Deborah Talmi

Human Pavlovian–Instrumental Transfer

The vigor with which a participant performs actions that produce valuable outcomes is subject to a complex set of motivational influences. Many of these are believed to involve the amygdala and the nucleus accumbens, which act as an interface between limbic and motor systems. One prominent class of influences is called pavlovian–instrumental transfer (PIT), in which the motivational characteristics of a predictor influence the vigor of an action with respect to which it is formally completely independent. We provide a demonstration of behavioral PIT in humans, with an audiovisual predictor of the noncontingent delivery of money inducing participants to perform more avidly an action involving squeezing a handgrip to earn money. Furthermore, using functional magnetic resonance imaging, we show that this enhanced motivation was associated with a trial-by-trial correlation with the blood oxygenation level-dependent (BOLD) signal in the nucleus accumbens and a subject-by-subject correlation with the BOLD signal in the amygdala. Our data dovetails well with the animal literature and sheds light on the neural control of vigor.

Can semantic relatedness explain the enhancement of memory for emotional words

Memory for emotional items is often better than memory for neutral items. In three experiments, we examined whether this typical finding is due to the higher semantic relatedness inherent to emotional items, a confound in previous studies. We also controlled for other possible confounding variables, such as imagery. In Experiments 1 and 2, participants encoded lists of emotional and categorized neutral words equivalent in semantic relatedness, as well as lists of random neutral words with lower semantic relatedness. In Experiment 3, the lists were mixed, containing words from all the conditions. Surprise free recall was tested after a 40- to 55-min retention interval. Free recall of emotional words was better than that of random neutral words, replicating the classic effect. Importantly, categorized words were recalled better than random neutral words, and not worse than emotional words. These results emphasize the important role of semantic relatedness in the classic effect and suggest that organizational processes operate alongside arousal-related ones to enhance memory for emotional material.

The role of attention and relatedness in emotionally enhanced memory

Examining the positive and negative pictures separately revealed that emotionally enhanced memory (EEM) for positive pictures was mediated by attention, with no significant influence of emotional arousal, whereas the reverse was true of negative pictures. Consistent with this finding, in Experiment 2 EEM for negative pictures was found even when task emphasis was manipulated so that equivalent attention was allocated to negative and neutral pictures. The results show that attention and semantic relatedness contribute to EEM, with the extent varying with emotional valence. Negative emotion can influence memory independently of these 2 factors.

Choosing to make an effort: the role of striatum in signaling physical effort of a chosen action.

The possibility that we will have to invest effort influences our future choice behavior. Indeed deciding whether an action is actually worth taking is a key element in the expression of human apathy or inertia. There is a well developed literature on brain activity related to the anticipation of effort, but how effort affects actual choice is less well understood. Furthermore, prior work is largely restricted to mental as opposed to physical effort or has confounded temporal with effortful costs. Here we investigated choice behavior and brain activity, using functional magnetic resonance imaging, in a study where healthy participants are required to make decisions between effortful gripping, where the factors of force (high and low) and reward (high and low) were varied, and a choice of merely holding a grip device for minimal monetary reward. Behaviorally, we show that force level influences the likelihood of choosing an effortful grip. We observed greater activity in the putamen when participants opt to grip an option with low effort compared with when they opt to grip an option with high effort. The results suggest that, over and above a nonspecific role in movement anticipation and salience, the putamen plays a crucial role in computations for choice that involves effort costs.

How humans integrate the prospects of pain and reward during choice

The maxim “no pain, no gain” summarizes scenarios in which an action leading to reward also entails a cost. Although we know a substantial amount about how the brain represents pain and reward separately, we know little about how they are integrated during goal-directed behavior. Two theoretical models might account for the integration of reward and pain. An additive model specifies that the disutility of costs is summed linearly with the utility of benefits, whereas an interactive model suggests that cost and benefit utilities interact so that the sensitivity to benefits is attenuated as costs become increasingly aversive. Using a novel task that required integration of physical pain and monetary reward, we examined the mechanism underlying cost–benefit integration in humans. We provide evidence in support of an interactive model in behavioral choice. Using functional neuroimaging, we identify a neural signature for this interaction such that, when the consequences of actions embody a mixture of reward and pain, there is an attenuation of a predictive reward signal in both ventral anterior cingulate cortex and ventral striatum. We conclude that these regions subserve integration of action costs and benefits in humans, a finding that suggests a cross-species similarity in neural substrates that implement this function and illuminates mechanisms that underlie altered decision making under aversive conditions.

Immediate memory consequences of the effect of emotion on attention to pictures

Emotionally arousing stimuli are at once both highly attention grabbing and memorable. We examined whether emotional enhancement of memory (EEM) reflects an indirect effect of emotion on memory, mediated by enhanced attention to emotional items during encoding. We tested a critical prediction of the mediation hypothesis-that regions conjointly activated by emotion and attention would correlate with subsequent EEM. Participants were scanned with fMRI while they watched emotional or neutral pictures under instructions to attend to them a lot or a little, and were then given an immediate recognition test. A region in the left fusiform gyrus was activated by emotion, voluntary attention, and subsequent EEM. A functional network, different for each attention condition, connected this region and the amygdala, which was associated with emotion and EEM, but not with voluntary attention. These findings support an indirect cortical mediation account of immediate EEM that may complement a direct modulation model.

The Feedback-Related Negativity Signals Salience Prediction Errors, Not Reward Prediction Errors

Modulations of the feedback-related negativity (FRN) event-related potential (ERP) have been suggested as a potential biomarker in psychopathology. A dominant theory about this signal contends that it reflects the operation of the neural system underlying reinforcement learning in humans. The theory suggests that this frontocentral negative deflection in the ERP 230–270 ms after the delivery of a probabilistic reward expresses a prediction error signal derived from midbrain dopaminergic projections to the anterior cingulate cortex. We tested this theory by investigating whether FRN will also be observed for an inherently aversive outcome: physical pain. In another session, the outcome was monetary reward instead of pain. As predicted, unexpected reward omissions (a negative reward prediction error) yielded a more negative deflection relative to unexpected reward delivery. Surprisingly, unexpected pain omission (a positive reward prediction error) also yielded a negative deflection relative to unexpected pain delivery. Our data challenge the theory by showing that the FRN expresses aversive prediction errors with the same sign as reward prediction errors. Both FRNs were spatiotemporally and functionally equivalent. We suggest that FRN expresses salience prediction errors rather than reward prediction errors.

Enhanced Emotional Memory: Cognitive and Neural Mechanisms

Memory for emotional events is typically more vivid and accurate than memory for neutral ones. The modulation model focuses on the consolidation of memory traces to provide a partial account of enhanced emotional memory. Mediation theory focuses on encoding and retrieval to explain the selective enhancement of memory for emotional aspects of a complex event and why emotional memory also can be enhanced immediately after the experience, before consolidation has occurred. Mediation theory can therefore complement the modulation model, and together they may provide a more comprehensive account of human emotional memory.

Neuroimaging the Serial Position Curve: A Test of Single-Store Versus Dual-Store Models

Neuroimaging data could help clarify the longstanding dispute between dual-store and single-store models of the serial position curve. Dual-store models assume that retrieval from late positions is dependent on short-term memory (STM), whereas retrieval from early positions is dependent on long-term memory (LTM). Single-store models, however, assume that retrieval processes for early and late items are similar, but that early items are more difficult to discriminate than late items. The present study used functional magnetic resonance imaging to examine this question. Ten young adults were scanned while they recognized items from early or late serial positions. Recognition of early items uniquely activated brain areas traditionally associated with LTM, namely, regions within the hippocampal memory system. None of these areas was activated for retrieval of late items. These results indicate differential use of LTM retrieval processes, and therefore support dual-store models over single-store models.

Psychophysical and Neural Evidence for Emotion-Enhanced Perceptual Vividness

Highly emotional events are associated with vivid “flashbulb” memories. Here we examine whether the flashbulb metaphor characterizes a previously unknown emotion-enhanced vividness (EEV) during initial perceptual experience. Using a magnitude estimation procedure, human observers estimated the relative magnitude of visual noise overlaid on scenes. After controlling for computational metrics of objective visual salience, emotional salience was associated with decreased noise, or heightened perceptual vividness, demonstrating EEV, which predicted later memory vividness. Event-related potentials revealed a posterior P2 component at ∼200 ms that was associated with both increased emotional salience and decreased objective noise levels, consistent with EEV. Blood oxygenation level-dependent response in the lateral occipital complex (LOC), insula, and amygdala predicted online EEV. The LOC and insula represented complimentary influences on EEV, with the amygdala statistically mediating both. These findings indicate that the metaphorical vivid light surrounding emotional memories is embodied directly in perceptual cortices during initial experience, supported by cortico-limbic interactions.