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

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.

Orexins and stress

“…Given that orexins promote arousal, and changes in arousal can modulate cognitive function (Maran et al, 2017; Packard and Goodman, 2012), these neuropeptides likely play an important role in cognition. In support of this, narcoleptic patients show specific cognitive impairments (Blackwell et al, 2017).…”

Pupil-based states of brain integration across cognitive states

“…The fluctuations of arousal within active wake states have been assessed by measuring baseline pupil size, a surrogate measure of arousal. Such studies have shown that baseline pupil size allows distinguishing active task solving versus mind wandering (Kristjansson et al, 2009;Smallwood et al, 2011;Unsworth & Robison, 2016van den Brink et al, 2016a), exploitation versus exploration states (Jepma & Nieuwenhuis, 2011;Murphy et al, 2011;Pajkossy et al, 2017), focused attention versus fatigue (Nishiyama et al, 2007) or stress (Maran et al, 2017), all of which may alternate even during the course of a task. In addition to studies in humans, animal studies have shown that states associated with different level of arousal during the wake state show different pupil signatures, as well as different signatures of activity at the neuronal level.…”

Dynamic arousal signals construct memories of time and events

“…First, like event boundaries, emotional stimuli or acute stressors that induce arousal elicit exaggerated estimates of time duration [23,24]. Second, viewing highly arousing videos prior to navigation or sequence learning has been shown to impair temporal order memory for neutral events [25][26][27]. Third, emotionally arousing stimuli also enhance local item-context source memory, at least when attention is directed towards relevant contextual information or when these details are intrinsic to the emotional stimulus [28][29][30][31].…”