The Neural Representations of Emotional Experiences Are More Similar Than Those of Neutral Experiences.

Stimuli that evoke the same feelings can nevertheless look different and have different semantic meanings. Although we know much about the neural representation of emotion, the neural underpinnings of emotional similarity are unknown. One possibility is that the same brain regions represent similarity between emotional and neutral stimuli, perhaps with different strengths. Alternatively, emotional similarity could be coded in separate regions, possibly those sensitive to emotional valence and arousal. In behavior, the extent to which people consider similarity along emotional dimensions when they evaluate the overall similarity between stimuli has never been investigated. Although the emotional features of stimuli may dominate explicit ratings of similarity, it is also possible that people neglect emotional dimensions as irrelevant to that judgment. We contrasted these hypotheses in (male and female) healthy controls using two measures of similarity and two picture databases of complex negative and neutral scenes, the second of which provided exquisite control over semantic and visual attributes. The similarity between emotional stimuli was greater than between neutral stimuli in the inferior temporal cortex, the fusiform face area, and the precuneus. Additionally, only the similarity between emotional stimuli was significantly represented in early visual cortex, anterior insula and dorsal anterior cingulate cortex. Intriguingly, despite the stronger neural similarity between emotional stimuli, the same participants did not rate them as more similar to each other than neutral stimuli. These results contribute to our understanding of how emotion is represented within a general conceptual workspace and of the overgeneralization bias in anxiety disorders.SIGNIFICANCE STATEMENT We tested differences in similarity between emotional and neutral scenes. Arousal and negative valence did not increase similarity ratings. When conditions were equated on semantic similarity, participants rated emotional stimuli as similar to each other as neutral ones. Despite this equivalence, the similarity among the neural representations of emotional compared with neutral stimuli was higher in regions, which also expressed similarity between neutral stimuli and in unique regions. We report a striking difference between behavioral and neural similarity; strong neural similarity between emotional pictures did not influence similarity judgements in the same participants in the behavioral rating task after the scan. These findings may have an impact on research about the neural representations of emotional categories and the overgeneralization bias in anxiety disorders.

Can neural correlates of encoding explain the context dependence of reward-enhanced memory?

Selective encoding can be studied by manipulating how valuable it is for participants to remember specific stimuli, for instance, by varying the monetary reward participants receive for recalling a particular stimulus in a subsequent memory test. It would be reasonable for participants to strategically attend more to high-reward items compared to low-reward items in mixed list contexts, but to attend both types of items equally in pure list contexts, where all items are of equal value. Reward-enhanced memory may be driven by automatic dopaminergic interactions between reward circuitry and the hippocampus and thus be insensitive to list context; or it may be driven by meta-cognitive strategies, and thus context-dependent. We contrasted these alternatives by manipulating list composition and tracked selective encoding through multiple EEG measures of attention and rehearsal. Behavioral results were context-dependent, such that recall of high-reward items was increased only in mixed lists. This result and aspects of the recall dynamics confirm predictions of the eCMR (emotional Context Maintenance and Retrieval) model. The power of ssVEPs was lower for high-reward items regardless of list composition, suggesting decreased visual processing of high-reward stimuli and that ssVEPs may index the modulation of context-to-item associations predicted by eCMR. By contrast, reward modulated the amplitude of Late Positive Potential and Frontal Slow Wave only in mixed lists. Taken together, the results provide evidence that reward-enhanced memory is caused by an interplay between strategic processes applied when high- and low-reward items compete for cognitive resources during encoding and context-dependent mechanisms operating during recall.

Are multiple types of associative memory differently impacted by emotion?

The effect of emotion on associative memory is still an open question. Our aim was to test whether discrepant findings are due to differential impact of emotion on different types of associative memory or to differences in the way participants encoded stimuli across studies. We examined the effect of negative content on multiple forms of associative memory, using the same encoding task. Two registered experiments were conducted in parallel with random allocation of participants to experiments. Each experiment included 4 encoding blocks, in which participants read a neutral text comprised of 6 paragraphs, which were interleaved with neutral or negative images. Images were controlled for visual properties and semantic similarity. Memory tests included recognition memory, Remember/Know, order memory, temporal source memory and contextual memory. Analyses showed that emotion decreased contextual memory but not order memory or temporal source memory. We also found that temporal source memory and contextual memory were correlated. Recognition accuracy and subjective recollection were not impacted by emotion. In agreement with previous work, participants self-reported a reduced ability to integrate blocks containing negative images with paragraphs. In contrast to our hypothesis, results suggest that emotion does not impact all types of associative memory when stimuli are controlled.

Reward does not modulate forgetting in free recall tests.

Reward is thought to attenuate forgetting through the automatic effect of dopamine on hippocampal memory traces. Here we report a conceptual replication of previous results where we did not observe this effect of reward. Participants encoded eight lists of pictures and recalled picture content immediately or the next day. They were informed that they could gain monetary reward for recalling the pictures, with the level of reward indicated through the frame surrounding the picture. Reward was manipulated both within and across lists. Bayesian statistics found moderate evidence for the null hypothesis that reward does not modulate forgetting in human free recall.

The effects of psychosocial stress on item, cued-pair and emotional memory.

Physical stress, such as from the cold-pressor test, has been robustly associated with altered memory retrieval, but it is less clear whether the same happens following psychosocial stress. Studies using psychosocial stressors report mixed effects on memory, leading to uncertainty about the common cognitive impact of both forms of stress. The current study uses a series of four carefully designed experiments, each differing by only a single critical factor to determine the effects of psychosocial stress on specific aspects of episodic memory. In three experiments, we induced psychosocial stress after participants encoded words, then assessed retrieval of those words after a prolonged delay. These experiments found no effect of post-encoding stress on recognition of neutral words or cued recall of word-pairs, but a small effect on recollection of semantically related words. There were, however, positive relationships within the stress group between measures of stress (cortisol in experiment 1 and self-reported-anxiety in experiment 3) and recollection of single word stimuli. In the fourth experiment, we found that psychosocial stress immediately before retrieval did not influence word recognition. Recollection, particularly for semantically related stimuli, may therefore be more susceptible to the effects of psychosocial stress, and future studies can assess how this relates to other forms of stress. Overall, our findings suggest that the effects of psychosocial stress on episodic memory may be more subtle than expected, warranting further exploration in larger studies.

In for a penny, in for a pound: examining motivated memory through the lens of retrieved context models.

When people encounter items that they believe will help them gain reward, they later remember them better than others. A recent model of emotional memory, the emotional context maintenance and retrieval model (eCMR), predicts that these effects would be stronger when stimuli that predict high and low reward can compete with each other during both encoding and retrieval. We tested this prediction in two experiments. Participants were promised £1 for remembering some pictures, but only a few pence for remembering others. Their recall of the content of the pictures they saw was tested after 1 min and, in experiment 2, also after 24 h. Memory at the immediate test showed effects of list composition. Recall of stimuli that predicted high reward was greater than of stimuli that predicted lower reward, but only when high- and low-reward items were studied and recalled together, not when they were studied and recalled separately. More high-reward items in mixed lists were forgotten over a 24-h retention interval compared with items studied in other conditions, but reward did not modulate the forgetting rate, a null effect that should be replicated in a larger sample. These results confirm eCMR's predictions, although further research is required to compare that model against alternatives.

Priming recognition memory test cues: No evidence for an attributional basis of recollection.

We argue that while the proposed memory model by Bastin et al. can explain familiarity-based memory judgements through the interaction of a core representation system and an attribution system, recollection-based memory judgements are not based on non-mnemonic signals being attributed to memory.

Testing the Possibility of Model-based Pavlovian Control of Attention to Threat.

Signals for reward or punishment attract attention preferentially, a principle termed value-modulated attention capture (VMAC). The mechanisms that govern the allocation of attention can be described with a terminology that is more often applied to the control of overt behaviors, namely, the distinction between instrumental and Pavlovian control, and between model-free and model-based control. Although instrumental control of VMAC can be either model-free or model-based, it is not known whether Pavlovian control of VMAC can be model-based. To decide whether this is possible, we measured steady-state visual evoked potentials (SSVEPs) while 20 healthy adults took part in a novel task. During the learning stage, participants underwent aversive threat conditioning with two conditioned stimuli (CSs): one that predicted pain (CS+) and one that predicted safety (CS-). Instructions given before the test stage allowed participants to infer whether novel, ambiguous CSs (new_CS+/new_CS-) were threatening or safe. Correct inference required combining stored internal representations and new propositional information, the hallmark of model-based control. SSVEP amplitudes quantified the amount of attention allocated to novel CSs on their very first presentation, before they were ever reinforced. We found that SSVEPs were higher for new_CS+ than new_CS-. This result is potentially indicative of model-based Pavlovian control of VMAC, but additional controls are necessary to verify this conclusively. This result underlines the potential transformative role of information and inference in emotion regulation.

The Emotional Facet of Subjective and Neural Indices of Similarity.

Emotional similarity refers to the tendency to group stimuli together because they evoke the same feelings in us. The majority of research on similarity perception that has been conducted to date has focused on non-emotional stimuli. Different models have been proposed to explain how we represent semantic concepts, and judge the similarity among them. They are supported from behavioural and neural evidence, often combined by using Multivariate Pattern Analyses. By contrast, less is known about the cognitive and neural mechanisms underlying the judgement of similarity between real-life emotional experiences. This review summarizes the major findings, debates and limitations in the semantic similarity literature. They will serve as background to the emotional facet of similarity that will be the focus of this review. A multi-modal and overarching approach, which relates different levels of neuroscientific explanation (i.e., computational, algorithmic and implementation), would be the key to further unveil what makes emotional experiences similar to each other.

Discussing factors associated with quality of life in cancer follow-up appointments: a preliminary test of a pragmatic model for clinical practice.

OBJECTIVE:: The aim of this study is to perform a preliminary test of a practical, evidence-based model to enable discussions around quality of life-related concerns during cancer follow-up appointments. DESIGN:: Cross-sectional study measuring quality of life, illness perceptions, emotional distress, fatigue, and subjective cognitive complaints. SETTING:: Cancer outpatient follow-up clinics in four National Health Services in the United Kingdom. PARTICIPANTS:: Working-age post-treatment cancer patients, treated with curative intent. INTERVENTIONS:: Not applicable. MAIN MEASURES:: European Organisation for the Research and Treatment of Cancer - Quality of Life Questionnaire - Core 30, Illness Perceptions Questionnaire - Revised, Hospital Anxiety and Depression Scale, Chalder Fatigue Scale, and Cognitive Failures Questionnaire. RESULTS:: Fifty-seven cancer patients, with a mean age of 36 years and on average 2.75 years post treatment, returned the completed questionnaires. Anxiety partially mediated the association between subjective cognitive complaints and illness identity (60%) and timeline (25%). Cognitive complaints mediated the relationships between quality of life and anxiety (45%), depression (30%), and fatigue (62%). Depression mediated the relationships between quality of life and illness identity (48%) and timeline (40%). CONCLUSION:: Our study provides a preliminary test of an evidence-based model to help elicit quality of life-related concerns during cancer follow-up appointments. Illness perceptions are associated with quality of life through the mediation of other cancer-relevant factors. Discussing the type, origin, and expected duration of symptoms may elicit other concerns, such as emotional distress, fatigue, or cognitive complaints, which explained a significant amount of the relationship between illness perceptions and quality of life.

Beneficial and detrimental effects of schema incongruence on memory for contextual events.

Mental schemas provide a framework into which new information can easily be integrated. In a series of experiments, we examined how incongruence that stems from a prediction error modulates memory for multicomponent events that instantiated preexisting schemas as noted in a previous study. Each event consisted of four stimulus pairs with overlapping components, presented in four blocks (A-B, B-C, C-D, D-A). A-B pairs elicited contextual expectations (A: Farm, B: Tractor) that were either met by a congruent C component (C: Farmer) or violated by an incongruent one (C: Lawyer). The baseline condition included unrelated pairs, where the C component was neither congruent nor incongruent. In experiment 2, events were presented in successive trials instead of blocks, and eye movements were recorded to analyze allocation of attention. Memory was tested through old-new item recognition followed by cued recall. Across experiments, recognition and recall performance for incongruent components was reduced compared to congruent components. Incongruent items were in some cases more accurately retrieved compared to unrelated ones, depending on task demands. Additionally, better recall was observed in the incongruent D-A pairs, compared to congruent and unrelated ones, because of reduced interference from C components. Eye-tracking revealed an increased number of fixations on C components in the incongruent and unrelated conditions. These results suggest that the integration of incongruent items into an episode is impaired, compared to congruent items, despite the contextual surprise and increased attention they elicited at encoding. However, there was a beneficial effect of prediction error on memory performance, compared to a baseline, depending on the task used.

Dissociation of immediate and delayed effects of emotional arousal on episodic memory.

Emotionally arousing events are usually better remembered than neutral ones. This phenomenon is in humans mostly studied by presenting mixed lists of neutral and emotional items. An emotional enhancement of memory is observed in these studies often already immediately after encoding and increases with longer delays and consolidation. A large body of animal research showed that the more efficient consolidation of emotionally arousing events is based on an activation of the central noradrenergic system and the amygdala (Modulation Hypothesis; Roozendaal & McGaugh, 2011). The immediately superior recognition of emotional items is attributed primarily to their attraction of attention during encoding which is also thought to be based on the amygdala and the central noradrenergic system. To investigate whether the amygdala and noradrenergic system support memory encoding and consolidation via shared neural substrates and processes a large sample of participants (n = 690) encoded neutral and arousing pictures. Their memory was tested immediately and after a consolidation delay. In addition, they were genotyped in two relevant polymorphisms (α2B-adrenergic receptor and serotonin transporter). Memory for negative and positive emotional pictures was enhanced at both time points where these enhancements were correlated (immediate r = 0.60 and delayed test r = 0.46). Critically, the effects of emotional arousal on encoding and consolidation correlated only very low (negative r = 0.14 and positive r = 0.03 pictures) suggesting partly distinct underlying processes consistent with a functional heterogeneity of the central noradrenergic system. No effect of genotype on either effect was observed.

Acute memory deficits in chemotherapy-treated adults.

Data from research on amnesia and epilepsy are equivocal with regards to the dissociation, shown in animal models, between rapid and slow long-term memory consolidation. Cancer treatments have lasting disruptive effects on memory and on brain structures associated with memory, but their acute effects on synaptic consolidation are unknown. We investigated the hypothesis that cancer treatment selectively impairs slow synaptic consolidation. Cancer patients and their matched controls were administered a novel list-learning task modelled on the Rey Auditory Verbal Learning Test. Learning, forgetting, and retrieval were tested before, and one day after patients' first chemotherapy treatment. Due to difficulties recruiting cancer patients at that sensitive time, we were only able to study 10 patients and their matched controls. Patients exhibited treatment-dependent accelerated forgetting over 24 hours compared to their own pre-treatment performance and to the performance of control participants, in agreement with our hypothesis. The number of intrusions increased after treatment, suggesting retrieval deficits. Future research with larger samples should adapt our methods to distinguish between consolidation and retrieval causes for treatment-dependent accelerated forgetting. The presence of significant accelerated forgetting in our small sample is indicative of a potentially large acute effect of chemotherapy treatment on forgetting, with potentially clinically relevant implications.

Emotionally arousing context modulates the ERP correlates of neutral picture processing: An ERP test of the GANE model.

The time scale of the effects of emotional arousal on neutral information processing is crucial for the predictions of the glutamate amplifies noradrenergic effects (GANE) model. GANE suggests that when emotional and neutral stimuli are presented in a sequence, neutral information processing will change. We review the literature on event-related potentials, including our own data set, to test this prediction.

Adaptive coding of reward prediction errors is gated by striatal coupling.

To efficiently represent all of the possible rewards in the world, dopaminergic midbrain neurons dynamically adapt their coding range to the momentarily available rewards. Specifically, these neurons increase their activity for an outcome that is better than expected and decrease it for an outcome worse than expected, independent of the absolute reward magnitude. Although this adaptive coding is well documented, it remains unknown how this rescaling is implemented. To investigate the adaptive coding of prediction errors and its underlying rescaling process, we used human functional magnetic resonance imaging (fMRI) in combination with a reward prediction task that involved different reward magnitudes. We demonstrate that reward prediction errors in the human striatum are expressed according to an adaptive coding scheme. Strikingly, we show that adaptive coding is gated by changes in effective connectivity between the striatum and other reward-sensitive regions, namely the midbrain and the medial prefrontal cortex. Our results provide evidence that striatal prediction errors are normalized by a magnitude-dependent alteration in the interregional connectivity within the brain's reward system.

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.

Pain perception as hierarchical Bayesian inference: A test case for the theory of constructed emotion.

An intriguing perspective about human emotion, the theory of constructed emotion considers emotions as generative models according to the Bayesian brain hypothesis. This theory brings fresh insight to existing findings, but its complexity renders it challenging to test experimentally. We argue that laboratory studies of pain could support the theory because although some may not consider pain to be a genuine emotion, the theory must at minimum be able to explain pain perception and its dysfunction in pathology. We review emerging evidence that bear on this question. We cover behavioral and neural laboratory findings, computational models, placebo hyperalgesia, and chronic pain. We conclude that there is substantial evidence for a predictive processing account of painful experience, paving the way for a better understanding of neuronal and computational mechanisms of other emotions.

Test-retest reliability of Bayesian estimations of the effects of stimulation, prior information and individual traits on pain perception.

BACKGROUND: There is inter-individual variability in the influence of different components (e.g. nociception and expectations) on pain perception. Identifying the individual effect of these components could serve for patient stratification, but only if these influences are stable in time. METHODS: In this study, 30 healthy participants underwent a cognitive pain paradigm in which they rated pain after viewing a probabilistic cue informing of forthcoming pain intensity and then receiving electrical stimulation. The trial information was then used in a Bayesian probability model to compute the relative weight each participant put on stimulation, cue, cue uncertainty and trait-like bias. The same procedure was repeated 2 weeks later. Relative and absolute test-retest reliability of all measures was assessed. RESULTS: Intraclass correlation results showed good reliability for the effect of the stimulation (0.83), the effect of the cue (0.75) and the trait-like bias (0.75 and 0.75), and a moderate reliability for the effect of the cue uncertainty (0.55). Absolute reliability measures also supported the temporal stability of the results and indicated that a change in parameters corresponding to a difference in pain ratings ranging between 0.47 and 1.45 (depending on the parameters) would be needed to consider differences in outcomes significant. The comparison of these measures with the closest clinical data we possess supports the reliability of our results. CONCLUSIONS: These findings support the hypothesis that inter-individual differences in the weight placed on different pain factors are stable in time and could therefore be a possible target for patient stratification. SIGNIFICANCE: Our results demonstrate the temporal stability of the weight healthy individuals place on the different factors leading to the pain response. These findings give validity to the idea of using Bayesian estimations of the influence of different factors on pain as a way to stratify patients for treatment personalization.

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.