Decreased associative processing and memory confidence in aphantasia.

Visual imagery and mental reconstruction of scenes are considered core components of episodic memory retrieval. Individuals with absent visual imagery (aphantasia) score lower on tests of autobiographical memory, suggesting that aphantasia may be associated with differences in episodic and associative processing. In this online study, we tested aphantasic participants and controls on associative recognition and memory confidence for three types of associations encoded incidentally: associations between visual-visual and audio-visual stimulus pairs, associations between an object and its location on the screen, and intraitem associations. Aphantasic participants had a lower rate of high-confidence hits in all associative memory tests compared with controls. Performance on auditory-visual associations was correlated with individual differences in a measure of object imagery in the aphantasic group but not in controls. No overall group difference in memory performance was found, indicating that visual imagery selectively contributes to memory confidence. Analysis of the encoding task revealed that aphantasics made fewer associative links between the stimuli, suggesting a role for visual imagery in associative processing of visual and auditory input. These data enhance our understanding of visual imagery contributions to associative memory and further characterize the cognitive profile of aphantasia.

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.

Behavioral specifications of reward-associated long-term memory enhancement in humans.

Recent functional imaging studies link reward-related activation of the midbrain substantia nigra-ventral tegmental area (SN/VTA), the site of origin of ascending dopaminergic projections, with improved long-term episodic memory. Here, we investigated in two behavioral experiments how (1) the contingency between item properties and reward, (2) the magnitude of reward, (3) the uncertainty of outcomes, and (4) the contextual availability of reward affect long-term memory. We show that episodic memory is enhanced only when rewards are specifically predicted by the semantic identity of the stimuli and changes nonlinearly with increasing reward magnitude. These effects are specific to reward and do not occur in relation to outcome uncertainty alone. These behavioral specifications are relevant for the functional interpretation of how reward-related activation of the SN/VTA, and more generally dopaminergic neuromodulation, contribute to long-term memory.

Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation.

Long-term potentiation in the hippocampus can be enhanced and prolonged by dopaminergic inputs from midbrain structures such as the substantia nigra. This improved synaptic plasticity is hypothesized to be associated with better memory consolidation in the hippocampus. We used a condition that reliably elicits a dopaminergic response, reward anticipation, to study the relationship between activity of dopaminergic midbrain areas and hippocampal long-term memory in healthy adults. Pictures of object drawings that predicted monetary reward were associated with stronger fMRI activity in reward-related brain areas, including the substantia nigra, compared with non-reward-predicting pictures. Three weeks later, recollection and source memory were better for reward-predicting than for non-reward-predicting pictures. FMRI activity in the hippocampus and the midbrain was higher for reward-predicting pictures that were later recognized compared with later forgotten pictures. These data are consistent with the hypothesis that activation of dopaminergic midbrain regions enhances hippocampus-dependent memory formation, possibly by enhancing consolidation.

Mesolimbic interaction of emotional valence and reward improves memory formation.

Animal studies suggest that dopaminergic neuromodulation is critical for hippocampal memory formation. Compatible with this notion, recent functional imaging evidence in humans showed that reward modulates the hippocampus-dependent formation of episodic memories through activation of areas belonging to the mesolimbic dopaminergic system, including the ventral striatum and substantia nigra/ventral tegmental area (SN/VTA). However, the amygdala is also closely embedded within this mesolimbic circuitry with reciprocal connections to the SN/VTA, raising the possibility that emotionally valenced stimuli might also interact with hippocampal encoding through dopaminergic neuromodulation. By the same token, emotional processing in the amygdala might be affected by reward-related processing in the mesolimbic system. In an event-related functional magnetic resonance imaging study, reward-related activity in the ventral striatum was enhanced by the concurrent presentation of emotionally positive but not emotionally negative stimuli. Emotional processing in the amygdala, on the other hand, was not affected by reward. One day after study, recollection of the positive stimuli was better when they were associated with reward at encoding as compared with unrewarded positive stimuli. The findings are compatible with the notion that the output of the reward system and memory formation in the hippocampus is influenced by positive emotional valence and suggest that the ventral striatum is a key structure for this modulation.

Ageing and early-stage Parkinson's disease affect separable neural mechanisms of mesolimbic reward processing.

The ability to learn stimulus-reward associations on the basis of reward prediction errors critically depends on the mesolimbic dopaminergic system including the dopaminergic midbrain and the ventral striatum. It is known that healthy elderly and patients with Parkinson's disease are less proficient than healthy young adults in learning stimulus-reward contingencies, but it is unclear whether this is due to dysfunctional mesolimbic reward prediction or due to deficiency in processing the rewards per se. We used a well-established event-related fMRI reward-prediction paradigm to address this question. Young adults showed the well-replicated pattern of midbrain and ventral striatal activation for stimuli that predicted monetary reward when compared with stimuli that predicted neutral feedback. Also, as expected, the predicted reward feedback itself did not elicit a mesolimbic response. Healthy elderly subjects and unmedicated early-stage idiopathic Parkinson's disease patients showed the opposite pattern with an absent mesolimbic reward prediction response, but mesolimbic activation to the reward feedback itself. This suggests that the healthy elderly and Parkinson's disease patients were less proficient in learning the predictive value of the reward cues despite preserved mesolimbic processing of reward prediction errors. Parkinson's disease patients additionally displayed a relatively increased response of the anterior cingulate during reward feedback processing and diminished functional connectivity of the midbrain and ventral striatum. Our results are compatible with existing behavioural evidence that both groups exhibit a particularly pronounced deficit in learning from positive feedback and support the view that a tendency to underestimate expected values of reward cues might underlie this deficit. Furthermore, alterations in reward processing in Parkinson's disease extend beyond accelerated ageing effects and include altered connectivity within the mesolimbic system.

Avoiding boredom: Caudate and insula activity reflects boredom-elicited purchase bias.

People show a strong tendency to avoid boring situations, but the neural systems mediating this behavioural bias are yet unknown. We used functional magnetic resonance imaging (fMRI) to investigate how the anticipation of a boring task influences decisions to purchase entertainment. Participants accepted higher prices to avoid boredom compared to control tasks, and individual differences in boredom experience predicted the increase in price. This behavioural bias was associated with higher activity in the caudate nucleus during music purchases driven by boredom avoidance. Insula activation was increased during performance of the boring task and subsequently associated with individual differences in boredom-related decision making. These results identify a mechanism that drives decisions to avoid boring situations and potentially underlies consumer decisions.

Memory Performance for Everyday Motivational and Neutral Objects Is Dissociable from Attention.

Episodic memory is typically better for items coupled with monetary reward or punishment during encoding. It is yet unclear whether memory is also enhanced for everyday objects with appetitive or aversive values learned through a lifetime of experience, and to what extent episodic memory enhancement for motivational and neutral items is attributable to attention. In a first experiment, we investigated attention to everyday motivational objects using eye-tracking during free-viewing and subsequently tested episodic memory using a remember/know procedure. Attention was directed more to aversive stimuli, as evidenced by longer viewing durations, whereas recollection was higher for both appetitive and aversive objects. In the second experiment, we manipulated the visual contrast of neutral objects through changes of contrast to further dissociate attention and memory encoding. While objects presented with high visual contrast were looked at longer, recollection was best for objects presented in unmodified, medium contrast. Generalized logistic mixed models on recollection performance showed that attention as measured by eye movements did not enhance subsequent memory, while motivational value (Experiment 1) and visual contrast (Experiment 2) had quadratic effects in opposite directions. Our findings suggest that an enhancement of incidental memory encoding for appetitive items can occur without an increase in attention and, vice versa, that enhanced attention towards salient neutral objects is not necessarily associated with memory improvement. Together, our results provide evidence for a double dissociation of attention and memory effects under certain conditions.

Attention in natural scenes: Affective-motivational factors guide gaze independently of visual salience.

In addition to low-level stimulus characteristics and current goals, our previous experience with stimuli can also guide attentional deployment. It remains unclear, however, if such effects act independently or whether they interact in guiding attention. In the current study, we presented natural scenes including every-day objects that differed in affective-motivational impact. In the first free-viewing experiment, we presented visually-matched triads of scenes in which one critical object was replaced that varied mainly in terms of motivational value, but also in terms of valence and arousal, as confirmed by ratings by a large set of observers. Treating motivation as a categorical factor, we found that it affected gaze. A linear-effect model showed that arousal, valence, and motivation predicted fixations above and beyond visual characteristics, like object size, eccentricity, or visual salience. In a second experiment, we experimentally investigated whether the effects of emotion and motivation could be modulated by visual salience. In a medium-salience condition, we presented the same unmodified scenes as in the first experiment. In a high-salience condition, we retained the saturation of the critical object in the scene, and decreased the saturation of the background, and in a low-salience condition, we desaturated the critical object while retaining the original saturation of the background. We found that highly salient objects guided gaze, but still found additional additive effects of arousal, valence and motivation, confirming that higher-level factors can also guide attention, as measured by fixations towards objects in natural scenes.

Motivational Objects in Natural Scenes (MONS): A Database of >800 Objects.

In daily life, we are surrounded by objects with pre-existing motivational associations. However, these are rarely controlled for in experiments with natural stimuli. Research on natural stimuli would therefore benefit from stimuli with well-defined motivational properties; in turn, such stimuli also open new paths in research on motivation. Here we introduce a database of Motivational Objects in Natural Scenes (MONS). The database consists of 107 scenes. Each scene contains 2 to 7 objects placed at approximately equal distance from the scene center. Each scene was photographed creating 3 versions, with one object ("critical object") being replaced to vary the overall motivational value of the scene (appetitive, aversive, and neutral), while maintaining high visual similarity between the three versions. Ratings on motivation, valence, arousal and recognizability were obtained using internet-based questionnaires. Since the main objective was to provide stimuli of well-defined motivational value, three motivation scales were used: (1) Desire to own the object; (2) Approach/Avoid; (3) Desire to interact with the object. Three sets of ratings were obtained in independent sets of observers: for all 805 objects presented on a neutral background, for 321 critical objects presented in their scene context, and for the entire scenes. On the basis of the motivational ratings, objects were subdivided into aversive, neutral, and appetitive categories. The MONS database will provide a standardized basis for future studies on motivational value under realistic conditions.

Reward and Novelty Enhance Imagination of Future Events in a Motivational-Episodic Network.

Thinking about personal future events is a fundamental cognitive process that helps us make choices in daily life. We investigated how the imagination of episodic future events is influenced by implicit motivational factors known to guide decision making. In a two-day functional magnetic resonance imaging (fMRI) study, we controlled learned reward association and stimulus novelty by pre-familiarizing participants with two sets of words in a reward learning task. Words were repeatedly presented and consistently followed by monetary reward or no monetary outcome. One day later, participants imagined personal future events based on previously rewarded, unrewarded and novel words. Reward association enhanced the perceived vividness of the imagined scenes. Reward and novelty-based construction of future events were associated with higher activation of the motivational system (striatum and substantia nigra/ ventral tegmental area) and hippocampus, and functional connectivity between these areas increased during imagination of events based on reward-associated and novel words. These data indicate that implicit past motivational experience contributes to our expectation of what the future holds in store.

Levodopa administration modulates striatal processing of punishment-associated items in healthy participants.

RATIONALE: Appetitive and aversive processes share a number of features such as their relevance for action and learning. On a neural level, reward and its predictors are associated with increased firing of dopaminergic neurons, whereas punishment processing has been linked to the serotonergic system and to decreases in dopamine transmission. Recent data indicate, however, that the dopaminergic system also responds to aversive stimuli and associated actions. OBJECTIVES: In this pharmacological functional magnetic resonance imaging study, we investigated the contribution of the dopaminergic system to reward and punishment processing in humans. METHODS: Two groups of participants received either placebo or the dopamine precursor levodopa and were scanned during alternating reward and punishment anticipation blocks. RESULTS: Levodopa administration increased striatal activations for cues presented in punishment blocks. In an interaction with individual personality scores, levodopa also enhanced striatal activation for punishment-predictive compared with neutral cues in participants scoring higher on the novelty-seeking dimension. CONCLUSIONS: These data support recent indications that dopamine contributes to punishment processing and suggest that the novelty-seeking trait is a measure of susceptibility to drug effects on motivation. These findings are also consistent with the possibility of an inverted U-shaped response function of dopamine in the striatum, suggesting an optimal level of dopamine release for motivational processing.

Prior fear conditioning and reward learning interact in fear and reward networks.

The ability to flexibly adapt responses to changes in the environment is important for survival. Previous research in humans separately examined the mechanisms underlying acquisition and extinction of aversive and appetitive conditioned responses. It is yet unclear how aversive and appetitive learning interact on a neural level during counterconditioning in humans. This functional magnetic resonance imaging (fMRI) study investigated the interaction of fear conditioning and subsequent reward learning. In the first phase (fear acquisition), images predicted aversive electric shocks or no aversive outcome. In the second phase (counterconditioning), half of the CS+ and CS- were associated with monetary reward in the absence of electric stimulation. The third phase initiated reinstatement of fear through presentation of electric shocks, followed by CS presentation in the absence of shock or reward. Results indicate that participants were impaired at learning the reward contingencies for stimuli previously associated with shock. In the counterconditioning phase, prior fear association interacted with reward representation in the amygdala, where activation was decreased for rewarded compared to unrewarded CS- trials, while there was no reward-related difference in CS+ trials. In the reinstatement phase, an interaction of previous fear association and previous reward status was observed in a reward network consisting of substantia nigra/ventral tegmental area (SN/VTA), striatum and orbitofrontal cortex (OFC), where activation was increased by previous reward association only for CS- but not for CS+ trials. These findings suggest that during counterconditioning, prior fear conditioning interferes with reward learning, subsequently leading to lower activation of the reward network.

Reprint of: DAT genotype modulates striatal processing and long-term memory for items associated with reward and punishment.

Previous studies have shown that appetitive motivation enhances episodic memory formation via a network including the substantia nigra/ventral tegmental area (SN/VTA), striatum and hippocampus. This functional magnetic resonance imaging (fMRI) study now contrasted the impact of aversive and appetitive motivation on episodic long-term memory. Cue pictures predicted monetary reward or punishment in alternating experimental blocks. One day later, episodic memory for the cue pictures was tested. We also investigated how the neural processing of appetitive and aversive motivation and episodic memory were modulated by dopaminergic mechanisms. To that end, participants were selected on the basis of their genotype for a variable number of tandem repeat polymorphism of the dopamine transporter (DAT) gene. The resulting groups were carefully matched for the 5-HTTLPR polymorphism of the serotonin transporter gene. Recognition memory for cues from both motivational categories was enhanced in participants homozygous for the 10-repeat allele of the DAT, the functional effects of which are not known yet, but not in heterozygous subjects. In comparison with heterozygous participants, 10-repeat homozygous participants also showed increased striatal activity for anticipation of motivational outcomes compared to neutral outcomes. In a subsequent memory analysis, encoding activity in striatum and hippocampus was found to be higher for later recognized items in 10-repeat homozygotes compared to 9/10-repeat heterozygotes. These findings suggest that processing of appetitive and aversive motivation in the human striatum involve the dopaminergic system and that dopamine plays a role in memory for both types of motivational information. In accordance with animal studies, these data support the idea that encoding of motivational events depends on dopaminergic processes in the hippocampus.

DAT genotype modulates striatal processing and long-term memory for items associated with reward and punishment.

Previous studies have shown that appetitive motivation enhances episodic memory formation via a network including the substantia nigra/ventral tegmental area (SN/VTA), striatum and hippocampus. This functional magnetic resonance imaging (fMRI) study now contrasted the impact of aversive and appetitive motivation on episodic long-term memory. Cue pictures predicted monetary reward or punishment in alternating experimental blocks. One day later, episodic memory for the cue pictures was tested. We also investigated how the neural processing of appetitive and aversive motivation and episodic memory were modulated by dopaminergic mechanisms. To that end, participants were selected on the basis of their genotype for a variable number of tandem repeat polymorphism of the dopamine transporter (DAT) gene. The resulting groups were carefully matched for the 5-HTTLPR polymorphism of the serotonin transporter gene. Recognition memory for cues from both motivational categories was enhanced in participants homozygous for the 10-repeat allele of the DAT, the functional effects of which are not known yet, but not in heterozygous subjects. In comparison with heterozygous participants, 10-repeat homozygous participants also showed increased striatal activity for anticipation of motivational outcomes compared to neutral outcomes. In a subsequent memory analysis, encoding activity in striatum and hippocampus was found to be higher for later recognized items in 10-repeat homozygotes compared to 9/10-repeat heterozygotes. These findings suggest that processing of appetitive and aversive motivation in the human striatum involve the dopaminergic system and that dopamine plays a role in memory for both types of motivational information. In accordance with animal studies, these data support the idea that encoding of motivational events depends on dopaminergic processes in the hippocampus.

Novelty seeking behaviour in Parkinson's disease.

Novelty seeking can be a positive trait leading to creativity and innovation, but it is also related to increased risk of damaging addictive behaviour. We have assessed novelty seeking with a three armed bandit task, in which novel stimuli were occasionally introduced, replacing choice options from which the participants had been choosing. This allowed us to assess whether or not they would be prone to selecting novel stimuli. We tested 25 non impulsive patients with Parkinson's disease (PD) and 27 PD patients with impulsive compulsive behaviours (ICBs). Both patient groups were examined "on" and "off" dopaminergic medication in a counterbalanced order and their behaviour was compared with 24 healthy controls. We found that PD patients with ICBs were significantly more prone to choose novel options than either non impulsive PD patients or controls, regardless of medication status. Our findings suggest that attraction to novelty is a personality trait in all PD patients with ICBs which is independent of medication status.

Functional imaging of the human dopaminergic midbrain.

Invasive recording of dopamine neurons in the substantia nigra and ventral tegmental area (SN/VTA) of behaving animals suggests a role for these neurons in reward learning and novelty processing. In humans, functional magnetic resonance imaging (fMRI) is currently the only non-invasive event-related method to measure SN/VTA activity, but it is debated to what extent fMRI enables inference about dopaminergic responses within the SN/VTA. We consider the anatomical and functional parcellation of the primate SN/VTA and find that its homogeneity suggests little variation in the regional specificity of fMRI signals for reward-related dopaminergic responses. Hence, these responses seem to be well captured by the compound fMRI signal from the SN/VTA, which seems quantitatively related to dopamine release in positron emission tomography (PET). We outline how systematic investigation of the functional parcellation of the SN/VTA in animals, new developments in fMRI analysis and combined PET-fMRI studies can narrow the gap between fMRI and dopaminergic neurotransmission.

Striatal activity underlies novelty-based choice in humans.

The desire to seek new and unfamiliar experiences is a fundamental behavioral tendency in humans and other species. In economic decision making, novelty seeking is often rational, insofar as uncertain options may prove valuable and advantageous in the long run. Here, we show that, even when the degree of perceptual familiarity of an option is unrelated to choice outcome, novelty nevertheless drives choice behavior. Using functional magnetic resonance imaging (fMRI), we show that this behavior is specifically associated with striatal activity, in a manner consistent with computational accounts of decision making under uncertainty. Furthermore, this activity predicts interindividual differences in susceptibility to novelty. These data indicate that the brain uses perceptual novelty to approximate choice uncertainty in decision making, which in certain contexts gives rise to a newly identified and quantifiable source of human irrationality.

Anticipation of novelty recruits reward system and hippocampus while promoting recollection.

The dopaminergic midbrain, which comprises the substantia nigra and ventral tegmental area (SN/VTA), plays a central role in reward processing. This region is also activated by novel stimuli, raising the possibility that novelty and reward have shared functional properties. It is currently unclear whether functional aspects of reward processing in the SN/VTA, namely, activation by unexpected rewards and cues that predict reward, also characterize novelty processing. To address this question, we conducted an fMRI experiment during which subjects viewed symbolic cues that predicted either novel or familiar images of scenes with 75% validity. We show that SN/VTA was activated by cues predicting novel images as well as by unexpected novel images that followed familiarity-predictive cues, an 'unexpected novelty' response. The hippocampus, a region implicated in detecting and encoding novel stimuli, showed an anticipatory novelty response but differed from the response profile of SN/VTA in responding at outcome to expected and 'unexpected' novelty. In a behavioral extension of the experiment, recollection increased relative to familiarity when comparing delayed recognition memory for anticipated novel stimuli with unexpected novel stimuli. These data reveal commonalities in SN/VTA responses to anticipating reward and anticipating novel stimuli. We suggest that this anticipatory response codes a motivational exploratory novelty signal that, together with anticipatory activation of the hippocampus, leads to enhanced encoding of novel events. In more general terms, the data suggest that dopaminergic processing of novelty might be important in driving exploration of new environments.