Holly J. Bowen

Reward-Enhanced Memory in Younger and Older Adults

OBJECTIVES We investigated how the anticipation of remote monetary reward modulates intentional episodic memory formation in younger and older adults. On the basis of prior findings of preserved reward-cognition interactions in aging, we predicted that reward anticipation would be associated with enhanced memory in both younger and older adults. On the basis of previous demonstrations of a time-dependent effect of reward anticipation on memory, we expected the memory enhancement to increase with study-test delay. METHOD In Experiment 1, younger and older participants encoded a series of picture stimuli associated with high- or low-reward values. At test (24-hr postencoding), recognition hits resulted in either high or low monetary rewards, whereas false alarms were penalized to discourage guessing. Experiment 2 was similar to Experiment 1, but the study-test delay was manipulated within subjects (immediate vs 24hr). RESULTS In Experiment 1, younger and older adults showed enhanced recognition for high-reward pictures compared with low-reward pictures. Experiment 2 replicated this finding and additionally showed that the effect did not extend to immediate recognition. DISCUSSION The current findings provide support for a time-dependent mechanism of reward-based memory enhancement. They also suggest that aging leaves intact the positive influence of reward anticipation on intentional long-term memory formation.

Neural responses to monetary incentives in younger and older adults

Reward anticipation is associated with activity in the dopaminergic midbrain as well as the ventral striatum, amygdala, and medial prefrontal cortex. Dopaminergic neuromodulation declines with age, suggesting that incentive processing should also undergo age-related change. However, the literature is mixed, perhaps reflecting variation in the degree to which tasks made demands on learning and memory. Furthermore, the emphasis has been on the reward network, with few studies addressing reward-related activations in other brain regions. In the current study, 16 younger adults (mean age: 25.4) and 15 older adults (mean age: 69.0) underwent fMRI while completing a monetary incentive delay task. This task allowed the separate assessment of responses to gain and loss incentive cues while minimizing memory demands. We assessed incentive-related activations using mean-centered Partial Least Squares, a data-driven multivariate technique optimal for identifying spatiotemporal whole-brain activation patterns associated with variation in task conditions. The analyses yielded two significant latent variables representing distinct incentive-related activation patterns. The first pattern showed robust activation of the reward network and was not modulated by age. The second pattern, peaking ~10s after cue onset, showed reduced deactivation of default-network regions, and increased activation of prefrontal cognitive-control regions in older adults, compared with younger adults. Neither pattern was modulated by incentive valence. Overall, these findings suggest that aging may not affect primary motivational signaling in the reward network, but may rather be associated with alterations in incentive-driven modulation of cortical networks that influence multiple cognitive domains. This article is part of a Special Issue entitled Memory & Aging.

Motivational incentives modulate age differences in visual perception.

This study examined whether motivational incentives modulate age-related perceptual deficits. Younger and older adults performed a perceptual discrimination task in which bicolored stimuli had to be classified according to their dominating color. The valent color was associated with either a positive or negative payoff, whereas the neutral color was not associated with a payoff. Effects of incentives on perceptual efficiency and response bias were estimated using the diffusion model (Ratcliff, 1978). Perception of neutral stimuli showed age-related decline, whereas perception of valent stimuli, both positive and negative, showed no age difference. This finding is interpreted in terms of preserved top-down control over the allocation of perceptual processing resources in healthy aging.

A Diffusion Model Analysis of Decision Biases Affecting Delayed Recognition of Emotional Stimuli.

Previous empirical work suggests that emotion can influence accuracy and cognitive biases underlying recognition memory, depending on the experimental conditions. The current study examines the effects of arousal and valence on delayed recognition memory using the diffusion model, which allows the separation of two decision biases thought to underlie memory: response bias and memory bias. Memory bias has not been given much attention in the literature but can provide insight into the retrieval dynamics of emotion modulated memory. Participants viewed emotional pictorial stimuli; half were given a recognition test 1-day later and the other half 7-days later. Analyses revealed that emotional valence generally evokes liberal responding, whereas high arousal evokes liberal responding only at a short retention interval. The memory bias analyses indicated that participants experienced greater familiarity with high-arousal compared to low-arousal items and this pattern became more pronounced as study-test lag increased; positive items evoke greater familiarity compared to negative and this pattern remained stable across retention interval. The findings provide insight into the separate contributions of valence and arousal to the cognitive mechanisms underlying delayed emotion modulated memory.

NEVER forget: negative emotional valence enhances recapitulation

A hallmark feature of episodic memory is that of “mental time travel,” whereby an individual feels they have returned to a prior moment in time. Cognitive and behavioral neuroscience methods have revealed a neurobiological counterpart: Successful retrieval often is associated with reactivation of a prior brain state. We review the emerging literature on memory reactivation and recapitulation, and we describe evidence for the effects of emotion on these processes. Based on this review, we propose a new model: Negative Emotional Valence Enhances Recapitulation (NEVER). This model diverges from existing models of emotional memory in three key ways. First, it underscores the effects of emotion during retrieval. Second, it stresses the importance of sensory processing to emotional memory. Third, it emphasizes how emotional valence – whether an event is negative or positive – affects the way that information is remembered. The model specifically proposes that, as compared to positive events, negative events both trigger increased encoding of sensory detail and elicit a closer resemblance between the sensory encoding signature and the sensory retrieval signature. The model also proposes that negative valence enhances the reactivation and storage of sensory details over offline periods, leading to a greater divergence between the sensory recapitulation of negative and positive memories over time. Importantly, the model proposes that these valence-based differences occur even when events are equated for arousal, thus rendering an exclusively arousal-based theory of emotional memory insufficient. We conclude by discussing implications of the model and suggesting directions for future research to test the tenets of the model.

Recapitulation of emotional source context during memory retrieval

Recapitulation involves the reactivation of cognitive and neural encoding processes at retrieval. In the current study, we investigated the effects of emotional valence on recapitulation processes. Participants encoded neutral words presented on a background face or scene that was negative, positive or neutral. During retrieval, studied and novel neutral words were presented alone (i.e., without the scene or face) and participants were asked to make a remember, know or new judgment. Both the encoding and retrieval tasks were completed in the fMRI scanner. Conjunction analyses were used to reveal the overlap between encoding and retrieval processing. These results revealed that, compared to positive or neutral contexts, words that were recollected and previously encoded in a negative context showed greater encoding-to-retrieval overlap, including in the ventral visual stream and amygdala. Interestingly, the visual stream recapitulation was not enhanced within regions that specifically process faces or scenes but rather extended broadly throughout visual cortices. These findings elucidate how memories for negative events can feel more vivid or detailed than positive or neutral memories.

Commentary: Episodic Memory Retrieval Functionally Relies on Very Rapid Reactivation of Sensory Information.

Several prominent memory theories are predicated on the idea that retrieval relies on reactivation of processes engaged during encoding, a process known as “ecphory” (Tulving, 1983). Functional magnetic resonance imaging (fMRI) work has shown reactivation effects in visual cortex (e.g., Slotnick and Schacter, 2006; Kark and Kensinger, 2015) highlighting the importance of sensory reactivation to episodic memory. Such fMRI studies do not have the temporal resolution to distinguish ecphoric from retrieval processes, which are thought to be distinctly successive in time (Tulving, 1976). Studies of brain oscillations have provided insight into the temporal unfolding of memory. While many of these studies have focused on the memory-facilitating effects of synchronization in the γ/ θ bands, recent work indicates that desynchronization in α/β bands plays a complementary role in memory (Hanslmayr et al., 2012). Specifically, mathematical models of information theory suggest that while synchronization corresponds to cortical inhibition and facilitates information transfer (i.e., “fire together, wire together”), desynchronization in oscillatory activity corresponds to disinhibition and enhances the capacity for computational complexity, which facilitates an information-rich memory trace (Hanslmayr et al., 2016). Oscillatory dynamics can be measured with electroencephalography (EEG) and manipulated using rhythmic transcranial magnetic stimulation (rTMS; Johnson et al., 2010), but until now have not been used in compliment to demonstrate a functional link between early oscillatory signatures of sensory reactivation and behavioral memory performance. Leveraging these techniques, Waldhauser et al. (2016) examined whether early sensory reactivation is necessary for episodic memory, in line with the theory of ecphory. In two experiments, participants encoded objects that were presented in the left or right visual field. During recognition, objects were presented centrally and participants made an old/new memory judgment followed by a spatial source judgment. Experiment 1 aimed to localize retrieval-related reactivation of oscillatory activity in sensory regions engaged during encoding, a potential neural marker of ecphory. EEG measured during encoding and retrieval revealed an early (~100–200 ms) signature of reactivation, as evidenced by desynchronization in the α/β band localized to the lateral occipital cortex in extrastriate cortex. In Experiment 2, rTMS during retrieval cue presentation disrupted retrieval-related desynchronization in lateral occipital cortex decreasing source memory for items originally presented to the contralateral—but not ipsilateral—visual field. These results provide the first evidence that early sensory reactivation is causally relevant for episodic memory and confirm that ecphory is critical for retrieval judgments. To provide further insight into the basis of the link between sensory reactivation and ecphoric processes, there are a number of interesting directions for future research. First, evidence of reactivation in extrastriate cortex does not eliminate the possibility that reactivation processes might begin either earlier or later in the visual processing stream for some memory traces. Visual processing involves feedforward and feedback sweeps between earlier and later visual regions (Lamme and Roelfsema, 2000). While some studies report reactivation in early visual regions (Slotnick and Schacter, 2006), others posit an efficient retrieval process whereby reactivation occurs in higher-order portions of the ventral visual stream, without reactivation of early visual regions involved in processing of low-level visual features (Wheeler and Buckner, 2003). Second, as mentioned by the authors, ecphoric processes are not necessarily specific to the α/β band. Future work is needed to further probe the spatial (e.g., early vs. late visual cortex) and temporal (e.g., other frequency bands and onset of effects) characteristics—and the spatio-temporal interactions—that underlie ecphoric processes. Further, questions remain regarding the underlying neuronal mechanisms that link α/β desynchronization in extrastriate cortex and memory performance. The authors find a significant—but small (7%)—decrease in memory performance for items presented to the contralateral visual field following rTMS. Thus, early reactivation might be necessary for some memories but clearly not all memories. A combined EEG-TMS approach is needed to confirm that high-frequency rTMS indeed disrupts desynchronization in extrastriate cortex. Conversely, additional evidence of causality could be revealed if rTMS can be used to induce extrastriate cortex into a greater state of α/β desynchronization, presumably driving a behavioral memory enhancement. Beyond clarification of neuronal mechanisms, the findings of Waldhauser et al. afford a number of future directions to strengthen the argument that extrastriate reactivation is functionally relevant to episodic memory. Extrastriate cortex has distinct upper visual field and lower-visual field representations that map onto more ventral and dorsal portions, respectively (Strother et al., 2010). Presenting objects in all four visual quadrants and applying rTMS to more dorsal or more ventral extrastriate cortex could demonstrate quadrant-specific memory disruption. Such a paradigm would reduce the possibility that a participant guesses the correct source. Second, Waldhauser et al.s argument that extrastriate cortex reactivation is functionally necessary for recollective episodic retrieval could be strengthened with the addition of a remember/know judgment to separate memories that are recollected (i.e., include episodic content) from those that are familiar (i.e., devoid of contextual information). Recollection and familiarity have unique neural correlates (Yonelinas et al., 2002) and oscillatory signatures (Burgess and Ali, 2002), suggesting they are qualitatively different. If evidence for reactivation in the extrastriate cortex consistently occurs for items endorsed with “remember,” this would bolster their conclusions regarding ecphoric processes. Finally, the question remains whether these findings are indicative of a general episodic memory mechanism. Although sensory reactivation appears functionally relevant visual-spatial source memory, it is not necessarily functionally relevant to episodic memory more generally, as they conclude. Episodic memory involves the conscious recollection of contextual information, but differing perspectives on how to test memory for context has led to the creation of a wide variety of episodic memory tasks. Results of different episodic memory paradigms are not always correlated, indicating the psychological and potentially neural processes that support these tasks are not always the same (Cheke and Clayton, 2013). Before concluding that early sensory reactivation supports episodic memory it is necessary to test the functional relevance of sensory reactivation to ecphoric processes using other episodic memory tasks.

Age differences in the neural response to negative feedback

ABSTRACT Affective processing is one domain that remains relatively intact in healthy aging. Investigations into the neural responses associated with reward anticipation have revealed that older and younger adults recruit the same midbrain reward regions, but other evidence suggests this recruitment may differ depending on the valence (gain, loss) of the incentive cue. The goal of the current study was to examine functional covariance during gain and loss feedback in younger and healthy older adults. A group of 15 older adults (mean age = 68.5) and 16 younger adults (mean age = 25.4) completed a revised Monetary Incentive Delay task (rMID; Knutson, Westdorp, Kaiser, & Hommer, 2000) while in the fMRI scanner. The rMID is a reaction time task where successful performance, either gaining a reward or avoiding a loss, is defined by hitting a button during the brief presentation of a visual target. Participants receive gain and loss anticipation cues before each trial and feedback after each trial with four possible outcomes: +

Memory-related functional connectivity in visual processing regions varies by prior emotional context

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Chronic exposure to violent video games is not associated with alterations of emotional memory

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