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Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information

Biased cognition during high arousal states is a relevant phenomenon in a variety of topics: from the development of post-traumatic stress disorders or stress-triggered addictive behaviors to forensic considerations regarding crimes of passion. Recent evidence indicates that arousal modulates the en...

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Autores principales: Maran, Thomas, Sachse, Pierre, Martini, Markus, Weber, Barbara, Pinggera, Jakob, Zuggal, Stefan, Furtner, Marco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5684831/
https://www.ncbi.nlm.nih.gov/pubmed/29170634
http://dx.doi.org/10.3389/fnbeh.2017.00206
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author Maran, Thomas
Sachse, Pierre
Martini, Markus
Weber, Barbara
Pinggera, Jakob
Zuggal, Stefan
Furtner, Marco
author_facet Maran, Thomas
Sachse, Pierre
Martini, Markus
Weber, Barbara
Pinggera, Jakob
Zuggal, Stefan
Furtner, Marco
author_sort Maran, Thomas
collection PubMed
description Biased cognition during high arousal states is a relevant phenomenon in a variety of topics: from the development of post-traumatic stress disorders or stress-triggered addictive behaviors to forensic considerations regarding crimes of passion. Recent evidence indicates that arousal modulates the engagement of a hippocampus-based “cognitive” system in favor of a striatum-based “habit” system in learning and memory, promoting a switch from flexible, contextualized to more rigid, reflexive responses. Existing findings appear inconsistent, therefore it is unclear whether and which type of context processing is disrupted by enhanced arousal. In this behavioral study, we investigated such arousal-triggered cognitive-state shifts in human subjects. We validated an arousal induction procedure (three experimental conditions: violent scene, erotic scene, neutral control scene) using pupillometry (Preliminary Experiment, n = 13) and randomly administered this method to healthy young adults to examine whether high arousal states affect performance in two core domains of contextual processing, the acquisition of spatial (spatial discrimination paradigm; Experiment 1, n = 66) and sequence information (learned irrelevance paradigm; Experiment 2, n = 84). In both paradigms, spatial location and sequences were encoded incidentally and both displacements when retrieving spatial position as well as the predictability of the target by a cue in sequence learning changed stepwise. Results showed that both implicit spatial and sequence learning were disrupted during high arousal states, regardless of valence. Compared to the control group, participants in the arousal conditions showed impaired discrimination of spatial positions and abolished learning of associative sequences. Furthermore, Bayesian analyses revealed evidence against the null models. In line with recent models of stress effects on cognition, both experiments provide evidence for decreased engagement of flexible, cognitive systems supporting encoding of context information in active cognition during acute arousal, promoting reduced sensitivity for contextual details. We argue that arousal fosters cognitive adaptation towards less demanding, more present-oriented information processing, which prioritizes a current behavioral response set at the cost of contextual cues. This transient state of behavioral perseverance might reduce reliance on context information in unpredictable environments and thus represent an adaptive response in certain situations.
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spelling pubmed-56848312017-11-23 Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information Maran, Thomas Sachse, Pierre Martini, Markus Weber, Barbara Pinggera, Jakob Zuggal, Stefan Furtner, Marco Front Behav Neurosci Neuroscience Biased cognition during high arousal states is a relevant phenomenon in a variety of topics: from the development of post-traumatic stress disorders or stress-triggered addictive behaviors to forensic considerations regarding crimes of passion. Recent evidence indicates that arousal modulates the engagement of a hippocampus-based “cognitive” system in favor of a striatum-based “habit” system in learning and memory, promoting a switch from flexible, contextualized to more rigid, reflexive responses. Existing findings appear inconsistent, therefore it is unclear whether and which type of context processing is disrupted by enhanced arousal. In this behavioral study, we investigated such arousal-triggered cognitive-state shifts in human subjects. We validated an arousal induction procedure (three experimental conditions: violent scene, erotic scene, neutral control scene) using pupillometry (Preliminary Experiment, n = 13) and randomly administered this method to healthy young adults to examine whether high arousal states affect performance in two core domains of contextual processing, the acquisition of spatial (spatial discrimination paradigm; Experiment 1, n = 66) and sequence information (learned irrelevance paradigm; Experiment 2, n = 84). In both paradigms, spatial location and sequences were encoded incidentally and both displacements when retrieving spatial position as well as the predictability of the target by a cue in sequence learning changed stepwise. Results showed that both implicit spatial and sequence learning were disrupted during high arousal states, regardless of valence. Compared to the control group, participants in the arousal conditions showed impaired discrimination of spatial positions and abolished learning of associative sequences. Furthermore, Bayesian analyses revealed evidence against the null models. In line with recent models of stress effects on cognition, both experiments provide evidence for decreased engagement of flexible, cognitive systems supporting encoding of context information in active cognition during acute arousal, promoting reduced sensitivity for contextual details. We argue that arousal fosters cognitive adaptation towards less demanding, more present-oriented information processing, which prioritizes a current behavioral response set at the cost of contextual cues. This transient state of behavioral perseverance might reduce reliance on context information in unpredictable environments and thus represent an adaptive response in certain situations. Frontiers Media S.A. 2017-11-09 /pmc/articles/PMC5684831/ /pubmed/29170634 http://dx.doi.org/10.3389/fnbeh.2017.00206 Text en Copyright © 2017 Maran, Sachse, Martini, Weber, Pinggera, Zuggal and Furtner. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Maran, Thomas
Sachse, Pierre
Martini, Markus
Weber, Barbara
Pinggera, Jakob
Zuggal, Stefan
Furtner, Marco
Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information
title Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information
title_full Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information
title_fullStr Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information
title_full_unstemmed Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information
title_short Lost in Time and Space: States of High Arousal Disrupt Implicit Acquisition of Spatial and Sequential Context Information
title_sort lost in time and space: states of high arousal disrupt implicit acquisition of spatial and sequential context information
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5684831/
https://www.ncbi.nlm.nih.gov/pubmed/29170634
http://dx.doi.org/10.3389/fnbeh.2017.00206
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