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Neural correlates of proactive and reactive inhibition of saccadic eye movements

Abstract

Although research on goal-directed, proactive inhibitory control (IC) and stimulus-driven, reactive IC is growing, no previous study has compared proactive IC in conditions of uncertainty with regard to upcoming inhibition to conditions of certain upcoming IC. Therefore, we investigated effects of certainty and uncertainty on behavior and blood oxygen level dependent (BOLD) signal in proactive and reactive IC. In two studies, healthy adults performed saccadic go/no-go and prosaccade/antisaccade tasks. The certainty manipulation had a highly significant behavioral effect in both studies, with inhibitory control being more successful under certain than uncertain conditions on both tasks (p ≤ 0.001). Saccadic go responses were significantly less efficient under conditions of uncertainty than certain responding (p < 0.001). Event-related functional magnetic resonance imaging (fMRI) (one study) revealed a dissociation of certainty- and uncertainty-related proactive inhibitory neural correlates in the go/no-go task, with lateral and medial prefrontal and occipital cortex showing stronger deactivations during uncertainty than during certain upcoming inhibition, and lateral parietal cortex being activated more strongly during certain upcoming inhibition than uncertainty or certain upcoming responding. In the antisaccade task, proactive BOLD effects arose due to stronger deactivations in uncertain response conditions of both tasks and before certain prosaccades than antisaccades. Reactive inhibition-related BOLD increases occurred in inferior parietal cortex and supramarginal gyrus (SMG) in the go/no-go task only. Proactive IC may imply focusing attention on the external environment for encoding salient or alerting events as well as inhibitory mechanisms that reduce potentially distracting neural processes. SMG and inferior parietal cortex may play an important role in both proactive and reactive IC of saccades.

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Notes

  1. 1.

    An anecdotal scenario illustrates the concept of proactive inhibition in no-go and antisaccade situations as they were assessed in the current study. No-go scenario: Imagine you are talking to a friend at a party, facing him, with the door into the room on your left side and the buffet on the right side. Suddenly, he says to you “oh my god, you won’t like who is about to come in. Do not look towards the door. Just keep looking at me whilst I continue talking...”. Antisaccade scenario: In a variant of this conversation, he might say “oh my god, you won’t like who is about to come in. When I give you a sign, just look over towards the buffet and pretend you are going to get another drink...”. It should become apparent from both scenarios that the friend’s sudden instruction triggers proactive inhibitory demands required in this situation to intentionally avoid a glance towards the door.

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Acknowledgements

The authors would like to thank Bertalan Polner (Budapest University of Technology and Economics, Budapest) for his valuable contribution to a pilot of this study.

Funding

This study was funded by the DFG (Et 31/2–1).

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Correspondence to Ulrich Ettinger.

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The study was approved by the ethics committee of the Department of Psychology at the University of Bonn and conducted in conformity with the Declaration of Helsinki.

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The authors declare no conflict of interest.

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All participants gave informed consent before participating in the study.

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Talanow, T., Kasparbauer, A., Lippold, J.V. et al. Neural correlates of proactive and reactive inhibition of saccadic eye movements. Brain Imaging and Behavior 14, 72–88 (2020). https://doi.org/10.1007/s11682-018-9972-3

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Keywords

  • Proactive inhibition
  • Eye movements
  • Antisaccade task
  • Go/no-go task
  • Event-related fMRI
  • Reactive inhibition
  • Go/no-go
  • Antisaccade
  • Eye tracking
  • fMRI