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.

Trial registration: ClinicalTrials.gov NCT00047853.

Keywords: Go/NoGo; fMRI; response inhibition; sustained attention; threat of shock.

Published by Oxford University Press 2016. This work is written by US Government employees and is in the public domain in the United States.

Figures

Fig. 1.

Percent accuracy within trial type and condition. Error bars = s.e.m.

Fig. 2.

All Go trials, in a Threat vs Safe contrast. Maps corrected at T > ±3.65, P < 0.001, k = 13, N = 31. Results in this and subsequent figures are overlaid on an average of all subject’s normalized structural scans. Numbers represent Z levels in Talairach space. See also Table 1A.

Fig. 3.

(A) Four trials prior to EoC vs four trials prior to correct NoGos across conditions (safe and threat). From left to right: less activation in right ventrolateral PFC, MFG and right IPL (arrows). See Table 1B for additional regions. N = 29. Coloring and thresholding of statistics are the same as in Figure 2. (B) Regression coefficients for Go trials just previous to either correct or incorrect NoGos. Beta coefficients are averaged between the three regions highlighted at left, and separated by condition (safe: blue, threat: red) and type of NoGo accuracy they precede. Error bars = s.e.m.

Fig. 4.

All correct NoGo trials, in a Threat vs Safe contrast. N = 31. (A) VTA and putamen. (B) Betas from regions, red = under threat, blue = safe from threat. See also Table 1C.

Fig. 5.

Right MFG beta coefficients from correct Go trials in Threat vs Safe contrast and correlated with subjective report of anxiety during threat blocks. r = 0.55, P = 0.0014.