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Talmi, D.

Publications and source records attributed to Talmi, D..

At least 19 recordsLinked to original sources

Contribution of the Late Positive Potential to Emotional Memory: A Joint Neuro-Cognitive Approach to Memory Prediction

Emotional events are better remembered than neutral events. The emotional Context Maintenance and Retrieval model (eCMR) explains this effect by simulating preferential encoding of emotional items, implemented by a free parameter that scales the learning rate. Incorporating a neural signal measured during encoding could make the model's account more specific, permitting a prediction not only of average increased recall but also which emotional items are likely to be recalled. We investigated whether the late positive potential (LPP) event-related potential (ERP) effect could provide this item-specific information in a secondary analysis of EEG recorded while 38 participants encoded negative and neutral pictures for an immediate free recall test (Zarubin et al. 2020). First, we established that the LPP effect was modulated by emotion in an early (400-1000 ms) and a late (1000-2000 ms) time window and this modulation was reliable in 73.7% and 50% of the participants respectively. Second, we investigated at what level the LPP was related to subsequent memory. Emotion-enhanced LPP did not covary with emotion-enhanced memory between participants or across lists within participants, but the early LPP specifically predicted memory for emotional items on a single-trial level. Third, we compared eCMR variants to test whether trial-level early LPP should scale learning for both categories or only for emotional items, and whether it could replace or complement a common learning-rate increase for all emotional items. The best-fitting model combined emotion-specific LPP scaling with the common learning-rate increase. The finding that early LPP predicted enhanced recall only for emotional items is difficult to reconcile with accounts on which the LPP reflects attention or stimulus significance more generally, which predict a relationship to memory for neutral items as well. These results pave the way to quantitative prediction of internal recall trajectories by individual participants without requiring behavioural output.

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Interactions between the representations of pain and reward suggest dynamic shifts in reference point

With an aim to understand how brains compute the expected utility of mixed prospects, namely those associated with both negative and positive attributes, we designed a task which equated the opportunity to learn about these attributes and their hedonic value. Participants underwent fMRI scanning while they experienced a classical conditioning paradigm where emotionally-neutral faces predicted a probability of pain and reward conforming to a 2 (Electric Pain: high, low) x 2 (Monetary Reward: high, low) factorial design. We found a robust interaction between the anticipation of pain and reward in the BOLD signal. Analysis of simple effects revealed that sensitivity to each attribute increased under high levels of the other attribute. In the bilateral insula and mid-cingulate gyrus sensitivity to pain was greater under high reward, and in the OFC, caudate, ventral striatum and VTA sensitivity to reward was greater under high pain. We speculate that this pattern is due to dynamic shifts in the reference point participants considered to evaluate each attribute.

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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. Behavioural 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.

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Adaptive coding of pain prediction error in the anterior insula

BackgroundUnderstanding the mechanisms behind the influence of expectation and context on pain perception is crucial for improving analgesic treatments. Prediction error (PE) signals how much a noxious stimulus deviates from expectation and is therefore crucial for our understanding of pain perception. It is thought that the brain engages in adaptive coding of pain PE, such that sensitivity to unexpected outcomes is modulated by contextual information. While there is behavioural evidence that pain is coded adaptively, and evidence that reward PE signals are coded adaptively, controversy remains regarding the underlying neural mechanism of adaptively-coded pain PEs. MethodsA cued-pain task was performed by 19 healthy adults while undergoing FMRI scanning. BOLD responses to the task were tested using an axiomatic approach to identify areas that may code pain PE adaptively. ResultsThe left dorsal anterior insula demonstrated a pattern of response consistent with adaptively-coded pain PE. Signals from this area were sensitive to both predicted pain magnitudes on the instigation of expectation, and the unexpectedness of pain delivery. Crucially however, the response at pain delivery was consistent with the local context of the pain stimulation, rather than the absolute magnitude of delivered pain, a pattern suggestive of an adaptively-coded PE signal. ConclusionsThe study advances our understanding of the neural basis of pain prediction. Alongside existing evidence that the periaqueductal grey codes pain PE and the posterior insula codes pain magnitude, the results highlight a distinct contribution of the left dorsal anterior insula in the processing of pain. Significance statementAlthough there is behavioural evidence that pain is coded adaptively, the neural mechanisms serving this process are not well understood. This study used functional MRI to provide the first evidence that the left dorsal anterior insula, an area associated with aversive learning, responds to pain in a manner consistent with the adaptive coding of pain prediction error. This study aids our understanding of the neural basis of subjective pain representation, and thus can contribute to the advancement of analgesic treatments.

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An EEG study on the effect of being overweight on anticipatory and consummatory reward in response to pleasant taste stimuli

Two-thirds of adults in the United Kingdom currently suffer from overweight or obesity, making it one of the biggest contributors to health problems. Within the framework of the incentive sensitisation theory, it has been hypothesised that overweight people experience heightened reward anticipation when encountering cues that signal food, such as pictures and smells of food, but that they experience less reward from consuming food compared to normal-weight people. There is, however, little evidence for this prediction. Few studies test both anticipation and consumption in the same study, and even fewer with electroencephalography (EEG). This study sought to address this gap in the literature by measuring scalp activity when overweight and normal-weight people encountered cues signalling the imminent arrival of pleasant and neutral taste stimuli, and when they received these stimuli. The behavioural data showed that there was a smaller difference in valence ratings between the pleasant and neutral taste in the overweight than normal-weight group, in accordance with our hypothesis. However, contrary to our hypothesis, the groups did not differ in their electrophysiological response to taste stimuli. Instead, there was a reduction in N1 amplitude to both taste and picture cues in overweight relative to normal-weight participants. This suggests that reduced attention to cues may be a crucial factor in risk of overweight.

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Emotion increases the similarity between neural representations of pictures, but not their perceived similarity.

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 that govern judgements of emotional similarity are unknown. One possibility is that the same brain regions will represent similarity between emotional and neutral stimuli, perhaps with different strengths. Alternatively, emotional similarity could be coded in separate regions, possibly those known to express emotional valence and arousal preferentially. In behaviour, the extent to which people consider similarity along the emotional dimension when they evaluate the overall similarity between stimuli has never been investigated. While the emotional features of stimuli may dominate explicit ratings of similarity, it is also possible that people neglect the emotional dimension as irrelevant. We contrasted these hypotheses with two measures of similarity and two different databases of complex negative and neutral pictures, the second of which afforded exquisite control over semantic and visual attributes. Emotion increased neural similarity in a set of regions that represented both emotional and neutral stimuli, including the inferior temporal cortex, the fusiform face area, and the precuneus. Emotion also increased neural similarity in early visual cortex, anterior insula and dorsal anterior cingulate cortex, despite no increase in BOLD-signal amplitudes in these regions. Despite the stronger neural similarity between emotional stimuli, participants rated pictures taken from two distinct emotional categories as equally similar. These results contribute to our understanding of how emotion is represented within a general conceptual workspace.

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Development of a Semantically Related Emotional and Neutral Stimulus Set

When measuring memory performance for emotional and neutral stimuli many studies are confounded by not controlling for differential semantic relatedness between stimulus sets. This could lead to the misattribution of the cause of an emotional enhancement of memory effect (EEM), because differential semantic relatedness also contributes to the EEM. Participants rated static visual emotional and neutral scenes on measures of arousal, valence, and semantic relatedness. These measures were used to create a novel stimulus set, which - in addition to demonstrating significant differences in measures of valence and arousal - also controlled for within-set semantic relatedness; thus resolving a crucial issue that has not previously been addressed in the use of visual emotional stimuli. As an added advantage, the stimulus set developed here are controlled for measures of objective visual complexity, also implicated as confounding to the investigation of memory. This article introduces a collection of emotional and neutral colour images which can be organised flexibly according to experimental requirements. These stimuli are made freely available for non-commercial use within the scientific community.

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The Effects of Social Stress on Memory: If, How and When

Physical stress, such as from the cold-pressor test, has been robustly associated with altered memory retrieval, but it is not yet 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 stepped replication design, with four near-identical experiments, each differing by a single critical factor. In three experiments we induced psychosocial stress after participants encoded word stimuli, then assessed retrieval after a prolonged delay. These experiments found no group level influence of postencoding stress on recognition of neutral words or cued recall of word-pairs, but a small effect on recollection of semantically-related words. There was, however, some indication of 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. Overall, our findings demonstrate that psychosocial stress has a typically modest impact on memory, lower than previously claimed, but that individual differences in stress responsivity, particularly for tasks that tap recollection, may help to explain variability in previous findings.

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The use of 'artificial saliva' as a neutral control condition in gustatory research

Distilled water with NaHCO3 and KCl, a solution often referred to as artificial saliva because its chemical composition mimics human saliva, is the control liquid of choice in gustatory research, because it is believed to be entirely affectively neutral. Yet evidence that human research volunteers perceive this liquid as emotionally neutral is lacking. Unpublished data from our lab suggested that this solution might be perceived as aversive. This study set out to systematically test the parameters influencing taste neutrality. We used two different concentrations of distilled water with NaHCO3 and KCl, as well as bottled water as a control taste. Healthy adults rated all tastes on two separate scales to rule out an interpretation based on the specifics of a single scale. Our participants rated artificial saliva as aversive on both scales. The bottled water was rated as neutral on both scales, and as significantly less intense in sensation than both concentrations of the distilled water solution. This is the first study to have directly tested the subjective feelings that accompany the ingestion of these oft-used solutions. We found that these liquids, which were previously assumed to be neutral, may not be perceived as such by research participants. Therefore, future gustatory studies should take care when using this solution as a neutral baseline. It is advised that trial-by-trial ratings are collected. Also, depending on the nature of future studies, bottled water may be considered as a preferable neutral baseline.

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A new test of value-modulated attentional bias in mice

The allocation of attention can be modulated by the emotional value of a stimulus. In order to understand the biasing influence of emotion on attention allocation further, we require an animal test of how motivational salience modulates attention. In mice, female odour triggers arousal and elicits emotional responses in males. Here, we determined the extent to which objects labelled with female odour modulated the attention of C57BL/6J male mice. Seven experiments were conducted, using a modified version of the spontaneous Novel Object Recognition task. Attention was operationalised as differential exploration time of identical objects that were labelled with either female mouse odour (O+), a non-social odour, almond odour (Oa) or not labelled with any odour (O-). In some experiments we tested trial unique (novel) objects than never carried an odour (X-). We found that when single objects were presented, as well as when two objects were presented simultaneously (so competed with each other for attention), O+ received preferential attention compared to O-. This result was independent of whether O+ was at a novel or familiar location. When compared with Oa at a novel location, O+ at a familiar location attracted more attention. Compared to X-, O+ received more exploration only when placed at a novel location, but attention to O+ and X- was equivalent when they were placed in a familiar location. These results suggest that C57BL/6J male mice weigh up aspects of odour, object novelty and special novelty for motivational salience, and that, in some instances, female odour elicits more attention (object exploration) compared to other olfactory stimuli and visual object novelty. The findings of this study pave the way to using motivationally-significant odours to modulate the cognitive processes that give rise to novel object recognition.

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Boundary effects of expectation in human pain perception

Perception of sensory stimulation is influenced by numerous psychological variables. One example is placebo analgesia, where expecting low pain causes a painful stimulus to feel less painful. Yet, because pain evolved to signal threats to survival, it should be maladaptive for highly-erroneous expectations to yield unrealistic pain experiences. Therefore, we hypothesised that a cue followed by a highly discrepant stimulus intensity, which generates a large prediction error, will have a weaker influence on the perception of that stimulus. To test this hypothesis we collected two independent pain-cueing datasets. The second dataset and the analysis plan were preregistered (osf.io/5r6z7). Regression modelling revealed that reported pain intensities were best explained by a quartic polynomial model of the prediction error. The results indicated that the influence of cues on perceived pain decreased when stimulus intensity was very different from expectations, suggesting that prediction error size has an immediate functional role in pain perception.

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In for a pound, in for a penny: How the opportunity to gain reward influences the competition for memory resources

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 both during encoding and retrieval. We tested this prediction in two experiments. Participants were promised {pound}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 one minute and in Experiment 2, also after 24 hours. Memory at 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-hour retention interval compared to items studied in other conditions, but reward did not modulate the forgetting rate, a null effect which should be replicated in a larger sample. These results confirm eCMRs predictions, although further research is required to compare that model against alternatives.

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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 resources can be productively described with a terminology that is more often applied to the control of overt behaviours, namely, the distinction between instrumental and Pavlovian control, and between model-free and model-based control. While 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 CSs, one that predicted pain (CS+) and one that predicted safety (CS-). Instructions given prior to the test stage in the task 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-. Because task design precluded model-free or instrumental control this result demonstrates a model-based Pavlovian control of VMAC. It confirms, in the domain of internal resource allocation, the model-based Pavlovian control of incentive behaviour and underlines the potential transformative role of information as an emotion regulation technique.

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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 (2B-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.

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Sensitivity to Pain Expectations: A Bayesian Model of Individual Differences

The thoughts and feelings people have about pain (referred to as pain expectations) are known to alter the perception of pain. However little is known about the cognitive processes that underpin pain expectations, or what drives the differing effect that pain expectations have between individuals. This paper details the testing of a model of pain perception which formalises the response to pain in terms of a Bayesian prior-to-posterior updating process. Using data acquired from a short and deception-free predictive cue task, it was found that this Bayesian model predicted ratings of pain better than other, simpler models. At the group level, the results confirmed two core predictions of predictive coding; that expectation alters perception and that increased uncertainty in the expectation reduces its impact on perception. The addition to the model of parameters relating to trait differences in pain expectation, improved its fit, suggesting that such traits play a significant role in perception beyond those expectations triggered by the pain cue. When model parameters were allowed to vary by participant, the models fit improved further. This final model produced a characterisation of each individuals sensitivity to pain expectations. This model is relevant for the understanding of the cognitive basis of pain expectations and could potentially act as a useful tool for guiding patient stratification and clinical experimentation.

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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.

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Temporal dissociation of salience and prediction error responses to appetitive and aversive taste

The feedback-related negativity, a frontocentral event-related potential (ERP) occurring 200350 milliseconds (ms) after emotionally-valued outcomes, has been posited as the neural correlate of reward prediction error, a key component of associative learning. Recent evidence challenged this interpretation and has led to the suggestion that this ERP expresses salience, instead. Here we distinguish between utility prediction error and salience by delivering or withholding hedonistically matched appetitive and aversive tastes, and measure ERPs to cues signalling each taste. We observed a typical FRN (computed as the loss-minus-gain difference wave) to appetitive taste, but a reverse-FRN to aversive taste. When tested axiomatically, frontocentral ERPs showed a salience response across tastes, with a particularly early response to outcome delivery, supporting recent propositions of a fast, unsigned and unspecific response to salient stimuli. ERPs also expressed aversive prediction error peaking at 285ms, which conformed to the logic of an axiomatic model of prediction error. With stimuli that most resemble those used in animal models we did not detect any frontocentral ERP signal for utility prediction error, in contrast with dominant views of the functional role of the feedback-related negativity ERP. We link the animal and human literature and present a challenge for current perspectives on associative learning research using ERPs.

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Local context influences memory for emotional stimuli but not electrophysiological markers of emotion-dependent attention

Emotional Enhancement of free recall can be context dependent. It is readily observed when emotional and neutral scenes are encoded and recalled together, in a mixed list, but diminishes when these scenes are encoded separately, in pure lists. We examined the hypothesis that this effect is due to differences of allocation of attention to neutral stimuli according to whether they are presented in mixed or pure lists, especially when encoding is intentional. Using picture stimuli that were controlled for semantic relatedness, our results contradicted this hypothesis. The amplitude of well-known electrophysiological markers of emotion-related attention - the Early Posterior Negativity (EPN), the Late Positive Potential (LPP), and the Slow Wave (SW) - was higher for emotional stimuli. Crucially, the emotional modulation of these ERPs was insensitive to list context, observed equally in pure and mixed lists. Although list context did not modulate neural markers of emotion-related attention, list context did modulate the effect of emotion on free recall. The apparent decoupling of the emotional effects on attention and memory challenges existing hypotheses accounting for the emotional enhancement of memory. We close by discussing whether findings are more compatible with an alternative hypothesis, where the magnitude of emotional memory enhancement is, at least in part, a consequence of retrieval dynamics.

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