Anterior cingulate is a source of valence-specific information about value and uncertainty.
ABSTRACT: Anterior cingulate cortex (ACC) is thought to control a wide range of reward, punishment, and uncertainty-related behaviors. However, how it does so is unclear. Here, in a Pavlovian procedure in which monkeys displayed a diverse repertoire of reward-related, punishment-related, and uncertainty-related behaviors, we show that many ACC-neurons represent expected value and uncertainty in a valence-specific manner, signaling value or uncertainty predictions about either rewards or punishments. Other ACC-neurons signal prediction information about rewards and punishments by displaying excitation to both (rather than excitation to one and inhibition to the other). This diversity in valence representations may support the role of ACC in many behavioral states that are either enhanced by reward and punishment (e.g., vigilance) or specific to either reward or punishment (e.g., approach and avoidance). Also, this first demonstration of punishment-uncertainty signals in the brain suggests that ACC could be a target for the treatment of uncertainty-related disorders of mood.Rewards or punishments elicit diverse behavioral responses; however, the neural circuits underlying such flexibility are unclear. Here Monosov shows that this diversity could be supported by neurons in the anterior cingulate that represent expected value and uncertainty in a valence-specific manner.
Project description:Incentives are primary determinants of if and how well an organism will perform a given behavior. Here, we examined how incentive valence and magnitude influence task switching, a critical cognitive control process, and test the predictions that the anterior cingulate cortex (ACC) and the ventral striatum (vStr) function as key nodes linking motivation and control systems in the brain. Our results indicate that reward and punishment incentives have both common and distinct effects on cognitive control at the behavioral and neurobiological levels. For example, reward incentives led to greater activity in the ACC during the engagement of control relative to punishments. Furthermore, the neural responses to reward and punishment differed as a function of individual sensitivity to each incentive valence. Functional connectivity analyses suggest a role for vStr in signaling motivational value during cognitive control and as a potential link between motivation and control networks. Overall, our findings suggest that similar changes in observed behavior (e.g. response accuracy) under reward and punishment incentives are mediated by, at least partially, distinct neurobiological substrates.
Project description:Several studies have suggested that females and males differ in reward behaviors and their underlying neural circuitry. Whether human sex differences extend across neural and behavioral levels for both rewards and punishments remains unclear. We studied a community sample of 221 young women and men who performed a monetary incentive task known to engage the mesoaccumbal pathway and salience network. Both stimulus salience (behavioral relevance) and valence (win vs loss) varied during the task. In response to high- vs low-salience stimuli presented during the monetary incentive task, men showed greater subjective arousal ratings, behavioral accuracy and skin conductance responses (P <?0.006, Hedges' effect size g =?0.38 to 0.46). In a subsample studied with functional magnetic resonance imaging (n =?44), men exhibited greater responsiveness to stimulus salience in the nucleus accumbens, midbrain, anterior insula and dorsal anterior cingulate cortex (P <?0.02, g =?0.86 to 1.7). Behavioral, autonomic and neural sensitivity to the valence of stimuli did not differ by sex, indicating that responses to rewards vs punishments were similar in women and men. These results reveal novel and robust sex differences in reward- and punishment-related traits, behavior, autonomic activity and neural responses. These convergent results suggest a neurobehavioral basis for sexual dimorphism observed in the reward system, including reward-related disorders.
Project description:Reduced relative length of the 2nd to 4th digits (2D:4D) is thought to partially reflect fetal testosterone (FT) exposure, a process suspected to promote relatively permanent effects on the brain and behavior via structural and functional neuroadaptations. We examined the effect of 2D:4D on neural response - assessed by P2a and feedback-related negativity (FRN) event-related potentials (ERPs) - to motivational stimuli (reward or punishment) using two counterbalanced conditions of a passive S1/S2 outcome prediction design. P2a to expected and unexpected delivered rewards or punishments ($1 or white noise burst, respectively) and FRN to withheld rewards or punishments ($0 or silence, respectively) were observed in undergraduates. Lower left 2D:4D and greater 2D:4DR-L predicted amplified P2a to the delivery (but not FRN to the omission) of motivationally salient stimuli, regardless of valence and probability. These preliminary findings suggest that FT may organize dopamine neurons to respond more strongly to the delivery of motivational stimuli.
Project description:An action may lead to either a reward or a punishment. Therefore, an appropriate action needs to be chosen on the basis of the values of both expected rewards and expected punishments. To understand the underlying neural mechanisms, we conditioned monkeys using a Pavlovian procedure with two distinct contexts: one in which rewards were available and another in which punishments were feared. We found that the population of lateral habenula neurons was most strongly excited by a conditioned stimulus associated with the most unpleasant event in each context: the absence of the reward or the presence of the punishment. The population of lateral habenula neurons was also excited by the punishment itself and inhibited by the reward itself, especially when they were less predictable. These results suggest that the lateral habenula has the potential to adaptively control both reward-seeking and punishment-avoidance behaviors, presumably through its projections to dopaminergic and serotonergic systems.
Project description:To better understand the reward circuitry in human brain, we conducted activation likelihood estimation (ALE) and parametric voxel-based meta-analyses (PVM) on 142 neuroimaging studies that examined brain activation in reward-related tasks in healthy adults. We observed several core brain areas that participated in reward-related decision making, including the nucleus accumbens (NAcc), caudate, putamen, thalamus, orbitofrontal cortex (OFC), bilateral anterior insula, anterior cingulate cortex (ACC) and posterior cingulate cortex (PCC), as well as cognitive control regions in the inferior parietal lobule and prefrontal cortex (PFC). The NAcc was commonly activated by both positive and negative rewards across various stages of reward processing (e.g., anticipation, outcome, and evaluation). In addition, the medial OFC and PCC preferentially responded to positive rewards, whereas the ACC, bilateral anterior insula, and lateral PFC selectively responded to negative rewards. Reward anticipation activated the ACC, bilateral anterior insula, and brain stem, whereas reward outcome more significantly activated the NAcc, medial OFC, and amygdala. Neurobiological theories of reward-related decision making should therefore take distributed and interrelated representations of reward valuation and valence assessment into account.
Project description:The vigor with which humans and animals engage in a task is often a determinant of the likelihood of the task's success. An influential theoretical model suggests that the speed and rate at which responses are made should depend on the availability of rewards and punishments. While vigor facilitates the gathering of rewards in a bountiful environment, there is an incentive to slow down when punishments are forthcoming so as to decrease the rate of punishments, in conflict with the urge to perform fast to escape punishment. Previous experiments confirmed the former, leaving the latter unanswered. We tested the influence of punishment in an experiment involving economic incentives and contrasted this with reward related behavior on the same task. We found that behavior corresponded with the theoretical model; while instantaneous threat of punishment caused subjects to increase the vigor of their response, subjects' response times would slow as the overall rate of punishment increased. We quantitatively show that this is in direct contrast to increases in vigor in the face of increased overall reward rates. These results highlight the opposed effects of rewards and punishments and provide further evidence for their roles in the variety of types of human decisions.
Project description:Natural environments are uncertain. Uncertainty of emotional outcomes can induce anxiety and raise vigilance, promote and signal the opportunity for learning, modulate economic choice and regulate risk-seeking. Here we demonstrate that a subset of neurons in the anterodorsal region of the primate septum (ADS) are primarily devoted to processing uncertainty in a highly specific manner. Those neurons were selectively activated by visual cues indicating probabilistic delivery of reward (for example, 25%, 50% and 75% reward) and did not respond to cues indicating certain outcomes (0% and 100% reward). The average ADS uncertainty response was graded with the magnitude of reward uncertainty and selectively signaled uncertainty about rewards rather than punishments. The selective and graded information about reward uncertainty encoded by many neurons in the ADS may underlie modulation of uncertainty of value- and sensorimotor-related areas to regulate goal-directed behavior.
Project description:Feedback processing during decision making involves comparing anticipated and actual outcome. Although effects on ERPs of valence, magnitude, expectancy, and context during feedback processing have been extensively investigated, the electrophysiological processes underlying prediction formation in anticipation of feedback signals have received little attention. The aim of the present study was to explore these processes of prediction formation and their influence on subsequent feedback signals. Twenty healthy, right-handed volunteers performed a forced-choice task in which they had to indicate which of two presented objects was more expensive. After the volunteer's choice, an expert cue, which was accurate in 80% of trials, was presented to manipulate prediction formation about future reward and punishment. ERPs were recorded during presentation of the expert cue and during feedback. Results revealed that prediction formation of future rewards and punishments is accompanied by differences in the P2 component and a subsequent delay period. During feedback processing, the prediction-related P2 was associated with the processing of valence reflected in the feedback-related P2. Furthermore, the prediction-related difference in the delay period was associated with error processing in feedback-related medial frontal negativity. These findings suggest that prediction signals prior to feedback contain information about whether a prediction is correct or wrong (expectancy) and if the outcome will be a reward or punishment (valence).
Project description:Theories of instrumental learning aim to elucidate the mechanisms that integrate success and failure to improve future decisions. One computational solution consists of updating the value of choices in proportion to reward prediction errors, which are potentially encoded in dopamine signals. Accordingly, drugs that modulate dopamine transmission were shown to impact instrumental learning performance. However, whether these drugs act on conscious or subconscious learning processes remains unclear. To address this issue, we examined the effects of dopamine-related medications in a subliminal instrumental learning paradigm. To assess generality of dopamine implication, we tested both dopamine enhancers in Parkinson's disease (PD) and dopamine blockers in Tourette's syndrome (TS). During the task, patients had to learn from monetary outcomes the expected value of a risky choice. The different outcomes (rewards and punishments) were announced by visual cues, which were masked such that patients could not consciously perceive them. Boosting dopamine transmission in PD patients improved reward learning but worsened punishment avoidance. Conversely, blocking dopamine transmission in TS patients favored punishment avoidance but impaired reward seeking. These results thus extend previous findings in PD to subliminal situations and to another pathological condition, TS. More generally, they suggest that pharmacological manipulation of dopamine transmission can subconsciously drive us to either get more rewards or avoid more punishments.
Project description:The neural mechanisms supporting the ability to recognize and respond to fictive outcomes, outcomes of actions that one has not taken, remain obscure. We hypothesized that neurons in the anterior cingulate cortex (ACC), which monitors the consequences of actions and mediates subsequent changes in behavior, would respond to fictive reward information. We recorded responses of single neurons during performance of a choice task that provided information about the reward values of options that were not chosen. We found that ACC neurons signal fictive reward information and use a coding scheme similar to that used to signal experienced outcomes. Thus, individual ACC neurons process both experienced and fictive rewards.