Stress potentiates early and attenuates late stages of visual processing

Abstract

Stress can fundamentally alter neural responses to incoming information. Recent research suggests that stress and anxiety shift the balance of attention away from a task-directed mode, governed by prefrontal cortex, to a sensory-vigilance mode, governed by the amygdala and other threat-sensitive regions. A key untested prediction of this framework is that stress exerts dissociable effects on different stages of information processing. This study exploited the temporal resolution afforded by event-related potentials to disentangle the impact of stress on vigilance, indexed by early perceptual activity, from its impact on task-directed cognition, indexed by later postperceptual activity in humans. Results indicated that threat of shock amplified stress, measured using retrospective ratings and concurrent facial electromyography. Stress also double-dissociated early sensory-specific processing from later task-directed processing of emotionally neutral stimuli: stress amplified N1 (184-236 ms) and attenuated P3 (316-488 ms) activity. This demonstrates that stress can have strikingly different consequences at different processing stages. Consistent with recent suggestions, stress amplified earlier extrastriate activity in a manner consistent with vigilance for threat (N1), but disrupted later activity associated with the evaluation of task-relevant information (P3). These results provide a novel basis for understanding how stress can modulate information processing in everyday life and stress-sensitive disorders.

Figure 1.

Stress double-dissociated earlier from later task-evoked GFP (SD μV). Threat amplified the N1 (184–236 ms) and attenuated the P3 (316–488 ms), without substantially altering the P1 (112–144 ms). Confidence bars indicate the probability of the null hypothesis being rejected by chance; non-overlapping bars indicate p < 0.05 (Shackman et al., 2010).

Figure 2.

Stress amplified early perceptual processing (N1) and attenuated subsequent postperceptual processing (P3). The N1 and P3 components are shown in A and B, respectively. Three-dimensional topographic maps depict the thresholded threat versus safe contrast (uncorrected p < 0.05, corrected p < 0.10). Two-dimensional topographic maps depict the voltage for each condition. Results are shown for the average reference.

Figure 3.

Greater attenuation of the P3 at right-frontal electrodes predicted reduced task performance. Mean P3 activity in this cluster was attenuated under threat, depicted in the three-dimensional topographic map. Individuals showing greater P3 attenuation in this cluster exhibited worse performance on the discrimination task, indexed by increased RT, ρ = 0.45. The joint test was significant, p = 0.02.