Acute psychosocial stress modulates neural and behavioral substrates of cognitive control.

Acute psychosocial stress affects learning, memory, and attention, but the evidence for the influence of stress on the neural processes supporting cognitive control remains mixed. We investigated how acute psychosocial stress influences performance and neural processing during the Go/NoGo task-an established cognitive control task. The experimental group underwent the Trier Social Stress Test (TSST) acute stress induction, whereas the control group completed personality questionnaires. Then, participants completed a functional magnetic resonance imaging (fMRI) Go/NoGo task, with self-report, blood pressure and salivary cortisol measurements of induced stress taken intermittently throughout the experimental session. The TSST was successful in eliciting a stress response, as indicated by significant Stress > Control between-group differences in subjective stress ratings and systolic blood pressure. We did not identify significant differences in cortisol levels, however. The stress induction also impacted subsequent Go/NoGo task performance, with participants who underwent the TSST making fewer commission errors on trials requiring the most inhibitory control (NoGo Green) relative to the control group, suggesting increased vigilance. Univariate analysis of fMRI task-evoked brain activity revealed no differences between stress and control groups for any region. However, using multivariate pattern analysis, stress and control groups were reliably differentiated by activation patterns contrasting the most demanding NoGo trials (i.e., NoGo Green trials) versus baseline in the medial intraparietal area (mIPA, affiliated with the dorsal attention network) and subregions of the cerebellum (affiliated with the default mode network). These results align with prior reports linking the mIPA and the cerebellum to visuomotor coordination, a function central to cognitive control processes underlying goal-directed behavior. This suggests that stressor-induced hypervigilance may produce a facilitative effect on response inhibition which is represented neurally by the activation patterns of cognitive control regions.

Subjective valuation of performance feedback is robust to trait cognitive fatigue in multiple sclerosis.

BACKGROUND: Performance feedback is vital to rehabilitation interventions that treat cognitive impairments from multiple sclerosis (MS). Optimal treatment relies on participants' motivation to learn from feedback throughout these interventions. Cognitive fatigue, a prevalent symptom of MS, is associated with aberrant reward processing, which necessitates research into how fatigue affects perceived reward value of feedback in these individuals. The current study investigated how trait fatigue influences subjective valuation of feedback and subsequent feedback-seeking behavior in people with MS. METHODS: 33 MS and 32 neurotypical (NT) participants completed a willingness-to-pay associative memory paradigm that assessed feedback valuation via trial-by-trial decisions to either purchase or forego feedback in service of maximizing a performance-contingent monetary reward. Participant ratings of trait fatigue were also collected. Generalized logistic mixed modeling was used to analyze factors that influenced trial-wise feedback purchase decisions and task performance. RESULTS: Despite reporting greater trait fatigue, MS participants purchased comparable amounts of feedback as NT participants. Like NT participants, MS participants were more likely to purchase feedback when they were less confident about response accuracy. MS participants also performed comparably to NT participants, who both particularly benefited from purchase decisions that yielded negative feedback (i.e., indicating a response error). CONCLUSIONS: Trait cognitive fatigue may not impact performance feedback valuation in people with MS. Nonetheless, confidence in performance may drive their feedback-seeking behavior and may serve as a target for improving learning throughout cognitive rehabilitation and maximizing treatment success.

Altered functional connectivity during performance feedback processing in multiple sclerosis.

Effective learning from performance feedback is vital for adaptive behavior regulation necessary for successful cognitive performance. Yet, how this learning operates in clinical groups that experience cognitive dysfunction is not well understood. Multiple sclerosis (MS) is an autoimmune, degenerative disease of the central nervous system characterized by physical and cognitive dysfunction. A highly prevalent impairment in MS is cognitive fatigue (CF). CF is associated with altered functioning within cortico-striatal regions that also facilitate feedback-based learning in neurotypical (NT) individuals. Despite this cortico-striatal overlap, research about feedback-based learning in MS, its associated neural underpinnings, and its sensitivity to CF, are all lacking. The present study investigated feedback-based learning ability in MS, as well as associated cortico-striatal function and connectivity. MS and NT participants completed a functional magnetic resonance imaging (fMRI) paired-word association task during which they received trial-by-trial monetary, non-monetary, and uninformative performance feedback. Despite reporting greater CF throughout the task, MS participants displayed comparable task performance to NTs, suggesting preserved feedback-based learning ability in the MS group. Both groups recruited the ventral striatum (VS), caudate nucleus, and ventromedial prefrontal cortex in response to the receipt of performance feedback, suggesting that people with MS also recruit cortico-striatal regions during feedback-based learning. However, compared to NT participants, MS participants also displayed stronger functional connectivity between the VS and task-relevant regions, including the left angular gyrus and right superior temporal gyrus, in response to feedback receipt. Results indicate that CF may not interfere with feedback-based learning in MS. Nonetheless, people with MS may recruit alternative connections with the striatum to assist with this form of learning. These findings have implications for cognitive rehabilitation treatments that incorporate performance feedback to remediate cognitive dysfunction in clinical populations.

Neural responses to negative events and subsequent persistence behavior differ in individuals recovering from opioid use disorder compared to controls.

Background: Negative emotion is associated with substance craving and use in individuals recovering from substance use disorders, including prescription opioid use disorder (POUD). Decisions to abandon or persist towards a goal after negative emotion-eliciting events, and neural responses that shape such decisions, may be important in maintaining recovery from POUD.Objectives: We examined differences in neural responses to negative events and subsequent persistence decisions in individuals recovering from POUD without a history of a substance use disorder. Methods: 20 individuals with POUD (POUD group: 4 females, abstinent 2-3 weeks after admission to an inpatient treatment facility post-detoxification, no other substance use disorder), and 20 individuals with no substance use history (control group: 6 females) completed a persistence-after-setbacks task during functional magnetic resonance imaging. Participants advanced along a path toward a reward; after encountering each negative event (i.e., progress-erasing setback), participants made decisions to persist or abandon the path. Persistence decision rates were compared between groups and blood-oxygen-level-dependent signal to negative events was analyzed within a striatum region of interest (ROI) as well as whole-brain.Results: The POUD group persisted less (t(38) = 2.293, p = .028, d = .725) and showed lower striatum (left ventral putamen) signal to negative events compared to the control group (p < .05, corrected for striatum ROI).Conclusions: In POUD, neural and behavioral responses to negative events differ from controls. These differences are a target for research to address whether POUD treatment increases persistence and striatum responses to negative events and improves recovery outcomes.

Variability in the analysis of a single neuroimaging dataset by many teams.

Data analysis workflows in many scientific domains have become increasingly complex and flexible. Here we assess the effect of this flexibility on the results of functional magnetic resonance imaging by asking 70 independent teams to analyse the same dataset, testing the same 9 ex-ante hypotheses1. The flexibility of analytical approaches is exemplified by the fact that no two teams chose identical workflows to analyse the data. This flexibility resulted in sizeable variation in the results of hypothesis tests, even for teams whose statistical maps were highly correlated at intermediate stages of the analysis pipeline. Variation in reported results was related to several aspects of analysis methodology. Notably, a meta-analytical approach that aggregated information across teams yielded a significant consensus in activated regions. Furthermore, prediction markets of researchers in the field revealed an overestimation of the likelihood of significant findings, even by researchers with direct knowledge of the dataset2-5. Our findings show that analytical flexibility can have substantial effects on scientific conclusions, and identify factors that may be related to variability in the analysis of functional magnetic resonance imaging. The results emphasize the importance of validating and sharing complex analysis workflows, and demonstrate the need for performing and reporting multiple analyses of the same data. Potential approaches that could be used to mitigate issues related to analytical variability are discussed.

Effects of Expressive Writing on Neural Processing During Learning.

Expressive writing about past negative events has been shown to lead to a slew of positive outcomes. However, little is known about why writing about something negative would have positive effects. While some have posited that telling a narrative of a past negative event or current anxiety "frees up" cognitive resources, allowing individuals to focus more on the task at hand, there is little neural evidence suggesting that expressive writing has an effect on cognitive load. Moreover, little is known about how individual differences in the content of expressive writing could affect neural processing and the cognitive benefits writing confers. In our experiment, we compared brain activity in a group that had engaged in expressive writing vs. a control group, during performance on a feedback-based paired-associate word-learning task. We found that across groups, differential activation in the dorsal striatum in response to positive vs. negative feedback significantly predicted better later memory. Moreover, writing about a past failure resulted in more activation relative to the control group during the learning task in the mid-cingulate cortex (MCC), an area of the brain crucial to processing negative emotion. While our results do not provide support for the assertion that expressive writing alters attentional processing, our findings suggest that choosing to write about particularly intense past negative experiences like a difficult past failure may have resulted in changes in neural activation during task processing.

Ventromedial prefrontal cortex contributes to performance success by controlling reward-driven arousal representation in amygdala.

When preparing for a challenging task, potential rewards can cause physiological arousal that may impair performance. In this case, it is important to control reward-driven arousal while preparing for task execution. We recently examined neural representations of physiological arousal and potential reward magnitude during preparation, and found that performance failure was explained by relatively increased reward representation in the left caudate nucleus and arousal representation in the right amygdala (Watanabe, et al., 2019). Here we examine how prefrontal cortex influences the amygdala and caudate to control reward-driven arousal. Ventromedial prefrontal cortex (VMPFC) exhibited activity that was negatively correlated with trial-wise physiological arousal change, which identified this region as a potential modulator of amygdala and caudate. Next we tested the VMPFC - amygdala - caudate effective network using dynamic causal modeling (Friston et al., 2003). Post-hoc Bayesian model selection (Friston and Penny, 2011) identified a model that best fit data, in which amygdala activation was suppressively controlled by the VMPFC only in success trials. Furthermore, fixed connectivity strength from VMPFC to amygdala explained individual task performance. These findings highlight the role of effective connectivity from VMPFC to amygdala in order to control arousal during preparation for successful performance.

Reward-Driven Arousal Impacts Preparation to Perform a Task via Amygdala-Caudate Mechanisms.

Preparing for a challenging task can increase physiological arousal, in particular when potential incentives are large (e.g., a solo musical performance in front of an audience). Here, we examine how potential reward and its influence on arousal, measured by pupil dynamics, are represented in the brain while preparing for a challenging task. We further ask how neural representations during preparation relate to actual performance. Trials resulting in performance failure were characterized by increased pupil dilation as a function of increasing reward magnitude during preparation. Such failure trials were also associated with activation of the right amygdala representing pupil dilation, and the left caudate representing reward magnitude. Notably, increases in functional connectivity between amygdala and caudate preceded performance failure. These findings highlight increased connectivity between neural regions representing reward and arousal in circumstances where reward-driven arousal impairs performance.

Perceived control alters the effect of acute stress on persistence.

We often encounter setbacks while pursuing our goals. Success requires that we cope with these negative outcomes and choose to persist in spite of them. For example, learners may be more likely to continue a course after failing an assessment if they control their emotional reactions to the setback and study harder. However, the ability to effectively cope with the negative emotion inherent in such setbacks can be compromised by acute stress present in daily life (e.g., struggles in the household), which can subsequently lead to problems with persisting with a goal. The present study examined whether increasing the perception of control over setbacks (e.g., belief that a setback was caused by a correctable mistake rather than uncontrollable factors) can guard against the influence of a prior acute stressor on reactions to setbacks. Participants underwent a socially evaluated cold water stress or a nonstress control procedure. Afterward, they performed a behavioral task designed to measure persistence through controllable and uncontrollable setbacks. We observed that exposure to an acute stressor led to a detrimental effect on decision making by decreasing persistence behavior. Importantly, we also observed that the perception of control protected against the effect of preexisting stress and helped promote persistence. That is, stress impaired persistence through uncontrollable setbacks, but the impairment was alleviated by presenting setbacks as controllable. The findings demonstrate a potential avenue for improving the maintenance of goals aimed at behavior change, which can be susceptible to effects of stress.

Savoring the past: positive memories evoke value representations in the striatum.

Reminders of happy memories can bring back pleasant feelings tied to the original experience, suggesting an intrinsic value in reminiscing about the positive past. However, the neural circuitry underlying the rewarding aspects of autobiographical memory is poorly understood. Using fMRI, we observed enhanced activity during the recall of positive relative to neutral autobiographical memories in corticostriatal circuits that also responded to monetary reward. Enhanced activity in the striatum and medial prefrontal cortex was associated with increases in positive emotion during recall, and striatal engagement further correlated with individual measures of resiliency. Striatal response to the recall of positive memories was greater in individuals whose mood improved after the task. Notably, participants were willing to sacrifice a more tangible reward, money, in order to reminisce about positive past experiences. Our findings suggest that recalling positive autobiographical memories is intrinsically valuable, which may be adaptive for regulating positive emotion and promoting better well-being.

Perceived control influences neural responses to setbacks and promotes persistence.

How do people cope with setbacks and persist with their goals? We examine how perceiving control over setbacks alters neural processing in ways that increase persistence through adversity. For example, a student might retake a class if initial failure was due to controllable factors (e.g., studying) but give up if failure was uncontrollable (e.g., unfair exam questions). Participants persisted more when they perceived control over setbacks, and when they experienced increased negative affect to setbacks. Consistent with previous observations involving negative outcomes, ventral striatum and ventromedial prefrontal (VMPFC) activity was decreased in response to setbacks. Critically, these structures represented distinct neural mechanisms for persistence through adversity. Ventral striatum signal change to controllable setbacks correlated with greater persistence, whereas VMPFC signal change to uncontrollable setbacks mediated the relationship between increased negative affect and persistence. Taken together, the findings highlight how people process setbacks and adapt their behavior for future goal pursuit.

The social brain and reward: social information processing in the human striatum.

In the highly social life of humans, rewards that are sought and experienced are intertwined with social relationships and interactions between people. Just as we value nonsocial rewards such as food or money, we also value social outcomes (e.g., praise from a superior). We use social information to evaluate and form expectations of others and to make decisions involving others. Here we review research demonstrating how the neural circuitry of reward, particularly the striatum, is also involved in processing social information and making decisions in social situations. This research provides an understanding of the neural basis for social behavior from the perspective of how we evaluate social experiences and how our social interactions and decisions are motivated. We review research addressing the common neural systems underlying evaluation of social and nonsocial rewards. The human striatum, known to play a key role in reward processing, displays signals related to a broad spectrum of social functioning, including evaluating social rewards, making decisions influenced by social factors, learning about social others, cooperating, competing, and following social norms. WIREs Cogn Sci 2014, 5:61-73. doi: 10.1002/wcs.1266 Conflict of interest: The authors have declared no conflicts of interest for this article. For further resources related to this article, please visit the WIREs website.

Dissociable neural modulation underlying lasting first impressions, changing your mind for the better, and changing it for the worse.

Unattractive job candidates face a disadvantage when interviewing for a job. Employers' evaluations are colored by the candidate's physical attractiveness even when they take job interview performance into account. This example illustrates unexplored questions about the neural basis of social evaluation in humans. What neural regions support the lasting effects of initial impressions (even after getting to know someone)? How does the brain process information that changes our minds about someone? Job candidates' competence was evaluated from photographs and again after seeing snippets of job interviews. Left lateral orbitofrontal cortex modulation serves as a warning signal for initial reactions that ultimately undermine evaluations even when additional information is taken into account. The neural basis of changing one's mind about a candidate is not a simple matter of computing the amount of competence-affirming information in their job interview. Instead, seeing a candidate for the better is somewhat distinguishable at the neural level from seeing a candidate for the worse. Whereas amygdala modulation marks the extremity of evaluation change, favorable impression change additionally draws on parametric modulation of lateral prefrontal cortex and unfavorable impression change additionally draws on parametric modulation of medial prefrontal cortex, temporal cortex, and striatum. Investigating social evaluation as a dynamic process (rather than a one-time impression) paints a new picture of its neural basis and highlights the partially dissociable processes that contribute to changing your mind about someone for the better or the worse.

Unpacking the neural associations of emotion and judgment in emotion-congruent judgment.

The current study takes a new approach to understand the neural systems that support emotion-congruent judgment. The bulk of previous neural research has inferred emotional influences on judgment from disadvantageous judgments or non-random individual differences. The current study manipulated the influence of emotional information on judgments of stimuli that were equivocally composed of positive and negative attributes. Emotion-congruent processing was operationalized in two ways: neural activation significantly associated with primes that lead to emotionally congruent judgments and neural activation significantly associated with judgments that were preceded by emotionally congruent primes. Distinct regions of medial orbitofrontal cortex were associated with these patterns of emotion-congruent processing. Judgments that were incongruent with preceding primes were associated with dorsomedial prefrontal cortex, ventrolateral prefrontal cortex and lateral orbitofrontal cortex activity. The current study demonstrates a new approach to investigate the neural systems associated with emotion-congruent judgment. The findings suggest that medial OFC may support attentional processes that underlie emotion-congruent judgment.

Taking a different perspective: mindset influences neural regions that represent value and choice.

Most choices are complex and can be considered from a number of different perspectives. For example, someone choosing a snack may have taste, health, cost or any number of factors at the forefront of their mind. Although previous research has examined neural systems related to value and choice, very little is known about how mindset influences these systems. In the current study, participants were primed with Health or Taste while they made decisions about snack foods. Some neural regions showed consistent associations with value and choice across Health or Taste mindsets. Regardless of mindset, medial orbitofrontal cortex (MOFC) tracked value in terms of taste, regions in left lateral prefrontal cortex (LPFC) tracked value in terms of health, and MOFC and dorsal anterior cingulate were associated with choice. However, activity in other neural regions was modulated by the mindset manipulation. When primed with Taste, rostral anterior cingulate tracked value in terms of taste whereas left amygdala and left putamen were associated with choice. When primed with Health, right LPFC and posterior MOFC tracked value in terms of health. The findings contribute to the neural research on decision-making by demonstrating that changing perspectives can modulate value- and choice-related neural activity.

Taking a gamble or playing by the rules: dissociable prefrontal systems implicated in probabilistic versus deterministic rule-based decisions.

A decision may be difficult because complex information processing is required to evaluate choices according to deterministic decision rules and/or because it is not certain which choice will lead to the best outcome in a probabilistic context. Factors that tax decision making such as decision rule complexity and low decision certainty should be disambiguated for a more complete understanding of the decision making process. Previous studies have examined the brain regions that are modulated by decision rule complexity or by decision certainty but have not examined these factors together in the context of a single task or study. In the present functional magnetic resonance imaging study, both decision rule complexity and decision certainty were varied in comparable decision tasks. Further, the level of certainty about which choice to make (choice certainty) was varied separately from certainty about the final outcome resulting from a choice (outcome certainty). Lateral prefrontal cortex, dorsal anterior cingulate cortex, and bilateral anterior insula were modulated by decision rule complexity. Anterior insula was engaged more strongly by low than high choice certainty decisions, whereas ventromedial prefrontal cortex showed the opposite pattern. These regions showed no effect of the independent manipulation of outcome certainty. The results disambiguate the influence of decision rule complexity, choice certainty, and outcome certainty on activity in diverse brain regions that have been implicated in decision making. Lateral prefrontal cortex plays a key role in implementing deterministic decision rules, ventromedial prefrontal cortex in probabilistic rules, and anterior insula in both.

Neural responses to monetary incentives in major depression.

BACKGROUND: Reduced responsiveness to positive incentives is a central feature of Major Depressive Disorder (MDD). In the present study, we compared neural correlates of monetary incentive processing in unmedicated depressed participants and never-depressed control subjects. METHODS: Fourteen currently depressed and 12 never-depressed participants underwent functional magnetic resonance imaging while participating in a monetary incentive delay task. During the task, participants were cued to anticipate and respond to a rapidly presented target to gain or avoid losing varying amounts of money. RESULTS: Depressed and never-depressed participants did not differ in nucleus accumbens (NAcc) activation or in affective or behavioral responses during gain anticipation. Depressed participants did, however, exhibit increasing anterior cingulate activation during anticipation of increasing gains, whereas never-depressed participants showed increasing anterior cingulate activation during anticipation of increasing loss. Depressed participants also showed reduced discrimination of gain versus nongain outcomes. CONCLUSIONS: The present findings indicate that although unmedicated depressed individuals have the capacity to experience positive arousal and recruit NAcc activation during gain anticipation, they also exhibit increased anterior cingulate cortex activation, suggestive of increased conflict during anticipation of gains, in addition to showing reduced discrimination of gain versus nongain outcomes.