Low lifetime stress exposure is associated with reduced stimulus-response memory

Abstract

Exposure to stress throughout life can cumulatively influence later health, even among young adults. The negative effects of high cumulative stress exposure are well-known, and a shift from episodic to stimulus-response memory has been proposed to underlie forms of psychopathology that are related to high lifetime stress. At the other extreme, effects of very low stress exposure are mixed, with some studies reporting that low stress leads to better outcomes, while others demonstrate that low stress is associated with diminished resilience and negative outcomes. However, the influence of very low lifetime stress exposure on episodic and stimulus-response memory is unknown. Here we use a lifetime stress assessment system (STRAIN) to assess cumulative lifetime stress exposure and measure memory performance in young adults reporting very low and moderate levels of lifetime stress exposure. Relative to moderate levels of stress, very low levels of lifetime stress were associated with reduced use and retention (24 h later) of stimulus-response (SR) associations, and a higher likelihood of using context memory. Further, computational modeling revealed that participants with low levels of stress exhibited worse expression of memory for SR associations than those with moderate stress. These results demonstrate that very low levels of stress exposure can have negative effects on cognition.

Figure 1.

Search task to measure multiple memory systems. During the search phase (left), participants implicitly learned associations with mnemonic cues that could help them respond to the target. On contextually cued (CC) trials, repeated spatial patterns provided a cue for the location of the target. On stimulus–response (SR) trials, the color probabilistically cued the approximate target location and motor response. During the probe test (right), the two mnemonic cues were combined, each predicting a distinct target location and motor response.

Figure 2.

Proportion of participants choosing context or stimulus–response cued target during the first trial of the probe test. More Moderate Stress participants chose the target cued by the stimulus–response association, whereas more Low Stress participants chose the target cued by the context association.

Figure 3.

Search task performance. (A) Learning during the search task on Day 1 (Epoch 1–6) and retention on Day 2 (Epoch 7–8) for Low Stress (left) and Moderate Stress (right) participants. (B) Memory-guided search during the end of Day 1 (left) and Day 2 (right). Positive values indicate faster reaction time (RT) when using a memory cue compared with no memory cue. (***) P < 0.001; (**) P < 0.01; (*) P < 0.05. (C) STRAIN variables predict SR performance during learning (left) and retention (right). Severity of acute stressors negatively correlated with SR performance in Low Stress participants during learning and retention. Full list of predictive STRAIN variables in Supplemental Table S2. (CC) Contextually cued, (SR) stimulus–response cue, (LS) Low Stress, (MS) Moderate Stress.

Figure 4.

Computational model of visual search performance. (A) Model estimates (lines) and actual reaction time data (open circles) are shown for Moderate Stress (left) and Low Stress (right) participants, per block of search during Day 1. (B) Derived estimates of model parameter values for Moderate Stress (left) participants are shown, along with any change in these parameters that was necessary to describe Low Stress participants (right). Error bars represent 95% confidence intervals. When the range indicated by these bars does not include zero, this estimate is significantly different from zero. The only change parameter that differed from zero was β_SR. All parameters described in Supplemental Text.