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Neural index of reinforcement learning predicts improved stimulus-response retention under high working memory load

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J Neurosci. 2023 Mar 16:JN-RM-1274-22. doi: 10.1523/JNEUROSCI.1274-22.2023. Online ahead of print.


Human learning and decision making is supported by multiple systems operating in parallel. Recent studies isolating the contributions of reinforcement learning (RL) and working memory (WM) have revealed a trade-off between the two. An interactive WM-RL computational model predicts that while high WM load slows behavioral acquisition, it also induces larger prediction errors in the RL system that enhance robustness and retention of learned behaviors. Here we tested this account by parametrically manipulating WM load during RL in conjunction with EEG, in both male and female participants, and administered two surprise memory tests. We further leveraged single trial decoding of EEG signatures of RL and WM to determine whether their interaction predicted robust retention. Consistent with the model, behavioral learning was slower for associations acquired under higher load but showed parametrically improved future retention. This paradoxical result was mirrored by EEG indices of RL, which were strengthened under higher WM loads and predictive of more robust future behavioral retention of learned stimulus-response contingencies. We further tested whether stress alters the ability to shift between the two systems strategically to maximize immediate learning versus retention of information and found that induced stress had only a limited effect on this trade-off. The present results offer a deeper understanding of the cooperative interaction between WM and RL and show that relying on WM can benefit the rapid acquisition of choice behavior during learning but impairs retention.SIGNIFICANCE STATEMENT:Successful learning is achieved by the joint contribution of the dopaminergic reinforcement learning (RL) system and working memory (WM). The cooperative WMRL model was productive in improving our understanding of the interplay between the two systems during learning, demonstrating that reliance on RL computations is modulated by WM load. However, the role of WM/RL systems in the retention of learned stimulus-response associations remained unestablished. Our results show that increased neural signatures of learning, indicative of greater RL computation, under high WM load also predicted better stimulus-response retention. This result supports a trade-off between the two systems, where degraded WM increases RL processing which improves retention. Notably, we show that this cooperative interplay remains largely unaffected by acute stress.

PMID:36931706 | DOI:10.1523/JNEUROSCI.1274-22.2023

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