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

Thomas Maran,Marco Furtner,Barbara Weber,Pierre Sachse,Stefan Zuggal,Markus Martini,Jakob Pinggera

doi:10.3389/fnbeh.2017.00206

Abstract

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.

Highlights

Cognitive adaptations during high arousal states play an important role in models of development of psychopathology, e.g., post-traumatic stress disorder or phobias (Acheson et al, 2012; Pitman et al, 2012; de Quervain et al, 2017), shooting decisions during police actions (Nieuwenhuys et al, 2015), implementation of military operations on the battlefield (Lieberman et al, 2016) and forensic considerations in the face of crimes committed in rage (Brookman, 2015)
Whereas pupillary response did not differ between high arousal groups, ∆ = 0.01, SE = 0.02, Bonferroni-adjusted p = 1, compared to the neutral group, relative pupil size was higher for both the aversive group with a difference of 0.04 (SE = 0.01), Bonferroni-adjusted p = 0.017, and in the appetitive group with a difference of 0.03 (SE = 0.01), Bonferroni-adjusted p = 0.033
Absolute pupil response differed across arousal conditions, F(2,24) = 10.63, MSE = 0.012 p < 0.001, ηP2art = 0.47, BF10 = 51.29

Summary

Introduction

Cognitive adaptations during high arousal states play an important role in models of development of psychopathology, e.g., post-traumatic stress disorder or phobias (Acheson et al, 2012; Pitman et al, 2012; de Quervain et al, 2017), shooting decisions during police actions (Nieuwenhuys et al, 2015), implementation of military operations on the battlefield (Lieberman et al, 2016) and forensic considerations in the face of crimes committed in rage (Brookman, 2015). Encoding and/or retrieval of both types of context information have been shown to strongly rely on a single hippocampusand prefrontal cortex-dependent memory system (Rajah et al, 2010a,b, 2011; Kraus et al, 2013; Cabral et al, 2014) This network is supposed to support the construction of a schematic model of a situation based on contextual information (Bar, 2004; Ranganath and Ritchey, 2012), such as spatial and temporal relationships, it is required to form contextualized, detailed representations of events and for allocentric spatial navigation (Squire et al, 2004; Howard and Eichenbaum, 2013; Pezzulo et al, 2014; Davachi and DuBrow, 2015). This narrowed focus on the essential core of experiences lacking contextual embeddedness and depth of detail is reflected by an increased rate of false alarms (Payne et al, 2002) and is directly related to autonomic arousal (Qin et al, 2012)

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