Dopaminergic error signals retune to social feedback during courtship.

Hunger, thirst, loneliness and ambition determine the reward value of food, water, social interaction and performance outcome1. Dopamine neurons respond to rewards meeting these diverse needs2-8, but it remains unclear how behaviour and dopamine signals change as priorities change with new opportunities in the environment. One possibility is that dopamine signals for distinct drives are routed to distinct dopamine pathways9,10. Another possibility is that dopamine signals in a given pathway are dynamically tuned to rewards set by the current priority. Here we used electrophysiology and fibre photometry to test how dopamine signals associated with quenching thirst, singing a good song and courting a mate change as male zebra finches (Taeniopygia guttata) were provided with opportunities to retrieve water, evaluate song performance or court a female. When alone, water reward signals were observed in two mesostriatal pathways but singing-related performance error signals were routed to Area X, a striatal nucleus specialized for singing. When courting a female, water seeking was reduced and dopamine responses to both water and song performance outcomes diminished. Instead, dopamine signals in Area X were driven by female calls timed with the courtship song. Thus the dopamine system handled coexisting drives by routing vocal performance and social feedback signals to a striatal area for communication and by flexibly re-tuning to rewards set by the prioritized drive.

Effort expenditure modulates feedback evaluations involving self-other agreement: evidence from brain potentials and neural oscillations.

The influence of effort expenditure on the subjective value in feedback involving material reward has been the focus of previous research. However, little is known about the impact of effort expenditure on subjective value evaluations when feedback involves reward that is produced in the context of social interaction (e.g. self-other agreement). Moreover, how effort expenditure influences confidence (second-order subjective value) in feedback evaluations remains unclear. Using electroencephalography, this study aimed to address these questions. Event-related potentials showed that, after exerting high effort, participants exhibited increased reward positivity difference in response to self-other (dis)agreement feedback. After exerting low effort, participants reported high confidence, and the self-other disagreement feedback evoked a larger P3a. Time-frequency analysis showed that the high-effort task evoked increased frontal midline theta power. In the low (vs. high)-effort task, the frontal midline delta power for self-other disagreement feedback was enhanced. These findings suggest that, at the early feedback evaluation stage, after exerting high effort, individuals exhibit an increased sensitivity of subjective value evaluation in response to self-other agreement feedback. At the later feedback evaluation stage, after completing the low-effort task, the self-other disagreement feedback violates the individuals'high confidence and leads to a metacognitive mismatch.

Get out of my head: social evaluative brain states carry over into post-feedback rest and influence remembering how others view us.

Learning how others perceive us helps us tune our behavior to form adaptive relationships. But which perceptions stick with us? And when in the learning process are they codified in memory? We leveraged a popular television series-The Office-to answer these questions. Prior to their functional magnetic resonance imaging (fMRI) session, viewers of The Office reported which characters they identified with, as well as which characters they perceived another person (i.e. counterpart) was similar to. During their fMRI scan, participants found out which characters other people thought they and the counterpart were like, and also completed rest scans. Participants remembered more feedback inconsistent with their self-views (vs. views of the counterpart). Although neural activity while encoding self-inconsistent feedback did not meaningfully predict memory, returning to the inconsistent self feedback during subsequent rest did. During rest, participants reinstated neural patterns engaged while receiving self-inconsistent feedback in the dorsomedial prefrontal cortex (DMPFC). DMPFC reinstatement also quadratically predicted self-inconsistent memory, with too few or too many reinstatements compromising memory performance. Processing social feedback during rest may impact how we remember and integrate the feedback, especially when it contradicts our self-views.

Performing a Motor Action Enhances Social Reward Processing and Modulates the Neural Processing of Predictive Cues.

Associative learning affects many areas of human behavior. Recently, we showed that the neural response to monetary reward is enhanced by performing an action, suggesting interactions between neural systems controlling motor behavior and reward processing. Given that many psychiatric disorders are associated with social anhedonia, a key open question is whether such effects generalize to social rewards, and in how far they affect associative learning. We developed a novel task in which participants (n = 66) received social reward feedback and social punishment either by pressing a button or waiting. Predictive cues were linked to feedback valence with 80% accuracy. Using EEG, we measured the neural response to both predictive cues and social feedback. We found enhanced reward positivity for social reward preceded by an action, and an enhanced N2 for cues predicting negative feedback. Cue-locked P3 amplitude was reduced for cues associated with negative feedback in passive trials only, showing a modulation of outcome anticipation by performing a motor action. This was supported by connectivity analyses showing stronger directed theta synchronization, in line with increased top-down modulation of attention, in active compared with passive trials. These findings suggest that actively obtaining social feedback enhances reward sensitivity and modulates outcome anticipation.

Concurrent behavioral modeling and multimodal neuroimaging reveals how feedback affects the performance of decision making in internet gaming disorder.

Internet gaming disorder (IGD) prompts inquiry into how feedback from prior gaming rounds influences subsequent risk-taking behavior and potential neural mechanisms. Forty-two participants, including 15 with IGD and 27 health controls (HCs), underwent a sequential risk-taking task. Hierarchy Bayesian modeling was adopted to measure risky propensity, behavioral consistence, and affection by emotion ratings from last trial. Concurrent electroencephalogram and functional near-infrared spectroscopy (EEG-fNIRS) recordings were performed to demonstrate when, where and how the previous-round feedback affects the decision making to the next round. We discovered that the IGD illustrated heightened risk-taking propensity as compared to the HCs, indicating by the computational modeling (p = 0.028). EEG results also showed significant time window differences in univariate and multivariate pattern analysis between the IGD and HCs after the loss of the game. Further, reduced brain activation in the prefrontal cortex during the task was detected in IGD as compared to that of the control group. The findings underscore the importance of understanding the aberrant decision-making processes in IGD and suggest potential implications for future interventions and treatments aimed at addressing this behavioral addiction.

The impact of social hierarchies on neural response to feedback evaluations after advice giving.

Advisors generally evaluate advisee-relevant feedback after advice giving. The response to these feedback-(1) whether the advice is accepted and (2) whether the advice is optimal-usually involves prestige. Prior literature has found that prestige is the basis by which individuals attain a superior status in the social hierarchy. However, whether advisors are motivated to attain a superior status when engaging in advice giving remains uncharacterized. Using event-related potentials, this study investigates how advisors evaluate feedback after giving advice to superior (vs. inferior) status advisees. A social hierarchy was first established based on two advisees (one was ranked as superior status and another as inferior status) as well as participants' performance in a dot-estimation task in which all participants were ranked as medium status. Participants then engaged in a game in which they were assigned roles as advisors to a superior or inferior status advisee. Afterward, the participants received feedback in two phases. In Phase 1, participants were told whether the advisees accepted the advice provided. In Phase 2, the participants were informed whether the advice they provided was correct. In these two phases, when the advisee was of superior status, participants exhibited stronger feedback-related negativity and P300 difference in response to (1) whether their advice was accepted, and (2) whether their advice was correct. Moreover, the P300 was notably larger when the participants' correct advice led to a gain for a superior-status advisee. In the context of advice giving, advisors are particularly motivated to attain a superior status when the feedback involving social hierarchies, which is reflected in higher sensitivity to feedback associated with superior status advisees at earlier and later stages during feedback evaluations in brains.

Beneficial effects of communicating intentions when delivering moral criticism: Cognitive and neural responses.

People often do not accept criticism on their morality, especially when delivered by outgroup members. In two preregistered studies, we investigated whether people become more receptive to such negative feedback when feedback senders communicate their intention to help. Participants received negative feedback from ostensible others on their selfish (rather than altruistic) decisions in a donation task. We manipulated the identity of a feedback sender (ingroup vs. outgroup) and the intention that they provided for giving feedback. A sender either did not communicate any intentions, indicated the intention to help the feedback receiver improve, or communicated the intention to show moral superiority. We measured participants' self-reported responses to the feedback (Study 1, N = 44) and additionally recorded an EEG in Study 2 (N = 34). Results showed that when no intentions were communicated, participants assumed worse intentions from outgroup senders than ingroup senders (Study 1). However, group membership had no significant effect once feedback senders made their intentions explicit. Moreover, across studies, when feedback senders communicated their intention to help, participants perceived feedback as less unfair compared with when senders tried to convey their moral superiority. Complementing these results, exploratory event-related potential results of Study 2 suggested that communicating the intention to help reduced participants' attentional vigilance toward negative feedback messages on their morality (i.e., decreased P200 amplitudes). These results demonstrate the beneficial effects of communicating the intention to help when one tries to encourage others' moral growth through criticism.

Effect of positive social comparative feedback on the resting state connectivity of dopaminergic neural pathways: A preliminary investigation.

Positive social comparative feedback is hypothesized to generate a dopamine response in the brain, similar to reward, by enhancing expectancies to support motor skill learning. However, no studies have utilized neuroimaging to examine this hypothesized dopaminergic mechanism. Therefore, the aim of this preliminary study was to investigate the effect of positive social comparative feedback on dopaminergic neural pathways measured by resting state connectivity. Thirty individuals practiced an implicit, motor sequence learning task and were assigned to groups that differed in feedback type. One group received feedback about their actual response time to complete the task (RT ONLY), while the other group received feedback about their response time with positive social comparison (RT + POS). Magnetic resonance imaging was acquired at the beginning and end of repetitive motor practice with feedback to measure practice-dependent changes in resting state brain connectivity. While both groups showed improvements in task performance and increases in performance expectancies, ventral tegmental area and the left nucleus accumbens (mesolimbic dopamine pathway) resting state connectivity increased in the RT + POS group but not in the RT ONLY group. Instead, the RT ONLY group showed increased connectivity between ventral tegmental area and primary motor cortex. Positive social comparative feedback during practice of a motor sequence task may induce a dopaminergic response in the brain along the mesolimbic pathway. However, given that absence of effects on expectancies and motor learning, more robust and individualized approaches may be needed to provide beneficial psychological and behavioral effects.

Willingness valued more than ability in partner choice: Insights into behavioral and ERP data.

In human cooperation, people prefer to choose partners with high willingness and ability-while both are valued by partners, individuals often prioritize willingness. Two event-related potential (ERP) experiments were conducted to discern the neural processes underpinning this preference. In the first experiment, participants made a choice between two potential partners and received feedback on the selected partner's willingness to cooperate. This was followed by feedback on the partner's task performance (ability) or a gambling outcome. In contrast, the second experiment first provided feedback on ability, then presented feedback on willingness or a gambling outcome. This study revealed that a potential partner's willingness trait significantly influences individuals' emotional evaluations and monetary allocations than the ability trait. Electrophysiological data indicated that low-willingness feedback elicited a diminished feedback-related negative (FRN) and an amplified P3 compared to high-willingness feedback. In contrast, no such difference was discernible between high- and low-ability feedback. Moreover, the P3 difference from high versus low willingness was considerably more pronounced than that from gambling outcomes, whereas the difference wave between high and low ability paralleled gambling outcomes. These findings bolster the novel finding that partner willingness may provide more substantial social rewards than ability. Furthermore, this study provides the first ERP evidence of willingness and ability trait perceptions in partner choice decisions.

Reward positivity affects temporal interval production in a continuous timing task.

The neural circuits of reward processing and interval timing (including the perception and production of temporal intervals) are functionally intertwined, suggesting that it might be possible for momentary reward processing to influence subsequent timing behavior. Previous animal and human studies have mainly focused on the effect of reward on interval perception, whereas its impact on interval production is less clear. In this study, we examined whether feedback, as an example of performance-contingent reward, biases interval production. We recorded EEG from 20 participants while they engaged in a continuous drumming task with different realistic tempos (1728 trials per participant). Participants received color-coded feedback after each beat about whether they were correct (on time) or incorrect (early or late). Regression-based EEG analysis was used to unmix the rapid occurrence of a feedback response called the reward positivity (RewP), which is traditionally observed in more slow-paced tasks. Using linear mixed modeling, we found that RewP amplitude predicted timing behavior for the upcoming beat. This performance-biasing effect of the RewP was interpreted as reflecting the impact of fluctuations in reward-related anterior cingulate cortex activity on timing, and the necessity of continuous paradigms to make such observations was highlighted.

The tail of the caudate is sensitive to both gain and loss feedback during information integration categorization.

Although most category learning studies use feedback for training, little attention has been paid to how individuals utilize feedback implemented as gains or losses during categorization. We compared skilled categorization under three different conditions: Gain (earn points for correct answers), Gain and Loss (earn points for correct answers and lose points for wrong answers) and Correct or Wrong (accuracy feedback only). We also manipulated difficulty and point value, with near boundary stimuli having the highest number of points to win or lose, and stimuli far from the boundary having the lowest point value. We found that the tail of the caudate was sensitive to feedback condition, with highest activity when both Gain and Loss feedback were present and least activity when only Gain or accuracy feedback was present. We also found that activity across the caudate was affected by distance from the decision bound, with greatest activity for the near boundary high value stimuli, and lowest for far low value stimuli. Overall these results indicate that the tail of the caudate is sensitive not only to positive rewards but also to loss and punishment, consistent with recent animal research finding tail of the caudate activity in aversive learning.

How does error correction occur during lexical learning?

We examined two theories of the mechanisms that enable error correction via corrective feedback. One theory focuses on enhancing the encoding of corrective feedback (corrective feedback-encoding facilitation account). The other is the recursive reminding theory, which considers memory integration between an initial event with error generation and a subsequent event involving correct answer feedback. The Japanese idiom pronunciation task was used in two experiments, in which it was manipulated whether the generated errors were visually presented, as well as corrective feedback. In an immediate retest after a five-minute retention interval, participants recalled their errors in the initial test and their correct answers. In addition, error trials fell into three ordinal confidence categories (low, medium, and high). First, a typical hypercorrection was replicated in which higher-confidence errors are more likely to be corrected. However, this was not observed when errors from the initial test were not recalled in the final test, which does not align with the corrective feedback-encoding facilitation account. The second issue was whether additional experience with the generated errors would enhance the error correction. Given the recursive reminding theory, the additional experience of errors should reinforce the mutual dependence between an error and the correct answer provided by feedback, improving cued recall performance later. This prediction is supported. The present findings suggest that the recursive reminding theory can explain the benefits of generating errors when learning through corrective feedback and can also be expanded to understand the hypercorrection effect.

The effect of mood on shaping belief and recollection following false feedback.

The current study examined how mood affects the impact of false feedback on belief and recollection. In a three-session experiment, participants first watched 40 neutral mini videos, which were accompanied by music to induce either a positive or negative mood, or no music. Following a recognition test, they received false feedback to reduce belief in the occurrence of the events displayed in some of the videos (Session 2). This was followed by an immediate memory test and a delayed memory assessment one week later (Session 3). The results revealed that participants in negative mood reported higher belief scores compared to those in positive moods, despite an overall decline in belief scores for all groups following the false feedback. Notably, individuals in negative moods exhibited less reduction in their belief scores after encountering challenges, thereby maintaining a higher accuracy in their testimonies. Over time, a reduction in the clarity of participants' memory recall was observed, which correspondingly reduced their testimony accuracy. This study thus indicates that mood states play a role in shaping belief and memory recall under the influence of false feedback.

Emotional cues reduce Pavlovian interference in feedback-based go and nogo learning.

It is easier to execute a response in the promise of a reward and withhold a response in the promise of a punishment than vice versa, due to a conflict between cue-related Pavlovian and outcome-related instrumental action tendencies in the reverse conditions. This robust learning asymmetry in go and nogo learning is referred to as the Pavlovian bias. Interestingly, it is similar to motivational tendencies reported for affective facial expressions, i.e., facilitation of approach to a smile and withdrawal from a frown. The present study investigated whether and how learning from emotional faces instead of abstract stimuli modulates the Pavlovian bias in reinforcement learning. To this end, 137 healthy adult participants performed an orthogonalized Go/Nogo task that fully decoupled action (go/nogo) and outcome valence (win points/avoid losing points). Three groups of participants were tested with either emotional facial cues whose affective valence was either congruent (CON) or incongruent (INC) to the required instrumental response, or with neutral facial cues (NEU). Relative to NEU, the Pavlovian bias was reduced in both CON and INC, though still present under all learning conditions. Importantly, only for CON, the reduction of the Pavlovian bias effect was adaptive by improving learning performance in one of the conflict conditions. In contrast, the reduction of the Pavlovian bias in INC was completely driven by decreased learning performance in non-conflict conditions. These results suggest a potential role of arousal/salience in Pavlovian-instrumental regulation and cue-action congruency in the adaptability of goal-directed behavior. Implications for clinical application are discussed.

Feedback timing-modulated weather prediction reveals relative deficits in both procedural and declarative learning in adults with dyslexia.

A topic of recent debate is the hypothesis that deficits associated with developmental disorders of language, such as reading disability, can be explained by a selective weakness in procedural memory. Adults with (n = 29; RD) and without (n = 29; TD) reading disability completed a weather prediction task under immediate and delayed feedback conditions, that rely on the striatal (procedural) and hippocampal (declarative) circuits, respectively. We examined trial-by-trial accuracy by feedback condition (immediate vs. delayed) and group (RD vs. TD). In the immediate feedback condition, we found the TD group to have a higher learning rate than the RD group. In the delayed feedback condition, we found the TD group reach a high level of accuracy early, and outperform the RD group for the duration of the task. The TD group also made gains in reaction time under both conditions, while the RD group slowed in their responses. Taken together, it appears that while procedural memory is indeed impaired in adults with reading disability, to a lesser extent, declarative memory is also affected. This lends partial support to the PDH, and more broadly to the position that reading disability is associated with general (non-linguistic) difficulties in learning.

Neural Sensitivity to Peer Feedback and Depressive Symptoms: Moderation by Executive Function.

Theories of adolescent development suggest that elevated neural sensitivity to social evaluation confers tradeoffs for adolescents' wellbeing, promoting adaptation to changing social contexts but increasing risk for emotional distress and depression. This study investigated whether the association between neural processing of peer feedback and depressive symptoms depends on teacher-reported executive function (EF) ability in adolescent girls. Girls showed activation to negative and positive peer feedback in regions implicated in social-emotional processing that interacted with EF to predict depressive symptoms. Specifically, activation predicted more depression in youth with poorer EF but less depression in youth with better EF, suggesting that the impact of increased social sensitivity may depend on youths' ability to regulate this sensitivity in adaptive ways.

Processing abnormalities in monetary outcome evaluations among male individuals with opioid use disorder: evidence from feedback-related negativity.

Background: Numerous studies have highlighted the pivotal role of alterations in the monetary reward system in the development and maintenance of substance use disorder (SUD). Although these alterations have been well documented in various forms of SUD, the electrophysiological mechanisms specific to opioid use disorder (OUD) remain underexplored. Understanding these mechanisms is critical for developing targeted interventions and advancing theories of addiction specific to opioid use.Objectives: To explore abnormalities in monetary reward outcome processing in males with OUD. We hypothesized that control individuals would show higher feedback-related negativity (FRN) to losses, unlike those in the OUD group, where FRN to losses and gains would not differ significantly.Methods: Fifty-seven participants (29 male individuals with OUD [heroin] and 28 male controls) were evaluated. A combination of the monetary incentive delay task (MIDT) and event-related potential (ERP) technology was used to investigate electrophysiological differences in monetary reward feedback processing between the OUD and healthy control groups.Results: We observed a significant interaction between group (control vs. OUD) and monetary outcome (loss vs. gain), indicated by p < .05 and η2p = 0.116. Specifically, control participants showed stronger negative FRN to losses than gains (p < .05), unlike the OUD group (p > .05).Conclusion: This study's FRN data indicate that males with OUD show altered processing of monetary rewards, marked by reduced sensitivity to loss. These findings offer electrophysiological insights into why males with OUD may pursue drugs despite potential economic downsides.

Getting off track: Cortical feedback processing network modulated by continuous error signal during target-feedback mismatch.

Performance monitoring and feedback processing - especially in the wake of erroneous outcomes - represent a crucial aspect of everyday life, allowing us to deal with imminent threats in the short term but also promoting necessary behavioral adjustments in the long term to avoid future conflicts. Over the last thirty years, research extensively analyzed the neural correlates of processing discrete error stimuli, unveiling the error-related negativity (ERN) and error positivity (Pe) as two main components of the cognitive response. However, the connection between the ERN/Pe and distinct stages of error processing, ranging from action monitoring to subsequent corrective behavior, remains ambiguous. Furthermore, mundane actions such as steering a vehicle already transgress the scope of discrete erroneous events and demand fine-tuned feedback control, and thus, the processing of continuous error signals - a topic scarcely researched at present. We analyzed two electroencephalography datasets to investigate the processing of continuous erroneous signals during a target tracking task, employing feedback in various levels and modalities. We observed significant differences between correct (slightly delayed) and erroneous feedback conditions in the larger one of the two datasets that we analyzed, both in sensor and source space. Furthermore, we found strong error-induced modulations that appeared consistent across datasets and error conditions, indicating a clear order of engagement of specific brain regions that correspond to individual components of error processing.

The neural correlates of continuous feedback processing.

Feedback processing is commonly studied by analyzing the brain's response to discrete rather than continuous events. Such studies have led to the hypothesis that rapid phasic midbrain dopaminergic activity tracks reward prediction errors (RPEs), the effects of which are measurable at the scalp via electroencephalography (EEG). Although studies using continuous feedback are sparse, recent animal work suggests that moment-to-moment changes in reward are tracked by slowly ramping midbrain dopaminergic activity. Some have argued that these ramping signals index state values rather than RPEs. Our goal here was to develop an EEG measure of continuous feedback processing in humans, then test whether its behavior could be accounted for by the RPE hypothesis. Participants completed a stimulus-response learning task in which a continuous reward cue gradually increased or decreased over time. A regression-based unmixing approach revealed EEG activity with a topography and time course consistent with the stimulus-preceding negativity (SPN), a scalp potential previously linked to reward anticipation and tonic dopamine release. Importantly, this reward-related activity depended on outcome expectancy: as predicted by the RPE hypothesis, activity for expected reward cues was reduced compared to unexpected reward cues. These results demonstrate the possibility of using human scalp-recorded potentials to track continuous feedback processing, and test candidate hypotheses of this activity.

Learning to Synchronize: Midfrontal Theta Dynamics during Rule Switching.

In recent years, several hierarchical extensions of well-known learning algorithms have been proposed. For example, when stimulus-action mappings vary across time or context, the brain may learn two or more stimulus-action mappings in separate modules, and additionally (at a hierarchically higher level) learn to appropriately switch between those modules. However, how the brain mechanistically coordinates neural communication to implement such hierarchical learning remains unknown. Therefore, the current study tests a recent computational model that proposed how midfrontal theta oscillations implement such hierarchical learning via the principle of binding by synchrony (Sync model). More specifically, the Sync model uses bursts at theta frequency to flexibly bind appropriate task modules by synchrony. The 64-channel EEG signal was recorded while 27 human subjects (female: 21, male: 6) performed a probabilistic reversal learning task. In line with the Sync model, postfeedback theta power showed a linear relationship with negative prediction errors, but not with positive prediction errors. This relationship was especially pronounced for subjects with better behavioral fit (measured via Akaike information criterion) of the Sync model. Also consistent with Sync model simulations, theta phase-coupling between midfrontal electrodes and temporoparietal electrodes was stronger after negative feedback. Our data suggest that the brain uses theta power and synchronization for flexibly switching between task rule modules, as is useful, for example, when multiple stimulus-action mappings must be retained and used.SIGNIFICANCE STATEMENT Everyday life requires flexibility in switching between several rules. A key question in understanding this ability is how the brain mechanistically coordinates such switches. The current study tests a recent computational framework (Sync model) that proposed how midfrontal theta oscillations coordinate activity in hierarchically lower task-related areas. In line with predictions of this Sync model, midfrontal theta power was stronger when rule switches were most likely (strong negative prediction error), especially in subjects who obtained a better model fit. Additionally, also theta phase connectivity between midfrontal and task-related areas was increased after negative feedback. Thus, the data provided support for the hypothesis that the brain uses theta power and synchronization for flexibly switching between rules.