Motor Preparatory Activity in Posterior Parietal Cortex is Modulated by Subjective Absolute Value

For optimal response selection, the consequences associated with behavioral success or failure must be appraised. To determine how monetary consequences influence the neural representations of motor preparation, human brain activity was scanned with fMRI while subjects performed a complex spatial visuomotor task. At the beginning of each trial, reward context cues indicated the potential gain and loss imposed for correct or incorrect trial completion. FMRI-activity in canonical reward structures reflected the expected value related to the context. In contrast, motor preparatory activity in posterior parietal and premotor cortex peaked in high “absolute value” (high gain or loss) conditions: being highest for large gains in subjects who believed they performed well while being highest for large losses in those who believed they performed poorly. These results suggest that the neural activity preceding goal-directed actions incorporates the absolute value of that action, predicated upon subjective, rather than objective, estimates of one's performance

Temporal characteristics of the influence of punishment on perceptual decision making in the human brain

Perceptual decision making is the process by which information from sensory systems is combined and used to influence our behavior. In addition to the sensory input, this process can be affected by other factors, such as reward and punishment for correct and incorrect responses. To investigate the temporal dynamics of how monetary punishment influences perceptual decision making in humans, we collected electroencephalography (EEG) data during a perceptual categorization task whereby the punishment level for incorrect responses was parametrically manipulated across blocks of trials. Behaviorally, we observed improved accuracy for high relative to low punishment levels. Using multivariate linear discriminant analysis of the EEG, we identified multiple punishment-induced discriminating components with spatially distinct scalp topographies. Compared with components related to sensory evidence, components discriminating punishment levels appeared later in the trial, suggesting that punishment affects primarily late postsensory, decision-related processing. Crucially, the amplitude of these punishment components across participants was predictive of the size of the behavioral improvements induced by punishment. Finally, trial-by-trial changes in prestimulus oscillatory activity in the alpha and gamma bands were good predictors of the amplitude of these components. We discuss these findings in the context of increased motivation/attention, resulting from increases in punishment, which in turn yields improved decision-related processing

Neural Correlates of Opponent Processes for Financial Gains and Losses

Objective: Functional imaging studies offer alternative explanations for the neural correlates of monetary gain and loss related brain activity, and their opponents, omission of gains and losses. One possible explanation based on the psychology of opponent process theory suggests that successful avoidance of an aversive outcome is itself rewarding, and hence activates brain regions involved in reward processing. In order to test this hypothesis, we compared brain activation for successful avoidance of losses and receipt of monetary gains. Additionally, the brain regions involved in processing of frustrative neutral outcomes and actual losses were compared in order to test whether these two representations are coded in common or distinct brain regions. Methods: Using a 3 Tesla functional magnetic resonance imaging machine, fifteen healthy volunteers between the ages 22 to 28 were scanned for blood oxygen level dependent signal changes while they were performing a probabilistic learning task, wherein each trial a participant chose one of the two available options in order to win or avoid losing money. Results: The results confirmed, previous findings showing that medial frontal cortex and ventral striatum show significant activation (p<0.001) not only for monetary gains but also for successful avoidance of losses. A similar activation pattern was also observed for monetary losses and avoidance of gains in the medial frontal cortex, and posterior cingulate cortex, however, there was increased activation in amygdala specific to monetary losses (p<0.001). Further, subtraction analysis showed that regardless of the type of loss (i.e., frustrative neutral outcomes) posterior insula showed increased activation. Conclusion: This study provides evidence for a significant overlap not only between gains and losses, but also between their opponents. The results suggested that the overlapping activity pattern in the medial frontal cortex could be explained by a more abstract function of medial frontal cortex, such as outcome evaluation or performance monitoring, which possibly does not differentiate between winning and losing monetary outcomes.Peer reviewedFinal Published versio

Identification of an Operant Learning Circuit by Whole Brain Functional Imaging in Larval Zebrafish

When confronted with changing environments, animals can generally adjust their behavior to optimize reward and minimize punishment. The process of modifying one's behavior based on its consequences is referred to as operant or instrumental learning. Operant learning makes specific demands on the animal. The animal must exhibit some flexibility in its behavior, switching from unsuccessful motor responses to potentially successful ones. The animal must represent the consequence of its actions. Finally, the animal must select the correct response based on its past history of reinforcement. Studies in mammalian systems have found competing and complementary circuits in the cortex and striatum that mediate different aspects of this learning process. The larval zebrafish is an ideal system to extend the study of operant learning due to its genetic and optical properties. We have developed a behavioral paradigm and imaging system that have allowed us to comprehensively image neural activity throughout the zebrafish brain during the process of operant conditioning. Our analysis of the neural network activity underlying this learning process reveals several classes of neurons whose activity correlates with learning and decision making. The distribution of these learning-related neurons is highly localized to regions of the habenula and forebrain. We describe, in particular, a lateralized habenula circuit that may encode prediction and relief prediction error

Dysfunctional Social Reinforcement Processing in Disruptive Behavior Disorders: An Functional Magnetic Resonance Imaging Study.

ObjectivePrior functional magnetic resonance imaging (fMRI) work has revealed that children/adolescents with disruptive behavior disorders (DBDs) show dysfunctional reward/non-reward processing of non-social reinforcements in the context of instrumental learning tasks. Neural responsiveness to social reinforcements during instrumental learning, despite the importance of this for socialization, has not yet been previously investigated.MethodsTwenty-nine healthy children/adolescents and 19 children/adolescents with DBDs performed the fMRI social/non-social reinforcement learning task. Participants responded to random fractal image stimuli and received social and non-social rewards/non-rewards according to their accuracy.ResultsChildren/adolescents with DBDs showed significantly reduced responses within the caudate and posterior cingulate cortex (PCC) to non-social (financial) rewards and social non-rewards (the distress of others). Connectivity analyses revealed that children/adolescents with DBDs have decreased positive functional connectivity between the ventral striatum (VST) and the ventromedial prefrontal cortex (vmPFC) seeds and the lateral frontal cortex in response to reward relative to non-reward, irrespective of its sociality. In addition, they showed decreased positive connectivity between the vmPFC seed and the amygdala in response to non-reward relative to reward.ConclusionThese data indicate compromised reinforcement processing of both non-social rewards and social non-rewards in children/adolescents with DBDs within core regions for instrumental learning and reinforcement-based decision- making (caudate and PCC). In addition, children/adolescents with DBDs show dysfunctional interactions between the VST, vmPFC, and lateral frontal cortex in response to rewarded instrumental actions potentially reflecting disruptions in attention to rewarded stimuli

Task-load-dependent activation of dopaminergic midbrain areas in the absence of reward

Dopamine release in cortical and subcortical structures plays a central role in reward-related neural processes. Within this context, dopaminergic inputs are commonly assumed to play an activating role, facilitating behavioral and cognitive operations necessary to obtain a prospective reward. Here, we provide evidence from human fMRI that this activating role can also be mediated by task-demand-related processes and thus extendsbeyondsituationsthatonlyentailextrinsicmotivatingfactors. Using a visual discrimination task in which varying levels of task demands were precued, we found enhanced hemodynamic activity in the substantia nigra (SN) for high task demands in the absence of reward or similar extrinsic motivating factors. This observation thus indicates that the SN can also be activated in an endogenous fashion. In parallel to its role in reward-related processes, reward-independent activation likely serves to recruit the processing resources needed to meet enhanced task demands. Simultaneously, activity in a wide network of cortical and subcortical control regions was enhanced in response to high task demands, whereas areas of the default-mode network were deactivated more strongly. The present observations suggest that the SN represents a core node within a broader neural network that adjusts the amount of available neural and behavioral resources to changing situational opportunities and task requirements, which is often driven by extrinsic factors but can also be controlled endogenously

Reward and punishment: the neural correlates of reinforcement feedback during motor learning

‘By the carrot or the stick’ reward or punishment has been contemplated by instructors to motivate their pupils to learn a new motor skill. The reinforcements of reward and punishment have demonstrated dissociable effects on motor learning with punishment enhancing the learning rate and reward increasing retention of the motor task. However it is still unclear how the brain processes reward and punishment during motor learning. This study sought to investigate the role of reinforcement feedback in cortical neural activity associated with motor learning. A novel visuomotor rotation task was employed with reward punishment or null feedback as the participants adapted their movement to a 30-degree counter-clockwise rotation. We measured movement time and task accuracy throughout the task. Surface electroencephalography was utilized to record cortical neural activity throughout the learning and retention of the motor task. Event-related potentials (ERPs) were calculated to assess how the brain processes the reinforcement feedback and prepares for movement. Repeated measures ANOVAs were utilized to detect differences in the movement parameters and ERP amplitudes. This study found that reward and punishment feedback did not produce different effects on the rate of task learning. However punishment feedback impaired the retention (memory) of the motor task. These behavioral effects were accompanied by changes in the amplitude of ERPs during feedback presentation and movement preparation. These results suggest that punishment feedback alters brain processes involved in memory formation during motor learning