Additive Effects of Monetary Loss and Positive Emotion in the Human Brain.

In many real-life scenarios, our decisions could lead to multiple outcomes that conflict with value. Hence, an appropriate neural representation of the net experienced value of conflicting outcomes, which play a crucial role in guiding future decisions, is critical for adaptive behavior. As some recent functional neuroimaging work has primarily focused on the concurrent processing of monetary gains and aversive information, very little is known regarding the integration of conflicting value signals involving monetary losses and appetitive information in the human brain. To address this critical gap, we conducted a functional MRI study involving healthy human male participants to examine the nature of integrating positive emotion and monetary losses. We employed a novel experimental design where the valence (positive or neutral) of an emotional stimulus indicated the type of outcome (loss or no loss) in a choice task. Specifically, we probed two plausible integration patterns while processing conflicting value signals involving positive emotion and monetary losses: interactive versus additive. We found overlapping main effects of positive (vs neutral) emotion and loss (vs no loss) in multiple brain regions, including the ventromedial prefrontal cortex, striatum, and amygdala, notably with a lack of evidence for interaction. Thus, our findings revealed the additive integration pattern of monetary loss and positive emotion outcomes, suggesting that the experienced value of the monetary loss was not modulated by the valence of the image signaling those outcomes. These findings contribute to our limited understanding of the nature of integrating conflicting outcomes in the healthy human brain with potential clinical relevance.

Negative emotion reduces the discriminability of reward outcomes in the ventromedial prefrontal cortex.

Reward and emotion are tightly intertwined, so there is a growing interest in mapping their interactions. However, our knowledge of these interactions in the human brain, especially during the consummatory phase of reward is limited. To address this critical gap, we conducted a functional magnetic resonance imaging study to investigate the effects of negative emotion on reward outcome processing. We employed a novel design where emotional valence (negative or neutral) indicated the type of outcome (reward or no-reward) in a choice task. We focused our functional magnetic resonance imaging analysis on the ventro-medial prefrontal cortex (vmPFC), ventral striatum and amygdala, which were frequently implicated in reward outcome processing. In these regions of interest, we performed multi-voxel pattern analysis to specifically probe how negative emotion modulates reward outcome processing. In vmPFC, using decoding analysis, we found evidence consistent with the reduced discriminability of multi-variate activity patterns of reward vs no-reward outcomes when signaled by a negative relative to a neutral image, suggesting an emotional modulation of reward processing along the plausible common value/valence dimension. These findings advance our limited understanding of the basic brain mechanisms underlying the influence of negative emotion on consummatory reward processing, with potential implications for mental disorders, particularly anxiety and depression.

Arousal-driven interactions between reward motivation and categorization of emotional facial expressions.

Reward motivation and emotion share common dimensions of valence and arousal, but the nature of interactions between the two constructs is relatively unclear. On the one hand, based on the common valence dimension, valence-compatible interactions are expected where reward motivation would facilitate the processing of compatible (i.e., positive) emotion and hamper the processing of incompatible (i.e., negative) emotion. On the other hand, one could hypothesize valence-general interactions driven by the arousal dimension, where the processing of both positive and negative emotions would be facilitated under reward motivation. Currently, the evidence for valence-compatible vs. valence-general type interactions between reward motivation and goal-relevant emotion is relatively mixed. Moreover, as most of the previous work focused primarily on appetitive motivation, the influence of aversive motivation on goal-relevant emotion is largely unexplored. To address these important gaps, in the present study, we investigated the interactions between motivation and categorization of facial emotional expressions by manipulating the valence dimension of motivation (appetitive and aversive motivation levels) together with that of emotion (positive and negative valence stimuli). Specifically, we conducted two behavioral experiments to separately probe the influence of appetitive and aversive motivation (manipulated via an advance cue signaling the prospect of monetary gains in Experiment 1 and losses in Experiment 2, respectively) on the categorization of happy, fearful, and neutral faces. We tested the two competing hypotheses regarding the interactions between appetitive/aversive motivation and emotional face categorization: Valence-compatible vs. Valence-general. We found evidence consistent with valence-general interactions where both appetitive and aversive motivation facilitated the categorization of happy and fearful faces relative to the neutral ones. Our findings demonstrate that interactions between reward motivation and categorization of emotional faces are driven by the arousal dimension, not by valence.

Controllability over stressor decreases responses in key threat-related brain areas.

Controllability over stressors has major impacts on brain and behavior. In humans, however, the effect of controllability on responses to stressors is poorly understood. Using functional magnetic resonance imaging (fMRI), we investigated how controllability altered responses to a shock-plus-sound stressor with a between-group yoked design, where participants in controllable and uncontrollable groups experienced matched stressor exposure. Employing Bayesian multilevel analysis at the level of regions of interest and voxels in the insula, and standard voxelwise analysis, we found that controllability decreased stressor-related responses across threat-related regions, notably in the bed nucleus of the stria terminalis and anterior insula. Posterior cingulate cortex, posterior insula, and possibly medial frontal gyrus showed increased responses during control over stressor. Our findings support the idea that the aversiveness of stressors is reduced when controllable, leading to decreased responses across key regions involved in anxiety-related processing, even at the level of the extended amygdala.

To pool or not to pool: Can we ignore cross-trial variability in FMRI?

In this work, we investigate the importance of explicitly accounting for cross-trial variability in neuroimaging data analysis. To attempt to obtain reliable estimates in a task-based experiment, each condition is usually repeated across many trials. The investigator may be interested in (a) condition-level effects, (b) trial-level effects, or (c) the association of trial-level effects with the corresponding behavior data. The typical strategy for condition-level modeling is to create one regressor per condition at the subject level with the underlying assumption that responses do not change across trials. In this methodology of complete pooling, all cross-trial variability is ignored and dismissed as random noise that is swept under the rug of model residuals. Unfortunately, this framework invalidates the generalizability from the confine of specific trials (e.g., particular faces) to the associated stimulus category ("face"), and may inflate the statistical evidence when the trial sample size is not large enough. Here we propose an adaptive and computationally tractable framework that meshes well with the current two-level pipeline and explicitly accounts for trial-by-trial variability. The trial-level effects are first estimated per subject through no pooling. To allow generalizing beyond the particular stimulus set employed, the cross-trial variability is modeled at the population level through partial pooling in a multilevel model, which permits accurate effect estimation and characterization. Alternatively, trial-level estimates can be used to investigate, for example, brain-behavior associations or correlations between brain regions. Furthermore, our approach allows appropriate accounting for serial correlation, handling outliers, adapting to data skew, and capturing nonlinear brain-behavior relationships. By applying a Bayesian multilevel model framework at the level of regions of interest to an experimental dataset, we show how multiple testing can be addressed and full results reported without arbitrary dichotomization. Our approach revealed important differences compared to the conventional method at the condition level, including how the latter can distort effect magnitude and precision. Notably, in some cases our approach led to increased statistical sensitivity. In summary, our proposed framework provides an effective strategy to capture trial-by-trial responses that should be of interest to a wide community of experimentalists.

Interactions between emotion and action in the brain.

A growing literature supports the existence of interactions between emotion and action in the brain, and the central participation of the anterior midcingulate cortex (aMCC) in this regard. In the present functional magnetic resonance imaging study, we sought to investigate the role of self-relevance during such interactions by varying the context in which threating pictures were presented (with guns pointed towards or away from the observer). Participants performed a simple visual detection task following exposure to such stimuli. Except for voxelwise tests, we adopted a Bayesian analysis framework which evaluated evidence for the hypotheses of interest, given the data, in a continuous fashion. Behaviorally, our results demonstrated a valence by context interaction such that there was a tendency of speeding up responses to targets after viewing threat pictures directed towards the participant. In the brain, interaction patterns that paralleled those observed behaviorally were observed most notably in the middle temporal gyrus, supplementary motor area, precentral gyrus, and anterior insula. In these regions, activity was overall greater during threat conditions relative to neutral ones, and this effect was enhanced in the directed towards context. A valence by context interaction was observed in the aMCC too, where we also observed a correlation (across participants) of evoked responses and reaction time data. Taken together, our study revealed the context-sensitive engagement of motor-related areas during emotional perception, thus supporting the idea that emotion and action interact in important ways in the brain.

Interactions between reward motivation and emotional processing.

Much of the past research on how reward motivation and emotional information influence brain and behavior has been conducted separately. Recently, a few behavioral and brain imaging studies have investigated how reward and emotional information co-jointly impact brain and behavior. The present chapter reviews findings from this recent line of work to summarize our current knowledge about the influence of reward expectancy on brain and behavior in the context of emotional information. The available findings suggest that behaviorally reward counteracts the adverse impact of potent emotional distractors on task performance. Additionally, brain findings suggest that the ventral striatum plays an active role in upregulating attentional control processes to limit the influence of emotional distractors. Overall, task relevance seems to play an important role in shaping interactions between reward and emotional processing. We conclude by outlining a few open questions for future research.

Dynamic Threat Processing.

During real-life situations, multiple factors interact dynamically to determine threat level. In the current fMRI study involving healthy adult human volunteers, we investigated interactions between proximity, direction (approach vs. retreat), and speed during a dynamic threat-of-shock paradigm. As a measure of threat-evoked physiological arousal, skin conductance responses were recorded during fMRI scanning. Some brain regions tracked individual threat-related factors, and others were also sensitive to combinations of these variables. In particular, signals in the anterior insula tracked the interaction between proximity and direction where approach versus retreat responses were stronger when threat was closer compared with farther. A parallel proximity-by-direction interaction was also observed in physiological skin conductance responses. In the right amygdala, we observed a proximity by direction interaction, but intriguingly in the opposite direction as the anterior insula; retreat versus approach responses were stronger when threat was closer compared with farther. In the right bed nucleus of the stria terminalis, we observed an effect of threat proximity, whereas in the right periaqueductal gray/midbrain we observed an effect of threat direction and a proximity by direction by speed interaction (the latter was detected in exploratory analyses but not in a voxelwise fashion). Together, our study refines our understanding of the brain mechanisms involved during aversive anticipation in the human brain. Importantly, it emphasizes that threat processing should be understood in a manner that is both context-sensitive and dynamic.

Attentional capture by simultaneous pleasant and unpleasant emotional distractors.

Both high-arousal pleasant and unpleasant task-irrelevant stimuli capture attention and divert processing away from the main task leading to impaired behavioral performance in concurrent tasks. Most studies have separately investigated interference effects of unpleasant and pleasant stimuli on behavior. Thus, little is known about how pleasant and unpleasant task-irrelevant stimuli influence behavior simultaneously. In the present study, we investigated this question during a visual-letter search task. We tested two alternative hypotheses about the influence of simultaneous pleasant and unpleasant task-irrelevant stimuli on task performance. If behavior is purely determined by the intensity of the distractor stimuli (independent of valence), then we would expect the interference effect of simultaneous pleasant and unpleasant distractors to be similar to the influence of two pleasant or two unpleasant distractor stimuli. In contrast, because of opponent interactions between appetitive and aversive motivational systems, the interference effect of simultaneous pleasant and unpleasant stimuli might be weakened. We found that the interference effect of a compound pleasant-plus-unpleasant stimulus was greater than that of a neutral-plus-emotional stimulus and similar to that of two pleasant or two unpleasant stimuli. These results suggest that at the level of behavior, the influence of joint pleasant and unpleasant task-irrelevant stimuli during perception is mainly determined by the intensity of the stimuli, and independent of their valence. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Altered segregation between task-positive and task-negative regions in mild traumatic brain injury.

Changes in large-scale brain networks that accompany mild traumatic brain injury (mTBI) were investigated using functional magnetic resonance imaging (fMRI) during the N-back working memory task at two cognitive loads (1-back and 2-back). Thirty mTBI patients were examined during the chronic stage of injury and compared to 28 control participants. Demographics and behavioral performance were matched across groups. Due to the diffuse nature of injury, we hypothesized that there would be an imbalance in the communication between task-positive and Default Mode Network (DMN) regions in the context of effortful task execution. Specifically, a graph-theoretic measure of modularity was used to quantify the extent to which groups of brain regions tended to segregate into task-positive and DMN sub-networks. Relative to controls, mTBI patients showed reduced segregation between the DMN and task-positive networks, but increased functional connectivity within the DMN regions during the more cognitively demanding 2-back task. Together, our findings reveal that patients exhibit alterations in the communication between and within neural networks during a cognitively demanding task. These findings reveal altered processes that persist through the chronic stage of injury, highlighting the need for longitudinal research to map the neural recovery of mTBI patients.

Potential reward reduces the adverse impact of negative distractor stimuli.

Knowledge about interactions between reward and negative processing is rudimentary. Here, we employed functional MRI to probe how potential reward signaled by advance cues alters aversive distractor processing during perception. Behaviorally, the influence of aversive stimuli on task performance was reduced during the reward compared to no-reward condition. In the brain, at the task phase, paralleling the observed behavioral pattern, we observed significant interactions in the anterior insula and dorsal anterior cingulate cortex, such that responses during the negative (vs neutral) condition were reduced during the reward compared to no-reward condition. Notably, negative distractor processing in the amygdala appeared to be independent of the reward manipulation. During the initial cue phase, we observed increased reward-related responses in the ventral striatum/accumbens, which were correlated with behavioral interference scores at the subsequent task phase, revealing that participants with increased reward-related responses exhibited a greater behavioral benefit of reward in reducing the adverse effect of negative images. Furthermore, during processing of reward (vs no-reward) cues, the ventral striatum exhibited stronger functional connectivity with fronto-parietal regions important for attentional control. Together, our findings contribute to the understanding of how potential reward influences attentional control and reduces negative distractor processing in the human brain.

An fMRI Pilot Study of Cognitive Reappraisal in Children: Divergent Effects on Brain and Behavior.

Although neuroimaging studies in adults demonstrate that cognitive reappraisal effectively down-regulates negative affect and results in increased prefrontal and decreased amygdala activity, very limited empirical data exist on the neural basis of cognitive reappraisal in children. This study aimed to pilot test a developmentally-appropriate guided cognitive reappraisal task in order to examine the effects of cognitive reappraisal on children's self-reports of affect and brain responses. Study 1 (N =19, 4-10 years-old) found that children successfully employed guided cognitive reappraisal to decrease subjective ratings of negative affect, supporting the effectiveness of the guided cognitive reappraisal task. Study 2 (N =15, ages 6-10 years-old) investigated the neural responses to guided cognitive reappraisal and found that the neural responses showed increased activation in the amygdala and ventromedial prefrontal cortex during the cognitive reappraisal condition compared to the no regulation condition. In addition, amygdala activity was positively correlated with ventromedial prefrontal cortex activation during cognitive reappraisal. Findings suggest that the neural networks supporting cognitive reappraisal in children involve similar brain regions but brain responses deviate from findings in adults. Our findings suggest that the neural networks supporting emotion regulation are still developing during middle childhood, and future research is necessary to delineate age-related development of the neural network involved in cognitive reappraisal.

Reward learning and negative emotion during rapid attentional competition.

Learned stimulus-reward associations influence how attention is allocated, such that stimuli rewarded in the past are favored in situations involving limited resources and competition. At the same time, task-irrelevant, high-arousal negative stimuli capture attention and divert resources away from tasks resulting in poor behavioral performance. Yet, investigations of how reward learning and negative stimuli affect perceptual and attentional processing have been conducted in a largely independent fashion. We have recently reported that performance-based monetary rewards reduce negative stimuli interference during perception. The goal of the present study was to investigate how stimuli associated with past monetary rewards compete with negative stimuli during a subsequent attentional task when, critically, no performance-based rewards were at stake. Across two experiments, we found that target stimuli that were associated with high reward reduced the interference effect of potent, negative distractors. Similar to our recent findings with performance-based rewards, our results demonstrate that reward-associated stimuli reduce the deleterious impact of negative stimuli on behavior.

Counteracting effect of threat on reward enhancements during working memory.

Cognitive performance has been shown to be enhanced when performance-based rewards are at stake. On the other hand, task-irrelevant threat processing has been shown to have detrimental effects during several cognitive tasks. Crucially, the impact of reward and threat on cognition has been studied largely independently of one another. Hence, our understanding of how reward and threat simultaneously contribute to performance is incomplete. To fill in this gap, the present study investigated how reward and threat interact with one another during a cognitive task. We found that threat of shock counteracted the beneficial effect of reward during a working memory task. Furthermore, individual differences in self-reported reward-sensitivity and anxiety were linked to the extent to which reward and threat interacted during behaviour. Together, the current findings contribute to a limited but growing literature unravelling how positive and negative information processing jointly influence cognition.

Network organization unfolds over time during periods of anxious anticipation.

Entering a state of anxious anticipation triggers widespread changes across large-scale networks in the brain. The temporal aspects of this transition into an anxious state are poorly understood. To address this question, an instructed threat of shock paradigm was used while recording functional MRI in humans to measure how activation and functional connectivity change over time across the salience, executive, and task-negative networks and how they interact with key regions implicated in emotional processing; the amygdala and bed nucleus of the stria terminalis (BNST). Transitions into threat blocks were associated with transient responses in regions of the salience network and sustained responses in a putative BNST site, among others. Multivariate network measures of communication were computed, revealing changes to network organization during transient and sustained periods of threat, too. For example, the salience network exhibited a transient increase in network efficiency followed by a period of sustained decreased efficiency. The amygdala became more central to network function (as assessed via betweenness centrality) during threat across all participants, and the extent to which the BNST became more central during threat depended on self-reported anxiety. Together, our study unraveled a progression of responses and network-level changes due to sustained threat. In particular, our results reveal how network organization unfolds with time during periods of anxious anticipation.

Motivation versus aversive processing during perception.

Reward facilitates performance and boosts cognitive performance across many tasks. At the same time, negative affective stimuli interfere with performance when they are not relevant to the task at hand. Yet, the investigation of how reward and negative stimuli impact perception and cognition has taken place in a manner that is largely independent of each other. How reward and negative emotion simultaneously contribute to behavioral performance is currently poorly understood. The aim of the present study was to investigate how the simultaneous manipulation of positive motivational processing (here manipulated via reward) and aversive processing (here manipulated via negative picture viewing) influence behavior during a perceptual task. We tested 2 competing hypotheses about the impact of reward on negative picture viewing. On the one hand, suggestions about the automaticity of emotional processing predict that negative picture interference would be relatively immune to reward. On the other, if affective visual processing is not obligatory, as we have argued in the past, reward may counteract the deleterious effect of more potent negative pictures. We found that reward counteracted the effect of potent, negative distracters during a visual discrimination task. Thus, when sufficiently motivated, participants were able to reduce the deleterious impact of bodily mutilation stimuli.

Impact of appetitive and aversive outcomes on brain responses: linking the animal and human literatures.

Decision-making is motivated by the possibility of obtaining reward and/or avoiding punishment. Though many have investigated behavior associated with appetitive or aversive outcomes, few have examined behaviors that rely on both. Fewer still have addressed questions related to how anticipated appetitive and aversive outcomes interact to alter neural signals related to expected value, motivation, and salience. Here we review recent rodent, monkey, and human research that address these issues. Further development of this area will be fundamental to understanding the etiology behind human psychiatric diseases and cultivating more effective treatments.

Pervasive competition between threat and reward in the brain.

In the current functional MRI study, we investigated interactions between reward and threat processing. Visual cues at the start of each trial informed participants about the chance of winning monetary reward and/or receiving a mild aversive shock. We tested two competing hypothesis: according to the 'salience hypothesis', in the condition involving both reward and threat, enhanced activation would be observed because of increased salience; according to the 'competition hypothesis', the processing of reward and threat would trade-off against each other, leading to reduced activation. Analysis of skin conductance data during a delay phase revealed an interaction between reward and threat processing, such that the effect of reward was reduced during threat and the effect of threat was reduced during reward. Analysis of imaging data during the same task phase revealed interactions between reward and threat processing in several regions, including the midbrain/ventral tegmental area, caudate, putamen, bed nucleus of the stria terminalis, anterior insula, middle frontal gyrus and dorsal anterior cingulate cortex. Taken together, our findings reveal conditions during which reward and threat trade-off against each other across multiple sites. Such interactions are suggestive of competitive processes and may reflect the organization of opponent systems in the brain.

Interactions between reward and threat during visual processing.

Appetitive stimuli such as monetary incentives often improve performance whereas aversive stimuli such as task-irrelevant negative stimuli frequently impair performance. But our understanding of how appetitive and aversive processes simultaneously contribute to brain and behavior is rudimentary. In the current fMRI study, we investigated interactions between reward and threat by investigating the effects of monetary reward on the processing of task-irrelevant threat stimuli during a visual discrimination task. Reward was manipulated by linking fast and accurate responses to foreground stimuli with monetary reward; threat was manipulated by pairing the background context with mild aversive shock. The behavioral results in terms of both accuracy and reaction time revealed that monetary reward eliminated the influence of threat-related stimuli. Paralleling the behavioral results, during trials involving both reward and threat, the imaging data revealed increased engagement of the ventral caudate and anterior mid-cingulate cortex, which were accompanied by increased task-relevant processing in the visual cortex. Overall, our study illustrates how the simultaneous processing of appetitive and aversive information shapes both behavior and brain responses.

Network analysis reveals increased integration during emotional and motivational processing.

In recent years, a large number of human studies have investigated large-scale network properties of the brain, typically during the resting state. A critical gap in the knowledge base concerns the understanding of network properties of a focused set of brain regions during task conditions engaging these regions. Although emotion and motivation recruit many brain regions, it is currently unknown how they affect network-level properties of inter-region interactions. In the present study, we sought to characterize network structure during "mini-states" engendered by emotional and motivational cues investigated in separate studies. To do so, we used graph-theoretic network analysis to probe network-, community-, and node-level properties of the trial-by-trial functional connectivity between regions of interest. We used methods that operate on weighted graphs that make use of the continuous information of connectivity strength. In both the emotion and motivation datasets, global efficiency increased and decomposability decreased. Thus, processing became less segregated with the context signaled by the cue (potential shock or potential reward). Our findings also revealed several important features of inter-community communication, including notable contributions of the bed nucleus of the stria terminalis, anterior insula, and thalamus during threat and of the caudate and nucleus accumbens during reward. Together, the results suggest that one way in which emotional and motivational processing affect brain responses is by enhancing signal communication between regions, especially between cortical and subcortical ones.