Limits...
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

Source-level EEG results for the MS-IC WM task.(a) MS-IC ERSP following surprising versus standard tones in the WM task. Significant areas highlighted. The plot shows increased MS-IC activity for surprising tones in the WM task. (b) MS-IC single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted. (c) Mediation analysis. Areas in which ERSP significantly mediated surprise-related WM failures highlighted.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4837448&req=5

f4: Source-level EEG results for the MS-IC WM task.(a) MS-IC ERSP following surprising versus standard tones in the WM task. Significant areas highlighted. The plot shows increased MS-IC activity for surprising tones in the WM task. (b) MS-IC single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted. (c) Mediation analysis. Areas in which ERSP significantly mediated surprise-related WM failures highlighted.

Mentions: Following the MS-IC selection in each participant, we investigated its activity in the WM task. Hence, all the following analyses were performed on EEG source space, i.e., on independent component activity instead of scalp channel activity. We hypothesized, based on our prior study10 that the MS-ICs would be engaged following surprising events, indicated by increased 1–13 Hz activity within MS-ICs on surprising versus standard tones. This was indeed the case here (Fig. 4a). Hence, in line with our prior study10, we argue that the motor suppression process indexed by the MS-IC is active following surprising events (note that the MS-IC cannot reflect a process that is solely related to the surprise or infrequency of the tones, as it was identified based on its differential activity on successful versus failed stop trials in the SST. Stop-signals are not surprising, and successful and failed stop trials occur with equal frequency).


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)

Source-level EEG results for the MS-IC WM task.(a) MS-IC ERSP following surprising versus standard tones in the WM task. Significant areas highlighted. The plot shows increased MS-IC activity for surprising tones in the WM task. (b) MS-IC single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted. (c) Mediation analysis. Areas in which ERSP significantly mediated surprise-related WM failures highlighted.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: Source-level EEG results for the MS-IC WM task.(a) MS-IC ERSP following surprising versus standard tones in the WM task. Significant areas highlighted. The plot shows increased MS-IC activity for surprising tones in the WM task. (b) MS-IC single-trial GLM results from the WM task; group-average of the SURPRISE × WM interaction. Significant areas highlighted. (c) Mediation analysis. Areas in which ERSP significantly mediated surprise-related WM failures highlighted.
Mentions: Following the MS-IC selection in each participant, we investigated its activity in the WM task. Hence, all the following analyses were performed on EEG source space, i.e., on independent component activity instead of scalp channel activity. We hypothesized, based on our prior study10 that the MS-ICs would be engaged following surprising events, indicated by increased 1–13 Hz activity within MS-ICs on surprising versus standard tones. This was indeed the case here (Fig. 4a). Hence, in line with our prior study10, we argue that the motor suppression process indexed by the MS-IC is active following surprising events (note that the MS-IC cannot reflect a process that is solely related to the surprise or infrequency of the tones, as it was identified based on its differential activity on successful versus failed stop trials in the SST. Stop-signals are not surprising, and successful and failed stop trials occur with equal frequency).

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