Stress-induced bias of multiple memory systems during retrieval depends on training intensity

Abstract

Stressful events promote a shift from hippocampus-dependent ‘cognitive’ learning towards dorsal striatum-dependent ‘habit’ learning. Beyond modulating the recruitment of multiple memory systems during learning, recent evidence suggests that stress may also affect which of these memory systems is employed during retrieval, thereby affecting the nature of remembering. However, while some studies reported increased reliance on ‘habit’ memory retrieval after stress, other studies suggested even a bias towards ‘cognitive’ memory retrieval after stress. In the present experiment, we tested the hypothesis that the nature of the stress effect on the control of memory retrieval depends on the extent of initial training. To this end, participants completed a probabilistic classification learning (PCL) task that can be solved by both the ‘cognitive’ and the ‘habit’ memory systems, which is reflected in the engagement of specific behavioral strategies. Critically, participants received either moderate (100 trials) or intensive (200 trials) training in the PCL task. Participants then underwent a stress protocol or a non-stressful control procedure, before they completed a retrieval version of the PCL task. The effectiveness of the stress manipulation was verified by increases in salivary cortisol and autonomic arousal. Our results further revealed that participants who received moderate training showed, during retrieval, a stress-induced shift towards strategies indicative of the dorsal striatal ‘habit’ memory system. After prolonged training, however, stress did not affect which memory system guided retrieval. The present results indicate that the effect of stress on the engagement of multiple memory systems during retrieval is critically dependent on the extent of initial training and, by inference, on the strength of the multiple memory traces established during learning.