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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

Source-level EEG results for the stop-signal task.(a) ERP back projection into channel space at component's centre of gravity. Inset: average topographical IC projection in channel space (rectified to show positive at FCz). (b) MS-IC ERP onset on successful and failed stop trials. Points represent participants. Four participants had no significant P3-ERP on failed stop trials (i.e., plot shows N=16). Points below the grey identity line demarcate participants whose MS-IC onset was earlier on successful compared to failed stop-signals (paired samples t-test, N=16, t(15)=3.62, P=0.003, d=0.77), which illustrates the relation of the MS-IC EEG activity to the speed of stopping. (c) Correlation between MC-IC ERP onset on successful stop trials and SSRT in N=20. Dashed line denotes least squares fit (r=0.36, P=0.06).
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f3: Source-level EEG results for the stop-signal task.(a) ERP back projection into channel space at component's centre of gravity. Inset: average topographical IC projection in channel space (rectified to show positive at FCz). (b) MS-IC ERP onset on successful and failed stop trials. Points represent participants. Four participants had no significant P3-ERP on failed stop trials (i.e., plot shows N=16). Points below the grey identity line demarcate participants whose MS-IC onset was earlier on successful compared to failed stop-signals (paired samples t-test, N=16, t(15)=3.62, P=0.003, d=0.77), which illustrates the relation of the MS-IC EEG activity to the speed of stopping. (c) Correlation between MC-IC ERP onset on successful stop trials and SSRT in N=20. Dashed line denotes least squares fit (r=0.36, P=0.06).

Mentions: To apply this logic to our data set, we identified one source-level IC for each participant that represented the fronto-central P3-ERP (event-related potential) induced by the stop signal in the SST (see Supplementary Fig. 1 for complete ERP plots). Prior research has shown that this ERP specifically indexes the motor suppression process in the SST: its onset occurs in the precise time window when motor suppression is implemented30, correlates strongly with the speed of stopping (a large sample of N=62 revealed correlations between P3 onset and SSRT in excess of r >0.618), and occurs earlier on trials on which stopping is successful1831. Furthermore, the neural generators of this fronto-central component have been shown to be independent of other neural processes that are involved in the stop-signal task, such as those that reflect the attentional detection of the stop signal19. We selected one IC per subject that reflected this ERP (see Methods section), which we denote the MS-IC. To validate our MS-IC selection, we ensured that the onset of these selected source-level MS-ICs in our current data set showed the same tight relation to the success of stopping as prior studies (Fig. 3). Indeed, in line with prior studies1831, the onset of the MS-IC P3-ERP occurred significantly earlier on successful stop trials compared with failed stop trials (paired samples t-test, N=16, t(15)=3.62, P=0.003, d=0.77, Fig. 3b), and was positively correlated with SSRT across participants (r=0.36, P=0.06, one-sided, Fig. 3c; outliers were diagnosed based on Cook's d>1, no outliers were present in the sample).


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 stop-signal task.(a) ERP back projection into channel space at component's centre of gravity. Inset: average topographical IC projection in channel space (rectified to show positive at FCz). (b) MS-IC ERP onset on successful and failed stop trials. Points represent participants. Four participants had no significant P3-ERP on failed stop trials (i.e., plot shows N=16). Points below the grey identity line demarcate participants whose MS-IC onset was earlier on successful compared to failed stop-signals (paired samples t-test, N=16, t(15)=3.62, P=0.003, d=0.77), which illustrates the relation of the MS-IC EEG activity to the speed of stopping. (c) Correlation between MC-IC ERP onset on successful stop trials and SSRT in N=20. Dashed line denotes least squares fit (r=0.36, P=0.06).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4837448&req=5

f3: Source-level EEG results for the stop-signal task.(a) ERP back projection into channel space at component's centre of gravity. Inset: average topographical IC projection in channel space (rectified to show positive at FCz). (b) MS-IC ERP onset on successful and failed stop trials. Points represent participants. Four participants had no significant P3-ERP on failed stop trials (i.e., plot shows N=16). Points below the grey identity line demarcate participants whose MS-IC onset was earlier on successful compared to failed stop-signals (paired samples t-test, N=16, t(15)=3.62, P=0.003, d=0.77), which illustrates the relation of the MS-IC EEG activity to the speed of stopping. (c) Correlation between MC-IC ERP onset on successful stop trials and SSRT in N=20. Dashed line denotes least squares fit (r=0.36, P=0.06).
Mentions: To apply this logic to our data set, we identified one source-level IC for each participant that represented the fronto-central P3-ERP (event-related potential) induced by the stop signal in the SST (see Supplementary Fig. 1 for complete ERP plots). Prior research has shown that this ERP specifically indexes the motor suppression process in the SST: its onset occurs in the precise time window when motor suppression is implemented30, correlates strongly with the speed of stopping (a large sample of N=62 revealed correlations between P3 onset and SSRT in excess of r >0.618), and occurs earlier on trials on which stopping is successful1831. Furthermore, the neural generators of this fronto-central component have been shown to be independent of other neural processes that are involved in the stop-signal task, such as those that reflect the attentional detection of the stop signal19. We selected one IC per subject that reflected this ERP (see Methods section), which we denote the MS-IC. To validate our MS-IC selection, we ensured that the onset of these selected source-level MS-ICs in our current data set showed the same tight relation to the success of stopping as prior studies (Fig. 3). Indeed, in line with prior studies1831, the onset of the MS-IC P3-ERP occurred significantly earlier on successful stop trials compared with failed stop trials (paired samples t-test, N=16, t(15)=3.62, P=0.003, d=0.77, Fig. 3b), and was positively correlated with SSRT across participants (r=0.36, P=0.06, one-sided, Fig. 3c; outliers were diagnosed based on Cook's d>1, no outliers were present in the sample).

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