The neural basis of improved cognitive performance by threat of shock

Abstract

Anxiety can have both detrimental and facilitatory cognitive effects. This study investigates the neural substrates of a replicated facilitatory effect of anxiety on sustained attention and response inhibition. This effect consisted of improved performance on the Sustained Attention to Response Task (a Go-NoGo task consisting of 91% Go and 9% NoGo trials) in threat (unpredictable electrical shock) vs safe (no shock) conditions. This study uses the same experimental design with fMRI and relies on an event-related analysis of BOLD signal changes. Findings reveal that threat-related cognitive facilitation (improved NoGo accuracy) is associated with greater activation of a right-lateralized frontoparietal group of regions previously implicated in sustained attention and response inhibition. Moreover, these same regions show decreased activation in the Go trials preceding NoGo errors. During NoGo trials, striatal activity is also greater in the threat vs safe condition, consistent with the notion of enhanced inhibitory processing under threat. These findings identify potential mechanisms by which threat of unpredictable shock can facilitate distinct cognitive functions. A greater understanding of the complex interaction of the anxious state and cognitive processes may have critical clinical implications.

Towards an emotional ‘stress test’: a reliable, non-subjective cognitive measure of anxious responding

“…This improvement in accuracy replicates previous studies58 and an increase in reaction time under threat of shock replicates a line of previous research (see preprint and data*).…”

“…The impact of threat of shock on accuracy has been confirmed in numerous studies, improving accuracy to distractor stimuli5 and impairing accuracy to target stimuli7, but its test-retest reliability is unknown. The impact on reaction time is less clear; in some cases there are no effects58 whilst in a modified version of the SART an increase in reaction time was evidenced (see preprint and data doi:10.7287/PEERJ.PREPRINTS.1542V1).…”

Worry alters speed-accuracy tradeoffs but does not impair sustained attention

“…Beyond testing and accounting for tradeoffs, future research would benefit from explicitly characterizing these tradeoffs and their mechanisms in relation to worry and anxiety in their own right. Future research should also dissociate relative contributions of state anxiety, which has been reliably linked to enhanced response inhibition in threat-of-shock research (Grillon et al, 2016;Torrisi et al, 2016), from potential adverse consequences of distraction by worry-related thoughts.…”

The ‘Threat of Scream’ paradigm: A tool for studying sustained physiological and subjective anxiety

“…Given the ubiquity and persistence of anxiety disorders, as well as their massive impact upon quality of life (Leon, Portera, & Weissman, 1995), it is essential that neurobiologists and clinicians determine how anxiety influences human brain physiology and behavioural responses to stress or external threats, along the continuum from normal to pathological conditions. While high anxiety leads to exaggerated estimates of threat probability, a certain level of anxiety is crucial for an organism's survival because it ensures optimal sensitivity and decisiveness in the face of possible threat (Bateson, Brilot, & Nettle, 2011;Grillon, 2008;Marks & Nesse, 1994) The predictability of threats appears to be a major determinant of anxiety-related bodily manifestations, such as modulations of heart rate, startle reflex or skin conductance (Alvarez, Chen, Bodurka, Kaplan, & Grillon, 2011;Davis, Walker, Miles, & Grillon, 2010;Torrisi et al, 2016;Vansteenwegen, Iberico, Vervliet, Marescau, & Hermans, 2008). Indeed, predictable threats lead to phasic and acute fear responses that are directly associated with the appearance of a threat, e.g.…”

“…Such on-off alternations allow to manipulate the state of anxiety within subject as each participant can serve as her/his own control. The TOS paradigm proved to be a reliable method for inducing sustained anxiety, as reflected in participants' physiological (startle reflex and elevated tonic skin conductance level) and psychological (higher reports of subjective anxiety) responses during threat versus safe blocks (Bradley, Zlatar, & Lang, 2017;Grillon, Robinson, Mathur, & Ernst, 2016;Hubbard et al, 2011;Torrisi et al, 2016) Yet, and just like every paradigm, TOS has limitations. First, it is not clear whether it can induce sustained anxiety responses for long durations.…”