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.

The role of planfulness for well-being, stress, and goal disruption during COVID-19.

Planfulness refers to an individual's tendency to be future oriented, mentally flexible, and cognitively strategic when engaging with goals, and has been shown to predict goal completion. We investigated the relationships among planfulness, goal disruption, stress, and psychological well-being during the COVID-19 pandemic, which served as a unique setback context. We measured these constructs using the planfulness scale, an ad-hoc survey item probing goal disruption in the pandemic, the perceived stress scale, and the Warwick-Edinburgh Mental Wellbeing Scale, respectively. Participants were university students (N = 174; mean age 23.03, SD: 4.37; 77% female). Higher planfulness predicted lower goal-disruption, lower stress, and higher well-being during the pandemic, extending its benefits beyond the goal domain. High levels of planfulness did not protect against goal disruption among those participants in which the self-reported personal impact of the pandemic was highest. Differences in goal disruption across levels of planfulness were constrained to lower reported pandemic impact. However, the differences in psychological well-being and stress by levels of planfulness were retained even when self-reported perceptions of personal pandemic impact were high. More planful students maintained lower stress and higher psychological well-being than their less planful peers across levels of adversity. These findings suggest that even in extremely difficult contexts in which planfulness does not protect against goal disruption, it still confers personal benefits in terms of psychological health.

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.

Determining the effects of training duration on the behavioral expression of habitual control in humans: a multilaboratory investigation.

It has been suggested that there are two distinct and parallel mechanisms for controlling instrumental behavior in mammals: goal-directed actions and habits. To gain an understanding of how these two systems interact to control behavior, it is essential to characterize the mechanisms by which the balance between these systems is influenced by experience. Studies in rodents have shown that the amount of training governs the relative expression of these two systems: Behavior is goal-directed following moderate training, but the more extensively an instrumental action is trained, the more it becomes habitual. It is less clear whether humans exhibit similar training effects on the expression of goal-directed and habitual behavior, as human studies have reported contradictory findings. To tackle these contradictory findings, we formed a consortium, where four laboratories undertook a preregistered experimental induction of habits by manipulating the amount of training. There was no statistical evidence for a main effect of the amount of training on the formation and expression of habits. However, exploratory analyses suggest a moderating effect of the affective component of stress on the impact of training over habit expression. Participants who were lower in affective stress appeared to be initially goal-directed, but became habitual with increased training, whereas participants who were high in affective stress were already habitual even after moderate training, thereby manifesting insensitivity to overtraining effects. Our findings highlight the importance of the role of moderating variables such as individual differences in stress and anxiety when studying the experimental induction of habits in humans.

Demonstrating and disrupting well-learned habits.

Researchers have exerted tremendous efforts to empirically study how habits form and dominate at the expense of deliberation, yet we know very little about breaking these rigid habits to restore goal-directed control. In a three-experiment study, we first illustrate a novel approach of studying well-learned habits, in order to effectively demonstrate habit disruption. In Experiment 1, we use a Go/NoGo task with familiar color-response associations to demonstrate outcome-insensitivity when compared to novel, more flexible associations. Specifically, subjects perform more accurately when the required mapping is the familiar association of green-Go/red-NoGo than when it is red-Go/green-NoGo, confirming outcome-insensitive, habitual control. As a control condition, subjects show equivalent performance with unfamiliar color-response mappings (using the colors blue and purple mapped to Go and NoGo responses). Next, in Experiments 2 and 3, we test a motivation-based feedback manipulation in varying magnitudes (i.e., performance feedback with and without monetary incentives) to break the well-established habits elicited by our familiar stimuli. We find that although performance feedback prior to the contingency reversal test is insufficient to disrupt outcome-insensitivity in Experiment 2, a combination of performance feedback and monetary incentive is able to restore goal-directed control in Experiment 3, effectively breaking the habits. As the first successful demonstration of well-learned habit disruption in the laboratory, these findings provide new insights into how we execute and modify habits, while fostering new and translational research avenues that may be applicable to treating habit-based pathologies.

The neurobehavioral mechanisms of motivational control in attention-deficit/hyperactivity disorder.

Attention-deficit/hyperactivity disorder (ADHD) poses debilitating impairments in the neurobehavioral systems governing reward-related processes-key to the control of motivated behaviors. Individuals with ADHD may rely on a motivational control system that favors cue-driven habits-rooted in the posterior putamen-over caudate and prefrontal cortex-driven goal-directed behaviors. We examined the neurobehavioral correlates of motivational control in ADHD. Twenty-five adults with ADHD and 25 neurotypicals underwent fMRI while training on two stimulus-response-outcome associations. A devaluation procedure followed, whereby they were selectively satiated on one of the snack outcomes, decreasing its value. A subsequent extinction test determined outcome-sensitivity (i.e., whether responses towards devalued snack diminished). Despite behavioral similarities, the ADHD group displayed a distinct neural signature marked by enhanced posterior putamen activation as a function of training. This region also displayed diminished functional connectivity with the dorsal anterior cingulate cortex, which is associated with top-down control. Our whole-brain analysis yielded ADHD-specific posterior putamen and opercular/insular cortex activity over the course of training-regions associated with stimulus-sensitivity and maladaptively rigid behaviors, respectively. Neural comparisons also identified hyper-recruitment of the hippocampus in the ADHD group. These results highlight corticostriatal discrepancies in ADHD, possibly serving as a biomarker of the disorder.

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.

Habit Expression and Disruption as a Function of Attention-Deficit/Hyperactivity Disorder Symptomology.

Attention-deficit/hyperactivity disorder (ADHD) is associated with neurobehavioral reward system dysfunctions that pose debilitating impairments in adaptive decision-making. A candidate mechanism for such anomalies in ADHD may be a compromise in the control of motivated behaviors. Thus, demonstrating and restoring potential motivational control irregularities may serve significant clinical benefit. The motivational control of action guides goal-directed behaviors that are driven by outcome value, and habits that are inflexibly cue-triggered. We examined whether ADHD symptomology within the general population is linked to habitual control, and whether a motivation-based manipulation can break well-learned habits. We obtained symptom severity scores from 106 participants and administered a Go/NoGo task that capitalizes on familiar, well-learned associations (green-Go and red-NoGo) to demonstrate outcome-insensitivity when compared to newly learned Go/NoGo associations. We tested for outcome-insensitive habits by changing the Go and NoGo contingencies, such that Go signals became NoGo signals and vice versa. We found that generally, participants responded less accurately when green and red stimuli were mapped to color-response contingencies that were incongruent with daily experiences, whereas novel Go/NoGo stimuli evoked similar accuracy regardless of color-response mappings. Thus, our Go/NoGo task successfully elicited outcome-insensitive habits (i.e., persistent responses to familiar stimuli without regard for consequences); however, this effect was independent of ADHD symptomology. Nevertheless, we found an association between hyperactivity and congruent Go response latency, suggesting heightened pre-potency to perform habitual Go actions as hyperactivity increases. To examine habit disruption, participants returned to the lab and underwent the familiar version of the Go/NoGo task, but were given mid-experiment performance tracking information and a monetary incentive prior to contingency change. We found that this motivational boost via dual feedback prevented the incongruency-related accuracy impairment, effectively breaking the habit, albeit independent of ADHD symptomology. Our findings present only a modest link between ADHD symptomology and motivational control, which may be due to compensatory mechanisms in ADHD driving goal-directed control, or our task's potential insensitivity to individual differences in ADHD symptomology. Further investigations may be crucial for determining whether ADHD is related to motivational impairments.

Intelligence mindset shapes neural learning signals and memory.

Intelligence mindset, which denotes individual beliefs about whether intelligence is fixed versus malleable, shapes academic success, but the neural mechanisms underlying mindset-related differences in learning are unknown. Here, we probe the effects of individual differences in mindset on neural responses to negative feedback after a competence threat manipulation. We hypothesized that when their competence was threatened, participants with fixed mindsets would interpret further negative feedback as punishing. After receiving either no score or a competence-threatening IQ score, participants performed a learning task with feedback that emphasized either the evaluative or informational weight of negative feedback. Participants who experienced the competence threat had the strongest predictive relationships between mindset, performance, and caudate activation. The competence threat may have compounded the subjective punishment of negative feedback for fixed mindsets relative to growth mindsets, causing poorer learning from negative feedback in the evaluative context and inflexible striatal responses to negative feedback across feedback contexts.

Reward circuitry activation reflects social preferences in the face of cognitive effort.

Research at the intersection of social neuroscience and cognitive effort is an interesting new area for exploration. There is great potential to broaden our understanding of how social context and cognitive effort processes, currently addressed in disparate literatures, interact with one another. In this paper, we briefly review the literature on cognitive effort, focusing on effort-linked valuation and the gap in the literature regarding cognitive effort in the social domain. Next, we present a study designed to explore valuation processes linked to cognitive effort within the social context of an inequality manipulation. More specifically, we created monetary inequality among the participant (SELF, endowed with $50) and two confederates: one also endowed with $50 (OTHER HIGH) and another with only $5 (OTHER LOW). We then scanned participants using fMRI as they attempted to earn bonus payments for themselves and others through a cognitively effortful feedback-based learning task. Positive feedback produced significantly greater activation than negative feedback in key valuation regions, the ventral striatum (VS) and ventromedial prefrontal cortex (vmPFC), both when participants were performing the task on their own behalf and when earning rewards for others. While reward-related activity in the VS was exaggerated for SELF compared to OTHER HIGH for both positive and negative feedback, activity in the vmPFC did not distinguish between recipients in the group-level results. Furthermore, participants naturally fell into two groups: those most engaged when playing for themselves and those who reported engagement for others. While Self-Engaged participants showed differences between the SELF and both OTHER conditions in the VS and vmPFC, Other-Engaged participants only showed an attenuated response to negative feedback for OTHER HIGH compared to SELF in the VS and no differences between recipient conditions in the vmPFC. Together, this work shows the importance of individual differences and the fragility of advantageous inequality aversion in the face of cognitive effort, highlighting the need to study cognitive effort in the social domain.

Writing About Past Failures Attenuates Cortisol Responses and Sustained Attention Deficits Following Psychosocial Stress.

Acute stress can harm performance. Paradoxically, writing about stressful events-such as past failures-has been shown to improve cognitive functioning and performance, especially in tasks that require sustained attention. Yet, there is little physiological evidence for whether writing about past failures or other negative events improves performance by reducing stress. In this experiment, we studied the effects of an acute psychosocial stressor, the Trier Social Stress Test, on attentional performance and salivary cortisol release in humans. Additionally, we investigated whether an expressive writing task could reduce the detrimental effects of stress, both on performance and physiological response. We found that when individuals were asked to write about a past failure before experiencing a stressor, they exhibited attenuated stress responses. Moreover, those who wrote about a past failure before being exposed to stress also exhibited better behavioral performance. Our results suggest that writing about a previous failure may allow an individual to experience a new stressor as less stressful, reducing its physiological and behavioral effects.

Control and Effort Costs Influence the Motivational Consequences of Choice.

The act of making a choice, apart from any outcomes the choice may yield, has, paradoxically, been linked to both the enhancement and the detriment of intrinsic motivation. Research has implicated two factors in potentially mediating these contradictory effects: the personal control conferred by a choice and the costs associated with a choice. Across four experiments, utilizing a physical effort task disguised as a simple video game, we systematically varied costs across two levels of physical effort requirements (Low-Requirement, High-Requirement) and control over effort costs across three levels of choice (Free-Choice, Restricted-Choice, and No-Choice) to disambiguate how these factors affect the motivational consequences of choosing within an effortful task. Together, our results indicated that, in the face of effort requirements, illusory control alone may not sufficiently enhance perceptions of personal control to boost intrinsic motivation; rather, the experience of actual control may be necessary to overcome effort costs and elevate performance. Additionally, we demonstrated that conditions of illusory control, while otherwise unmotivating, can through association with the experience of free-choice, be transformed to have a positive effect on motivation.

Modulation of ventral striatal activity by cognitive effort.

Effort discounting theory suggests that the value of a reward should be lower if it was effortful to obtain, whereas contrast theory suggests that the contrast between the costly effort and the reward makes the reward seem more valuable. To test these alternative hypotheses, we used functional magnetic resonance imaging (fMRI) as participants engaged in feedback-based learning that required low or high cognitive effort to obtain positive feedback, while the objective amount of information provided by feedback remained constant. In the low effort condition, a single image was presented with four response options. In the high effort condition, two images were presented, each with two response options, and correct feedback was presented only when participants responded correctly to both of the images. Accuracy was significantly lower for the high effort condition, and all participants reported that the high effort condition was more difficult. A region of the ventral striatum selected for sensitivity to feedback value also showed increased activation to feedback presentation associated with the high effort condition relative to the low effort condition, when controlling for activation from corresponding control conditions where feedback was random. These results suggest that increased cognitive effort produces corresponding increases in positive feedback-related ventral striatum activity, in line with the predictions made by contrast theory. The accomplishment of obtaining a hard-earned intrinsic reward, such as positive feedback, may be particularly likely to promote reward-related brain activity.

Increases in brain activity during social competition predict decreases in working memory performance and later recall.

In our fMRI experiment, participants completed a learning task in both a noncompetitive and a socially competitive learning environment. Despite reporting a preference for completing the task while competing, participants remembered significantly more during the task and later recalled more from the noncompetitive learning environment. Furthermore, during working memory maintenance, there was performance-related deactivation in the medial prefrontal cortex (mPFC) and the precuneus/PCC. During feedback presentation, there was greater activation in the mPFC and the precuneus/PCC while competing. Differential activation in the precuneus/PCC predicted worse later recall for information learned competitively. Since previous research suggests that the mPFC is involved in social-referencing, while the precuneus/PCC is implicated in off-task thoughts, our results suggest that receiving feedback regarding competition produces more activation in brain regions implicated in social interaction, as well as task distraction. While competition may make a task more enjoyable, the goal of winning may distract from maximizing performance. Hum Brain Mapp 38:457-471, 2017. © 2016 Wiley Periodicals, Inc.

Are You Smarter Than a Teenager? Maybe Not When It Comes to Reinforcement Learning.

Adolescence is a time of tumultuous behavior that may result, in part, from brain circuitry that enhances reward seeking. In this issue of Neuron, Davidow et al. (2016) present a convincing argument that adolescent brain functionality can be adaptive in certain contexts, particularly probabilistic learning environments.

The Value of Being Wrong: Intermittent Feedback Delivery Alters the Striatal Response to Negative Feedback.

Whereas positive feedback is both rewarding and informative, negative feedback can be construed as either punishing (because it is indicative of poor performance) or informative (because it may lead to goal attainment). In this neuroimaging experiment, we highlighted the informational value of negative feedback by intermixing trials with and without feedback. When performance feedback is expected, positive feedback triggers an increase in striatal activity, whereas negative feedback elicits a decrease in striatal activity. We predicted that, in contrast, when feedback receipt is unpredictable, the striatal response to negative feedback would increase. Participants performed a paired-associate learning task during fMRI scanning. In one condition ("blocked feedback"), the receipt of feedback was predictable--participants knew whether or not they would receive feedback for their responses. In another condition ("mixed feedback"), the receipt of feedback was unpredictable--on a random 50% of trials, participants received feedback, and they otherwise received no feedback. Negative feedback in the mixed feedback condition elicited more striatal activity than negative feedback in the blocked feedback condition. In contrast, feedback omission evoked more striatal activity when feedback delivery was expected, compared to when it was unpredictable. This pattern emerged from an increase in caudate activity in response to negative feedback in the mixed feedback condition and a decrease in ventral striatal activity in response to no feedback in this condition. These results suggest that, by emphasizing the informational value of negative feedback, an unpredictable feedback context alters the striatal response to negative feedback and to the omission of feedback.

The power of competition: Effects of social motivation on attention, sustained physical effort, and learning.

Competition has often been implicated as a means to improve effort-based learning and attention. Two experiments examined the effects of competition on effort and memory. In Experiment 1, participants completed a physical effort task in which they were rewarded for winning an overall percentage, or for winning a competition they believed was against another player. In Experiment 2, participants completed a memory task in which they were rewarded for remembering an overall percentage of shapes, or more shapes than a "competitor." We found that, in the physical effort task, participants demonstrated faster reaction times (RTs)-a previous indicator of increased attention-in the competitive environment. Moreover, individual differences predicted the salience of competition's effect. Furthermore, male participants showed faster RTs and greater sustained effort as a result of a competitive environment, suggesting that males may be more affected by competition in physical effort tasks. However, in Experiment 2, participants remembered fewer shapes when competing, and later recalled less of these shapes during a post-test, suggesting that competition was harmful in our memory task. The different results from these two experiments suggest that competition can improve attention in a physical effort task, yet caution the use of competition in memory tasks.

Effects of intrinsic motivation on feedback processing during learning.

Learning commonly requires feedback about the consequences of one's actions, which can drive learners to modify their behavior. Motivation may determine how sensitive an individual might be to such feedback, particularly in educational contexts where some students value academic achievement more than others. Thus, motivation for a task might influence the value placed on performance feedback and how effectively it is used to improve learning. To investigate the interplay between intrinsic motivation and feedback processing, we used functional magnetic resonance imaging (fMRI) during feedback-based learning before and after a novel manipulation based on motivational interviewing, a technique for enhancing treatment motivation in mental health settings. Because of its role in the reinforcement learning system, the striatum is situated to play a significant role in the modulation of learning based on motivation. Consistent with this idea, motivation levels during the task were associated with sensitivity to positive versus negative feedback in the striatum. Additionally, heightened motivation following a brief motivational interview was associated with increases in feedback sensitivity in the left medial temporal lobe. Our results suggest that motivation modulates neural responses to performance-related feedback, and furthermore that changes in motivation facilitate processing in areas that support learning and memory.

Value and probability coding in a feedback-based learning task utilizing food rewards.

For the consequences of our actions to guide behavior, the brain must represent different types of outcome-related information. For example, an outcome can be construed as negative because an expected reward was not delivered or because an outcome of low value was delivered. Thus behavioral consequences can differ in terms of the information they provide about outcome probability and value. We investigated the role of the striatum in processing probability-based and value-based negative feedback by training participants to associate cues with food rewards and then employing a selective satiety procedure to devalue one food outcome. Using functional magnetic resonance imaging, we examined brain activity related to receipt of expected rewards, receipt of devalued outcomes, omission of expected rewards, omission of devalued outcomes, and expected omissions of an outcome. Nucleus accumbens activation was greater for rewarding outcomes than devalued outcomes, but activity in this region did not correlate with the probability of reward receipt. Activation of the right caudate and putamen, however, was largest in response to rewarding outcomes relative to expected omissions of reward. The dorsal striatum (caudate and putamen) at the time of feedback also showed a parametric increase correlating with the trialwise probability of reward receipt. Our results suggest that the ventral striatum is sensitive to the motivational relevance, or subjective value, of the outcome, while the dorsal striatum codes for a more complex signal that incorporates reward probability. Value and probability information may be integrated in the dorsal striatum, to facilitate action planning and allocation of effort.