Selectivity in Postencoding Connectivity with High-Level Visual Cortex Is Associated with Reward-Motivated Memory

Abstract

Reward motivation has been demonstrated to enhance declarative memory by facilitating systems-level consolidation. Although high-reward information is often intermixed with lower reward information during an experience, memory for high value information is prioritized. How is this selectivity achieved? One possibility is that postencoding consolidation processes bias memory strengthening to those representations associated with higher reward. To test this hypothesis, we investigated the influence of differential reward motivation on the selectivity of postencoding markers of systems-level memory consolidation. Human participants encoded intermixed, trial-unique memoranda that were associated with either high or low-value during fMRI acquisition. Encoding was interleaved with periods of rest, allowing us to investigate experience-dependent changes in connectivity as they related to later memory. Behaviorally, we found that reward motivation enhanced 24 h associative memory. Analysis of patterns of postencoding connectivity showed that, even though learning trials were intermixed, there was significantly greater connectivity with regions of high-level, category-selective visual cortex associated with high-reward trials. Specifically, increased connectivity of category-selective visual cortex with both the VTA and the anterior hippocampus predicted associative memory for high- but not low-reward memories. Critically, these results were independent of encoding-related connectivity and univariate activity measures. Thus, these findings support a model by which the selective stabilization of memories for salient events is supported by postencoding interactions with sensory cortex associated with reward.

Significance statement: Reward motivation is thought to promote memory by supporting memory consolidation. Yet, little is known as to how brain selects relevant information for subsequent consolidation based on reward. We show that experience-dependent changes in connectivity of both the anterior hippocampus and the VTA with high-level visual cortex selectively predicts memory for high-reward memoranda at a 24 h delay. These findings provide evidence for a novel mechanism guiding the consolidation of memories for valuable events, namely, postencoding interactions between neural systems supporting mesolimbic dopamine activation, episodic memory, and perception.

Keywords: VTA; category-selective visual cortex; consolidation; hippocampus; rest; reward.

Figure 1.

Overview of experimental design. A, Participants first completed a baseline rest scan followed by a scene/face localizer task. Following the localizer task, participants completed 3 rounds of motivated encoding, incentivized retrieval on a subset of trials, and postencoding rest. Postencoding rest followed retrieval as to ensure that individuals were not incentivized to rehearse information. At a 24 h delay, participants completed a nonincentivized memory test for memoranda that was not tested during the immediate test. B, During motivated encoding, participants were trying to associate trial-unique pictures and words. Before encoding, a condition cue appeared indicating whether successful encoding would contribute to a high-value bonus ($20) or a low-value bonus ($1). High- and low-value encoding was intermixed across encoding blocks.

Figure 2.

Motivated encoding influences 24 h associative memory. At a 24 h test, associative cued recall was greater for pairs encoded under high- versus low-reward motivation. Critically, participants showed a selectivity of memory for high-value information despite retrieval being nonincentivized. *p < 0.05.

Figure 3.

Postencoding interactions between the hippocampus and CSC predict 24 h associative memory. Experience-dependent changes in coupling (postencoding > baseline) of CSC (top left) with anterior and posterior hippocampus (bottom left) differentially predict high- and low-reward memory. Interactions between anterior hippocampus with high-reward CSC predict high-reward memory, although no such relationship exists between anterior hippocampus-low-reward CSC interactions and low-reward memory (top right). Conversely, interactions between posterior hippocampus with low-reward CSC predict low-reward memory, although no such relationship exists between posterior hippocampus-high-reward CSC interactions and high-reward memory (bottom right). High- and low-reward CSC refers to CSC associated with high- and low-rewards during encoding, respectively. Green dots indicate high-reward values. Gray dots indicates low-reward values. Solid lines indicate significant correlations. *p < 0.05. Hyphenated lines indicate nonsignificant correlations.

Figure 4.

Postencoding interactions between the VTA and CSC. We found experience-dependent increases in functional connectivity of the VTA (left) with both high-reward CSC and low-reward CSC (middle). However, interactions of VTA-high-reward CSC predicted high-reward associative memory, although no such relationship exists between VTA-low-reward CSC interactions and low-reward memories (right). Green dots indicate high-reward values. Gray dots indicates low-reward values. Solid lines indicate significant correlations. *p < 0.05. Hyphenated lines indicate nonsignificant correlations.