participant had significantly increased gamma-band activity in the STN following surprising tones (middle column of Fig. 5), and a significantly positive correlation with the SURPRISE × WM interaction (right column of Fig. 5). These results show that, just like the MS-IC scalp-EEG activity, LFP activity in the STN was significantly increased following surprising events. Furthermore and more importantly, just like the MS-IC scalp-EEG activity, LFP activity in the STN was significantly increased when stronger amounts of surprise lead to WM failure.


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 group results.(a) ERSP following surprising versus standard tones in the WM task. The plot shows increased MS-IC activity for surprising tones in the WM task. Significant areas highlighted. (b) Single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: STN group results.(a) ERSP following surprising versus standard tones in the WM task. The plot shows increased MS-IC activity for surprising tones in the WM task. Significant areas highlighted. (b) Single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted.
Mentions: We then analysed the LFP response in STN in the same way as the event-related spectral perturbation (ERSP) response of the MS-ICs in the scalp-EEG experiment, but with a broader frequency range (1–100 Hz), which included gamma activity. In line with our scalp-EEG results and our hypothesis, STN activity was increased following surprising events, notably in the delta (1–4 Hz), beta (13–30 Hz) and gamma (>30 Hz) frequency bands (Fig. 4a). The same single-subject GLM analysis as in the scalp-EEG experiment further showed that gamma-band activity was significantly related to the SURPRISE × WM interaction, just like the scalp MS-IC activity in the scalp-EEG experiment. Furthermore, single-subject plots (Fig. 5) show that each participant had significantly increased gamma-band activity in the STN following surprising tones (middle column of Fig. 5), and a significantly positive correlation with the SURPRISE × WM interaction (right column of Fig. 5). These results show that, just like the MS-IC scalp-EEG activity, LFP activity in the STN was significantly increased following surprising events. Furthermore and more importantly, just like the MS-IC scalp-EEG activity, LFP activity in the STN was significantly increased when stronger amounts of surprise lead to WM failure.

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