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Abstract Behaving adaptively requires selection of relevant memories and sensations and suppression of competing ones. We hypothesize that these mechanisms are linked, such that hippocampal computations that resolve competition in memory also shape the precision of sensory representations to guide selective attention. We leverage fMRI-based pattern similarity, receptive field modeling, and eye tracking to test this hypothesis in humans performing a memory-dependent visual search task. In the hippocampus, more distinct representations of competing memories are associated with the accuracy of memory-guided eye movements. In visual cortex, preparatory coding of remembered target locations precedes search successes, whereas preparatory coding of competing locations precedes search failures due to interference. These effects are linked: more distinct hippocampal memories are associated with lower competitor activation in visual cortex, yielding more precise preparatory representations. These results demonstrate a role for memory distinctiveness in shaping the precision of sensory representations, highlighting links between mechanisms that overcome competition in memory and perception. 

Abstract Forming memories requires a focus on the external world; retrieving memories requires attention to our internal world. Computational models propose that the hippocampus resolves the tension between encoding and retrieval by alternating between states that prioritize one over the other. We asked whether the success of a retrieval state affects the success of an encoding state, when both are measured in behavior. Across 3 Experiments (N = 197), we operationalized retrieval as the use of memories to make predictions about the future, and tested whether successful (vs. unsuccessful) prediction affected the likelihood of successful encoding. Participants viewed a series of scene categories that contained structure (e.g., beaches are followed by castles), which enabled memory retrieval to guide prediction. After structure learning, they completed a simultaneous prediction and encoding task. They were shown trial-unique category exemplars and made predictions about upcoming scene categories. Finally, participants completed a surprise memory test for the trial-unique images. Accurate (vs. inaccurate) predictions were associated with better encoding, and increasing prediction distance hurt both prediction and encoding. This association between encoding and prediction could not be explained by generic on- vs. off-task states. We propose that, in addition to stimulus and endogenous factors that modulate switches between encoding and retrieval, the success of one state can facilitate a switch to the other. Thus, although encoding and prediction depend on distinct and competitive computational mechanisms, the success of one in behavior can increase the likelihood of success for the other. 

While viewing a visual stimulus, we often cannot tell whether it is inherently memorable or forgettable. However, the memorability of a stimulus can be quantified and partially predicted by a collection of conceptual and perceptual factors. Higher-level properties that represent the “meaningfulness” of a visual stimulus to viewers best predict whether it will be remembered or forgotten across a population. Here, we hypothesize that the feelings evoked by an image, operationalized as the valence and arousal dimensions of affect, significantly contribute to the memorability of scene images. We ran two complementary experiments to investigate the influence of affect on scene memorability, in the process creating a new image set (VAMOS) of hundreds of natural scene images for which we obtained valence, arousal, and memorability scores. From our first experiment, we found memorability to be highly reliable for scene images that span a wide range of evoked arousal and valence. From our second experiment, we found that both valence and arousal are significant but weak predictors of image memorability. Scene images were most memorable if they were slightly negatively valenced and highly arousing. Images that were extremely positive or unarousing were most forgettable. Valence and arousal together accounted for less than 8% of the variance in image memorability. These findings suggest that evoked affect contributes to the overall memorability of a scene image but, like other singular predictors, does not fully explain it. Instead, memorability is best explained by an assemblage of visual features that combine, in perhaps unintuitive ways, to predict what is likely to stick in our memory. 

Some people exhibit impressive memory for a wide array of semantic knowledge. What makes these trivia experts better able to learn and retain novel facts? We hypothesized that new semantic knowledge may be more strongly linked to its episodic context in trivia experts. We designed a novel online task in which 132 participants varying in trivia expertise encoded “exhibits” of naturalistic facts with related photos in one of two “museums.” Afterward, participants were tested on cued recall of facts and recognition of the associated photo and museum. Greater trivia expertise predicted higher cued recall for novel facts. Critically, trivia experts but not non-experts showed superior fact recall when they remembered both features (photo and museum) of the encoding context. These findings illustrate enhanced links between episodic memory and new semantic learning in trivia experts, and show the value of studying trivia experts as a special population that can shed light on the mechanisms of memory. 

Everyday experience requires processing external signals from the world around us and internal information retrieved from memory. To do both, the brain must fluctuate between states that are optimized for external vs. internal attention. Here, we focus on the hippocampus as a region that may serve at the interface between these forms of attention, and ask how it switches between prioritizing sensory signals from the external world vs. internal signals related to memories and thoughts. Pharmacological, computational, and animal studies have identified input from the cholinergic basal forebrain as important for biasing the hippocampus towards processing external information, whereas complementary research suggests the dorsal attention network (DAN) may aid in allocating attentional resources towards accessing internal information. We therefore tested the hypothesis that the basal forebrain and DAN drive the hippocampus towards external and internal attention, respectively. We used data from 29 human participants (17 female) who completed 2 attention tasks during fMRI. One task (“memory-guided”) required proportionally more internal attention, and proportionally less external attention, than the other (“explicitly instructed”). We discovered that background functional connectivity between the basal forebrain and hippocampus was stronger during the explicitly instructed vs. memory-guided task. In contrast, DAN-hippocampus background connectivity was stronger during the memory-guided vs. explicitly instructed task. Finally, the strength of DAN-hippocampus background connectivity was correlated with performance on the memory-guided but not explicitly instructed task. Together, these results provide evidence that the basal forebrain and DAN may modulate the hippocampus to switch between external and internal attention. 

Goal-directed behavior requires adaptive systems that respond to environmental demands. In the absence of threat (or presence of reward), individuals can explore many behavioral trajectories, effectively interrogating the environment across multiple dimensions. This leads to flexible, relational memory encoding and retrieval. In the presence of danger, motivation shifts to an imperative state characterized by a narrow focus of attention on threatening information. This impairs flexible, relational memory. We test how these motivational shifts affect behavioral flexibility in an ecologically valid setting. Participants learned the structure of maze-like environments and navigated to the location of objects in both safe and threatening contexts. The latter contained a predator that could ‘capture’ participants, leading to electric shock. After learning, the path to some objects was unpredictably blocked, forcing a detour for which one route was significantly shorter. We predicted that threat would push participants toward an imperative state, leading to less efficient and less flexible navigation. Threat caused participants to take longer paths to goal objects and less efficient detours when obstacles were encountered. Threat-related impairments in detour navigation persisted after controlling for non-detour navigation performance, and non-detour navigation was not a reliable predictor of detour navigation. This suggests a specific impairment in flexible navigation during detours, an impairment unlikely to be explained by more general processes like predator avoidance or divided attention that may be present during non-detour navigation. These results provide ecologically valid evidence that dynamic, observable threats reduce flexible use of cognitive maps to guide behavior. 

Multiple types of memory guide attention: Both long-term memory (LTM) and working memory (WM) effectively guide visual search. Furthermore, both types of memories can capture attention automatically, even when detrimental to performance. It is less clear, however, how LTM and WM cooperate or compete to guide attention in the same task. In a series of behavioral experiments, we show that LTM and WM reliably cooperate to guide attention: Visual search is faster when both memories cue attention to the same spatial location (relative to when only one memory can guide attention). LTM and WM competed to guide attention in more limited circumstances: Competition only occurred when these memories were in different dimensions – particularly when participants searched for a shape and held an accessory color in mind. Finally, we found no evidence for asymmetry in either cooperation or competition: There was no evidence that WM helped (or hindered) LTM-guided search more than the other way around. This lack of asymmetry was found despite differences in LTM-guided and WM-guided search overall, and differences in how two LTMs and two WMs compete or cooperate with each other to guide attention. This work suggests that, even if only one memory is currently task-relevant, WM and LTM can cooperate to guide attention; they can also compete when distracting features are salient enough. This work elucidates interactions between WM and LTM during attentional guidance, adding to the literature on costs and benefits to attention from multiple active memories.