Reward enhances memory via age-varying online and offline neural mechanisms across development

Abstract

Reward motivation enhances memory through interactions between mesolimbic, hippocampal, and cortical systems - both during and after encoding. Developmental changes in these distributed neural circuits may lead to age-related differences in reward-motivated memory and the underlying neural mechanisms. Converging evidence from cross-species studies suggests that subcortical dopamine signaling is increased during adolescence, which may lead to stronger memory representations of rewarding, relative to mundane, events and changes in the contributions of underlying subcortical and cortical brain mechanisms across age. Here, we used fMRI to examine how reward motivation influences the "online" encoding and "offline" post-encoding brain mechanisms that support long-term associative memory from childhood to adulthood. We found that reward motivation led to both age-invariant as well as adolescent-specific enhancements in associative memory after 24 hours. Furthermore, reward-related memory benefits were linked to age-varying neural mechanisms. During encoding, interactions between the prefrontal cortex and ventral tegmental area (VTA) were associated with better high-reward memory to a greater degree with increasing age. Pre- to post-encoding changes in functional connectivity between the anterior hippocampus and VTA were also associated with better high-reward memory, but more so at younger ages. Our findings suggest that there may be developmental shifts - from offline subcortical to online cortical processes - in the brain mechanisms supporting reward-motivated memory.

Curiosity-Motivated Incidental Learning With And Without Incentives: Early Consolidation And Midbrain-Hippocampal Resting-State Functional Connectivity

“…Overall, our results add to previous findings showing that individual differences in systems-level interactions differentially or selectively predict high-reward memory, in comparison to low-reward memory, where these effects were interpreted in light of a selective stabilisation of high-value memories (Cohen et al, 2021; Gruber et al, 2016; Murty et al, 2017). Other studies (Cohen et al, 2021; Gruber et al, 2016; Murty et al, 2017) investigating consolidation processes supporting memories for high-value information have manipulated value (i.e., incentives for intentional encoding or rewards in an unrelated task during incidental encoding) using within-subject manipulations. On the other hand, our study used a between-subject manipulation where half of the participants were informed that correct responses would be associated with additional monetary bonus payments.…”

“…The authors showed that in the absence of an overall increase in RSFC between HPC and midbrain from pre- to post-learning rest, individual differences therein positively predicted the reward-driven associative memory effect. That interindividual differences in changes in RSFC between HPC and midbrain can predict later associative memory for information presented in high-reward contexts was recently replicated in an intentional encoding paradigm with a memory test after 24h (Cohen et al, 2021). In sum, the results provide evidence that monetary rewards influence neural post-encoding processes supporting the preferred consolidation of stimuli associated with rewards.…”

“…As such, stimuli that elicit curiosity can have a motivational salience within their own merit that can be similar to that found in the context of extrinsic incentives and rewards (FitzGibbon et al, 2020; Lau et al, 2020). Given previous studies showing that aHPC-VTA/SN-RSFC change supports memory for motivationally salient events in the context of extrinsic rewards (Cohen et al, 2021; Gruber et al, 2016), and proposals that extrinsic rewards and curiosity share features of incentive salience (FitzGibbon et al, 2020; Lau et al, 2020), it is tempting to predict that curiosity- and reward-motivated learning would use similar neural post-encoding mechanisms. However, we did not find that aHPC-VTA/SN-RSFC change predicted curiosity-driven memory benefit, neither across the whole sample nor within each group separately.…”

“…Due to the established roles of HPC and VTA/SN as well as their connectivity in motivated learning in the context of incentives and curiosity have previously been established (Adcock et al, 2006;Cohen et al, 2021;Gruber et al, 2014Gruber et al, , 2016Kahn & Shohamy, 2013;Murty & Adcock, 2014;Poh et al, 2021;Wolosin et al, 2012), we aimed to determine how their FC during post-encoding rest predicts behavioural measures of learning. Because evidence suggests that activity during encoding and consolidation in support of remembering is predominantly centred in anterior parts of the HPC (Kim, 2011;Murty et al, 2017;Spaniol et al, 2009), the analysis focused on the aHPC and the same masks were used as described in previous work (Meliss, van Reekum, et al, 2022).…”