Gregor Kohls

Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women

Motivation for goal-directed behaviour largely depends on the expected value of the anticipated reward. The aim of the present study was to examine how different levels of reward value are coded in the brain for two common forms of human reward: money and social approval. To account for gender differences 16 male and 16 female participants performed an incentive delay task expecting to win either money or positive social feedback. fMRI recording during the anticipation phase revealed proportional activation of neural structures constituting the human reward system for increasing levels of reward, independent of incentive type. However, in men activation in the prospect of monetary rewards encompassed a wide network of mesolimbic brain regions compared to only limited activation for social rewards. In contrast, in women, anticipation of either incentive type activated identical brain regions. Our findings represent an important step towards a better understanding of motivated behaviour by taking into account individual differences in reward valuation.

Dissociation of neural networks for anticipation and consumption of monetary and social rewards

Human behaviour is generally guided by the anticipation of potential outcomes that are considered to be rewarding. Reward processing can thus be dissected into a phase of reward anticipation and a phase of reward consumption. A number of brain structures have been suggested to be involved in reward processing. However, it is unclear whether anticipation and consumption are mediated by the same or different neural networks. We examined the neural basis of these processes using functional magnetic resonance imaging (fMRI) in an incentive delay task offering either money or social approval. In both conditions participants (N=28) were given a cue indicating potential reward. In order to receive reward a target button had to be pushed within a certain time window (adapted for individual reaction time). Cues triggering either monetary or social reward anticipation were presented sessionwise. Imaging was performed on a 1.5-Tesla Philips scanner in an event-related design. Anticipation of both reward types activated brain structures constituting the brain reward system including the ventral striatum. In contrast to the task independent activity in the anticipation phase, reward consumption evoked different patterns of activation for money and social approval, respectively. While social stimuli were mainly associated with amygdala activation, the thalamus was more strongly activated by the presentation of monetary rewards. Our results identify dissociable neural networks for the anticipation and consumption of reward. The findings implicate that the neural mechanisms underlying reward consumption are more modality-specific than those for reward anticipation, and that they are mediated by subjective reward value.

Reward System Dysfunction in Autism Spectrum Disorders

Although it has been suggested that social deficits of autism spectrum disorders (ASDs) are related to reward circuitry dysfunction, very little is known about the neural reward mechanisms in ASD. In the current functional magnetic resonance imaging study, we investigated brain activations in response to both social and monetary reward in a group of children with ASD, relative to matched controls. Participants with ASD showed the expected hypoactivation in the mesocorticolimbic circuitry in response to both reward types. In particular, diminished activation in the nucleus accumbens was observed when money, but not when social reward, was at stake, whereas the amygdala and anterior cingulate cortex were hypoactivated within the ASD group in response to both rewards. These data indicate that the reward circuitry is compromised in ASD in social as well as in non-social, i.e. monetary conditions, which likely contributes to atypical motivated behaviour. Taken together, with incentives used in this study sample, there is evidence for a general reward dysfunction in ASD. However, more ecologically valid social reward paradigms are needed to fully understand, whether there is any domain specificity to the reward deficit that appears evident in ASD, which would be most consistent with the ASD social phenotype.

Social ‘wanting’ dysfunction in autism: neurobiological underpinnings and treatment implications

Most behavioral training regimens in autism spectrum disorders (ASD) rely on reward-based reinforcement strategies. Although proven to significantly increase both cognitive and social outcomes and successfully reduce aberrant behaviors, this approach fails to benefit a substantial number of affected individuals. Given the enormous amount of clinical and financial resources devoted to behavioral interventions, there is a surprisingly large gap in our knowledge of the basic reward mechanisms of learning in ASD. Understanding the mechanisms for reward responsiveness and reinforcement-based learning is urgently needed to better inform modifications that might improve current treatments. The fundamental goal of this review is to present a fine-grained literature analysis of reward function in ASD with reference to a validated neurobiological model of reward: the ‘wanting’/’liking’ framework. Despite some inconsistencies within the available literature, the evaluation across three converging sets of neurobiological data (neuroimaging, electrophysiological recordings, and neurochemical measures) reveals good evidence for disrupted reward-seeking tendencies in ASD, particularly in social contexts. This is most likely caused by dysfunction of the dopaminergic–oxytocinergic ‘wanting’ circuitry, including the ventral striatum, amygdala, and ventromedial prefrontal cortex. Such a conclusion is consistent with predictions derived from diagnostic criteria concerning the core social phenotype of ASD, which emphasize difficulties with spontaneous self-initiated seeking of social encounters (that is, social motivation). Existing studies suggest that social ‘wanting’ tendencies vary considerably between individuals with ASD, and that the degree of social motivation is both malleable and predictive of intervention response. Although the topic of reward responsiveness in ASD is very new, with much research still needed, the current data clearly point towards problems with incentive-based motivation and learning, with clear and important implications for treatment. Given the reliance of behavioral interventions on reinforcement-based learning principles, we believe that a systematic focus on the integrity of the reward system in ASD promises to yield many important clues, both to the underlying mechanisms causing ASD and to enhancing the efficacy of existing and new interventions.

Atypical Brain Responses to Reward Cues in Autism as Revealed by Event-Related Potentials

Social motivation deficit theories suggest that children with autism do not properly anticipate and appreciate the pleasure of social stimuli. In this study, we investigated event-related brain potentials evoked by cues that triggered social versus monetary reward anticipation in children with autism. Children with autism showed attenuated P3 activity in response to cues associated with a timely reaction to obtain a reward, irrespective of reward type. We attribute this atypical P3 activity in response to reward cues as reflective of diminished motivated attention to reward signals, a possible contributor to reduced social motivation in autism. Thus, our findings suggest a general reward processing deficit rather than a specific social reward dysfunction in autism.

Hyperresponsiveness to social rewards in children and adolescents with attention-deficit/hyperactivity disorder (ADHD)

BackgroundCurrent research suggests that attention-deficit/hyperactivity disorder (ADHD) is associated with larger behavioral sensitivity to reinforcement contingencies. However, most studies have focused thus far on the enhancing effects of tangible rewards such as money, neglecting that social-emotional stimuli may also impact task performance in ADHD patients.MethodsTo determine whether non-social (monetary) and social (positive facial expressions) rewards differentially improve response inhibition accuracy in children and adolescents with ADHD, we applied an incentive go/no-go task with reward contingencies for successful inhibition and compared ADHD subjects with typically developing individuals.ResultsBoth social and monetary contingencies improved inhibition accuracy in all participants. However, individuals with ADHD displayed a particularly higher profit from social reward than healthy controls, suggesting that cognitive control in ADHD patients can be specifically improved by social reinforcement. By contrast, self-rated motivation associated with task performance was significantly lower in ADHD patients.ConclusionOur findings provide evidence for hyperresponsiveness to social rewards in ADHD patients, which is accompanied by limited self-awareness. These data suggest that social reward procedures may be particularly useful in behavioral interventions in children with ADHD.

Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials

Diminished responsivity to reward incentives is a key contributor to the social-communication problems seen in autism spectrum disorders (ASDs). Social motivation theories suggest that individuals with ASD do not experience social interactions as rewarding, leading to negative consequences for the development of brain circuitry subserving social information. In this study, we examined neural responses to social and non-social reward anticipation in 35 typically developing young adults, examining modulation of reward sensitivity by level of autistic traits. Using an Event-related potential incentive-delay task incorporating novel, more ecologically valid forms of reward, higher expression of autistic traits was associated with an attenuated P3 response to the anticipation of social (simulated real-time video feedback from an observer), but not non-social (candy), rewards. Exploratory analyses revealed that this was unrelated to mentalizing ability. The P3 component reflects motivated attention to reward signals, suggesting attenuated motivation allocation specific to social incentives. The study extends prior findings of atypical reward anticipation in ASD, demonstrating that attenuated social reward responsiveness extends to autistic traits in the range of typical functioning. Results support the development of innovative paradigms for investigating social and non-social reward responsiveness. Insight into vulnerabilities in reward processing is critical for understanding social function in ASD.

Atypical laterality of resting gamma oscillations in autism spectrum disorders.

Abnormal brain oscillatory activity has been found in autism spectrum disorders (ASD) and proposed as a potential biomarker. While several studies have investigated gamma oscillations in ASD, none have examined resting gamma power across multiple brain regions. This study investigated resting gamma power using EEG in 15 boys with ASD and 18 age and intelligence quotient matched typically developing controls. We found a decrease in resting gamma power at right lateral electrodes in ASD. We further explored associations between gamma and ASD severity as measured by the Social Responsiveness Scale (SRS) and found a negative correlation between SRS and gamma power. We believe that our findings give further support of gamma oscillations as a potential biomarker for ASD.

Neural evidence for an association between social proficiency and sensitivity to social reward

Data from developmental psychology suggests a link between the growth of socio-emotional competences and the infants sensitivity to the salience of social stimuli. The aim of the present study was to find evidence for this relationship in healthy adults. Thirty-five participants were recruited based on their score above the 85th or below the 15th percentile of the empathy quotient questionnaire (EQ, Baron-Cohen and Wheelwright, 2004). Functional magnetic resonance imaging (fMRI) was used to compare neural responses to cues of social and non-social (monetary) reward. When compared to the high-EQ group, the low-EQ group showed reduced activity of the brain s reward system, specifically the right nucleus accumbens, in response to cues predictive of social reward (videos showing gestures of approval)-but increased activation in this area for monetary incentives. Our data provide evidence for a link between self-reported deficits in social proficiency and reduced sensitivity to the motivational salience of positive social stimuli.

Differentiating neural reward responsiveness in autism versus ADHD.

Highlights • Brain responsiveness to social and monetary reward were studied in ADHD versus ASD.• Clinical groups versus TDC had different ventral striatum activation to both rewards.• Medial prefrontal overactivation in response to social reward was ADHD specific.• Ventral striatal underactivation in response to monetary reward was ASD specific.• Fronto-striato-parietal underactivation for money was shared by both clinical groups.