Social motivation theory suggests that deficits in social reward processing underlie social impairments in autism spectrum disorders (ASD). However, the extent to which abnormalities in reward processing generalize to other classes of stimuli remains unresolved. The aim of the current study was to examine if reward processing abnormalities in ASD are specific to social stimuli or can be generalized to other classes of reward. Additionally, we sought to examine the results in the light of behavioral impairments in ASD.
Participants performed adapted versions of the social and monetary incentive delay tasks. Data from 21 unmedicated right-handed male participants with ASD and 21 age- and IQ-matched controls were analyzed using a factorial design to examine the blood-oxygen-level-dependent (BOLD) response during the anticipation and receipt of both reward types.
Behaviorally, the ASD group showed less of a reduction in reaction time (RT) for rewarded compared to unrewarded trials than the control group. In terms of the fMRI results, there were no significant group differences in reward circuitry during reward anticipation. During the receipt of rewards, there was a significant interaction between group and reward type in the left dorsal striatum (DS). The ASD group showed reduced activity in the DS compared to controls for social rewards but not monetary rewards and decreased activation for social rewards compared to monetary rewards. Controls showed no significant difference between the two reward types. Increased activation in the DS during social reward processing was associated with faster response times for rewarded trials, compared to unrewarded trials, in both groups. This is in line with behavioral results indicating that the ASD group showed less of a reduction in RT for rewarded compared to unrewarded trials. Additionally, de-activation to social rewards was associated with increased repetitive behavior in ASD.
In line with social motivation theory, the ASD group showed reduced activation, compared to controls, during the receipt of social rewards in the DS. Groups did not differ significantly during the processing of monetary rewards. BOLD activation in the DS, during social reward processing, was associated with behavioral impairments in ASD.
Autism; Reward; Social motivation; Striatum; Functional magnetic resonance imaging; fMRI
One hypothesis for the social deficits that characterize autism spectrum disorders (ASD) is diminished neural reward response to social interaction and attachment. Prior research using established monetary reward paradigms as a test of non-social reward to compare with social reward may involve confounds in the ability of individuals with ASD to utilize symbolic representation of money and the abstraction required to interpret monetary gains. Thus, a useful addition to our understanding of neural reward circuitry in ASD includes a characterization of the neural response to primary rewards.
We asked 17 children with ASD and 18 children without ASD to abstain from eating for at least four hours before an MRI scan in which they viewed images of high-calorie foods. We assessed the neural reward network for increases in the blood oxygenation level dependent (BOLD) signal in response to the food images
We found very similar patterns of increased BOLD signal to these images in the two groups; both groups showed increased BOLD signal in the bilateral amygdala, as well as in the nucleus accumbens, orbitofrontal cortex, and insula. Direct group comparisons revealed that the ASD group showed a stronger response to food cues in bilateral insula along the anterior-posterior gradient and in the anterior cingulate cortex than the control group, whereas there were no neural reward regions that showed higher activation for controls than for ASD.
These results suggest that neural response to primary rewards is not diminished but in fact shows an aberrant enhancement in children with ASD.
A leading hypothesis to explain the social dysfunction in people with autism spectrum disorders (ASD) is that they exhibit a deficit in reward processing and motivation specific to social stimuli. However, there have been few direct tests of this hypothesis to date. Here we used an instrumental reward learning task that contrasted learning with social rewards (pictures of positive and negative faces) against learning with monetary reward (winning and losing money). The two tasks were structurally identical except for the type of reward, permitting direct comparisons. We tested 10 high-functioning people with ASD (7M, 3F) and 10 healthy controls who were matched on gender, age, and education. We found no significant differences between the two groups in terms of overall ability behaviorally to discriminate positive from negative slot machines, reaction-times, and valence ratings, However, there was a specific impairment in the ASD group in learning to choose social rewards, compared to monetary rewards: they had a significantly lower cumulative number of choices of the most rewarding social slot machine, and had a significantly slower initial learning rate for the socially rewarding slot machine, compared to the controls. The findings show a deficit in reward learning in ASD that is greater for social rewards than for monetary rewards, and support the hypothesis of a disproportionate impairment in social reward processing in ASD.
social reward; monetary reward; autism
This thematic series presents theoretical and empirical papers focused on understanding autism from the perspective of reward processing deficits. Although the core symptoms of autism have not traditionally been conceptualized with respect to altered reward-based processes, it is clear that brain reward circuitry plays a critical role in guiding social and nonsocial learning and behavior throughout development. Additionally, brain reward circuitry may respond to social sources of information in ways that are similar to responses to primary rewards, and recent clinical data consistently suggest abnormal behavioral and neurobiologic responses to rewards in autism. This thematic series presents empirical data and review papers that highlight the utility of considering autism from the perspective of reward processing deficits. Our hope is that this novel framework may further elucidate autism pathophysiology, with the ultimate goal of yielding novel insights with potential therapeutic implications.
Learning to make choices that yield rewarding outcomes requires the computation of three distinct signals: stimulus values that are used to guide choices at the time of decision making, experienced utility signals that are used to evaluate the outcomes of those decisions and prediction errors that are used to update the values assigned to stimuli during reward learning. Here we investigated whether monetary and social rewards involve overlapping neural substrates during these computations. Subjects engaged in two probabilistic reward learning tasks that were identical except that rewards were either social (pictures of smiling or angry people) or monetary (gaining or losing money). We found substantial overlap between the two types of rewards for all components of the learning process: a common area of ventromedial prefrontal cortex (vmPFC) correlated with stimulus value at the time of choice and another common area of vmPFC correlated with reward magnitude and common areas in the striatum correlated with prediction errors. Taken together, the findings support the hypothesis that shared anatomical substrates are involved in the computation of both monetary and social rewards.
social reward; monetary reward; ventromedial prefrontal cortex; ventral striatum
Efficient effort expenditure to obtain rewards is critical for optimal goal-directed behavior and learning. Clinical observation suggests that individuals with autism spectrum disorders (ASD) may show dysregulated reward-based effort expenditure, but no behavioral study to date has assessed effort-based decision-making in ASD.
The current study compared a group of adults with ASD to a group of typically developing adults on the Effort Expenditure for Rewards Task (EEfRT), a behavioral measure of effort-based decision-making. In this task, participants were provided with the probability of receiving a monetary reward on a particular trial and asked to choose between either an “easy task” (less motoric effort) for a small, stable reward or a “hard task” (greater motoric effort) for a variable but consistently larger reward.
Participants with ASD chose the hard task more frequently than did the control group, yet were less influenced by differences in reward value and probability than the control group. Additionally, effort-based decision-making was related to repetitive behavior symptoms across both groups.
These results suggest that individuals with ASD may be more willing to expend effort to obtain a monetary reward regardless of the reward contingencies. More broadly, results suggest that behavioral choices may be less influenced by information about reward contingencies in individuals with ASD. This atypical pattern of effort-based decision-making may be relevant for understanding the heightened reward motivation for circumscribed interests in ASD.
Reward; Motivation; Decision-making; Autism spectrum disorders; Dopamine
It has recently been suggested that schizophrenia involves dysfunction in brain connectivity at a neural level, and a dysfunction in reward processing at a behavioral level. The purpose of the present study was to link these two levels of analyses by examining effective connectivity patterns between brain regions mediating reward learning in patients with schizophrenia and healthy, age-matched controls. To this aim, we used functional magnetic resonance imaging and galvanic skin recordings (GSR) while patients and controls performed an appetitive conditioning experiment with visual cues as the conditioned (CS) stimuli, and monetary reward as the appetitive unconditioned stimulus (US). Based on explicit stimulus contingency ratings, conditioning occurred in both groups; however, based on implicit, physiological GSR measures, patients failed to show differences between CS+ and CS− conditions. Healthy controls exhibited increased blood-oxygen-level dependent (BOLD) activity across striatal, hippocampal, and prefrontal regions and increased effective connectivity from the ventral striatum to the orbitofrontal cortex (OFC BA 11) in the CS+ compared to the CS− condition. Compared to controls, patients showed increased BOLD activity across a similar network of brain regions, and increased effective connectivity from the striatum to hippocampus and prefrontal regions in the CS− compared to the CS+ condition. The findings of increased BOLD activity and effective connectivity in response to the CS− in patients with schizophrenia offer insight into the aberrant assignment of motivational salience to non-reinforced stimuli during conditioning that is thought to accompany schizophrenia.
schizophrenia; appetitive conditioning; fMRI; effective connectivity
Social interaction deficits and restricted repetitive behaviors and interests that characterize autism spectrum disorders (ASDs) may both reflect aberrant functioning of brain reward circuits. However, no neuroimaging study to date has investigated the integrity of reward circuits using an incentive delay paradigm in individuals with ASDs. In the present study, we used functional magnetic resonance imaging to assess blood-oxygen level-dependent activation during reward anticipation and outcomes in 15 participants with an ASD and 16 matched control participants. Brain activation was assessed during anticipation of and in response to monetary incentives and object image incentives previously shown to be visually salient for individuals with ASDs (e.g. trains, electronics). Participants with ASDs showed decreased nucleus accumbens activation during monetary anticipation and outcomes, but not during object anticipation or outcomes. Group × reward-type-interaction tests revealed robust interaction effects in bilateral nucleus accumbens during reward anticipation and in ventromedial prefrontal cortex during reward outcomes, indicating differential responses contingent on reward type in these regions. Results suggest that ASDs are characterized by reward-circuitry hypoactivation in response to monetary incentives but not in response to autism-relevant object images. The clinical implications of the double dissociation of reward type and temporal phase in reward circuitry function in ASD are discussed.
autism; reward; nucleus accumbens; anticipation; functional magnetic resonance imaging
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.
anticipation; social reward; monetary reward; gender; nucleus accumbens
Previous reports have described that neural activities in midbrain dopamine areas are sensitive to unexpected reward delivery and omission. These activities are correlated with reward prediction error in reinforcement learning models, the difference between predicted reward values and the obtained reward outcome. These findings suggest that the reward prediction error signal in the brain updates reward prediction through stimulus–reward experiences. It remains unknown, however, how sensory processing of reward-predicting stimuli contributes to the computation of reward prediction error. To elucidate this issue, we examined the relation between stimulus discriminability of the reward-predicting stimuli and the reward prediction error signal in the brain using functional magnetic resonance imaging (fMRI). Before main experiments, subjects learned an association between the orientation of a perceptually salient (high-contrast) Gabor patch and a juice reward. The subjects were then presented with lower-contrast Gabor patch stimuli to predict a reward. We calculated the correlation between fMRI signals and reward prediction error in two reinforcement learning models: a model including the modulation of reward prediction by stimulus discriminability and a model excluding this modulation. Results showed that fMRI signals in the midbrain are more highly correlated with reward prediction error in the model that includes stimulus discriminability than in the model that excludes stimulus discriminability. No regions showed higher correlation with the model that excludes stimulus discriminability. Moreover, results show that the difference in correlation between the two models was significant from the first session of the experiment, suggesting that the reward computation in the midbrain was modulated based on stimulus discriminability before learning a new contingency between perceptually ambiguous stimuli and a reward. These results suggest that the human reward system can incorporate the level of the stimulus discriminability flexibly into reward computations by modulating previously acquired reward values for a typical stimulus.
Few studies have examined underlying mechanisms linking social behavior, motivated behavior, and reward and punishment systems. The current study was designed to investigate these mechanisms by examining responses to both rewarding and punishing non-social stimuli in shy and non-shy adults. Ninety-three participants, comprising three social behavior groups (Shy, Non-shy, Control) completed the Monetary Incentive Delay task. Consistent with previous research, all participants were sensitive to incentive manipulations. There were also significant individual differences in response. Non-shy participants demonstrated sensitivity to both reward and punishment stimuli, and behavior indicative of high levels of arousal in approach motivation. Shy individuals demonstrated a large discrepancy in sensitivity to reward compared to punishment, with this discrepancy being driven by enhanced sensitivity to reward. Their behavior suggested conflict generated by increased arousal in both approach and withdrawal motivation systems. Current findings contribute to theoretical accounts of relations between social behavior and behavior modulated by reward and punishment. These findings carry implications for the study of psychopathology and neuroimaging research designed to examine relationships between social behavior, motivated behavior, and underlying reward and punishment systems.
Motivation; Reward; Punishment; Social behavior; Shyness; Anxiety; Behavioral inhibition
Problems with reward system function have been posited as a primary difficulty in autism spectrum disorders. The current study examined an electrophysiological marker of feedback monitoring, the feedback-related negativity (FRN), during a monetary reward task. The study advanced prior understanding by focusing exclusively on a developmental sample, applying rigorous diagnostic characterization and introducing an experimental paradigm providing more subtly different feedback valence (reward versus non-reward instead of reward versus loss).
Twenty-six children with autism spectrum disorder and 28 typically developing peers matched on age and full-scale IQ played a guessing game resulting in monetary gain (“win”) or neutral outcome (“draw”). ERP components marking early visual processing (N1, P2) and feedback appraisal (FRN) were contrasted between groups in each condition, and their relationships to behavioral measures of social function and dysfunction, social anxiety, and autism symptomatology were explored.
FRN was observed on draw trials relative to win trials. Consistent with prior research, children with ASD exhibited a FRN to suboptimal outcomes that was comparable to typical peers. ERP parameters were unrelated to behavioral measures.
Results of the current study indicate typical patterns of feedback monitoring in the context of monetary reward in ASD. The study extends prior findings of normative feedback monitoring to a sample composed exclusively of children and demonstrates that, as in typical development, individuals with autism exhibit a FRN to suboptimal outcomes, irrespective of neutral or negative valence. Results do not support a pervasive problem with reward system function in ASD, instead suggesting any dysfunction lies in more specific domains, such as social perception, or in response to particular feedback-monitoring contexts, such as self-evaluation of one’s errors.
Autism spectrum disorder; Reward processing; Event-related potentials; Electroencephalography; ERP; EEG; Feedback-related negativity; Medial-frontal negativity
The autism spectrum disorders (ASDs) arise from a diverse array of genetic and environmental origins that disrupt the typical developmental trajectory of neural connectivity and synaptogenesis. ASDs are marked by dysfunctional social behavior and cognition, among other deficits. Greater understanding of the biological substrates of typical social behavior in animal models will further our understanding of the etiology of ASDs. Despite the precision and tractability of molecular genetics models of ASDs in rodents, these organisms lack the complexity of human social behavior, thus limiting their impact on understanding ASDs to basic mechanisms. Non-human primates (NHPs) provide an attractive, complementary model for ASDs, due in part to the complexity and dynamics of social structures, reliance on vision for social signaling, and deep homology in brain circuitry mediating social behavior and reward. This knowledge is based on a rich literature, compiled over 50 years of observing primate behavior in the wild, which, in the case of rhesus macaques, is complemented by a large body of research characterizing neuronal activity during cognitive behavior. Several recent developments in this field are directly relevant to ASDs, including how the brain represents the perceptual features of social stimuli, how social information influences attention processes in the brain, and how the value of social interaction is computed. Because the symptoms of ASDs may represent extreme manifestations of traits that vary in intensity within the general population, we will additionally discuss ways in which nonhuman primates also show variation in social behavior and reward sensitivity. In cases where variation in species-typical behavior is analogous to similar variations in human behavior, we believe that study of the neural circuitry underlying this variation will provide important insights into the systems-level mechanisms contributing to ASD pathology.
Autism; Asperger’s; Non-human primate; Monkey
Purpose of review
This paper reviews current work investigating the neural bases of autism spectrum disorder (ASD) within the discipline of electrophysiological brain research. The manuscript focuses primarily on advances in understanding related to social information processing and interconnectivity among brain systems in ASD.
Recent research indicates anomalous function of social brain regions in ASD and highlights the specificity of processing problems to these systems. Atypical activity in this circuitry may reflect genetic susceptibility for ASD, with increased activity in compensatory areas marking the distinction between developing or not developing the disorder. Advances in understanding connectivity in ASD are highlighted by novel work providing initial evidence of atypical interconnectivity in infancy.
Emerging understanding of neural dysfunction in ASD indicates consistent but heterogeneous dysfunction across brain systems in ASD. Key objectives for the immediate future include: the use of multimethod approaches that encompass temporal and spatial imaging; behavioral phenotyping carried out in developmental context to reveal subgroups defined uniquely by trajectories; and individual-specific profiles of behavioral performance and brain function.
Autism Spectrum Disorder; social neuroscience; electrophysiology; EEG; ERP
Autism spectrum disorders (ASD) are characterized by significant social impairments, including deficits in orienting attention following social cues. Behavioral studies investigating social orienting in ASD, however, have yielded mixed results, as the use of naturalistic paradigms typically reveals clear deficits whereas computerized laboratory experiments often report normative behavior. The present study is the first to examine the neural mechanisms underlying social orienting in ASD in order to provide new insight into the social attention impairments that characterize this disorder. Using fMRI, we examined the neural correlates of social orienting in children and adolescents with ASD and in a matched sample of typically developing (TD) controls while they performed a spatial cueing paradigm with social (eye gaze) and nonsocial (arrow) cues. Cues were either directional (indicating left or right) or neutral (indicating no direction), and directional cues were uninformative of the upcoming target location in order to engage automatic processes by minimizing expectations. Behavioral results demonstrated intact orienting effects for social and nonsocial cues, with no differences between groups. The imaging results, however, revealed clear group differences in brain activity. When attention was directed by social cues compared to nonsocial cues, the TD group showed increased activity in frontoparietal attention networks, visual processing regions, and the striatum, whereas the ASD group only showed increased activity in the superior parietal lobule. Significant group × cue type interactions confirmed greater responsivity in task-relevant networks for social cues than nonsocial cues in TD as compared to ASD, despite similar behavioral performance. These results indicate that, in the autistic brain, social cues are not assigned the same privileged status as they are in the typically developing brain. These findings provide the first empirical evidence that the neural circuitry involved in social orienting is disrupted in ASD and highlight that normative behavioral performance in a laboratory setting may reflect compensatory mechanisms rather than intact social attention.
autism; attention; functional magnetic resonance imaging; gaze; social cue
It has been reported that individuals with autism spectrum disorder (ASD) have abnormal responses to the sensory environment. For these individuals sensory overload can impair functioning, raise physiological stress, and adversely affect social interaction. Early-stage (i.e. within 200ms of stimulus onset) auditory processing abnormalities have been widely examined in ASD using event-related potentials (ERP), while ERP studies investigating early-stage visual processing in ASD are less frequent. We wanted to test the hypothesis of early-stage visual processing abnormalities in ASD by investigating ERPs elicited in a visual oddball task using illusory figures. Our results indicate that individuals with ASD have abnormally large cortical responses to task irrelevant stimuli over both parieto-occipital and frontal regions-of-interest (ROI) during early stages of visual processing compared to the control group. Furthermore, ASD patients showed signs of an overall disruption in stimulus discrimination, and had a significantly higher rate of motor response errors.
Autism; event-related potentials; EEG; visual processing; evoked potentials
Individuals with autism spectrum disorders (ASD) demonstrate increased visual attention and elevated brain reward circuitry responses to images related to circumscribed interests (CI), suggesting that a heightened affective response to CI may underlie their disproportionate salience and reward value in ASD. To determine if individuals with ASD differ from typically developing (TD) adults in their subjective emotional experience of CI object images, non-CI object images and social images, 213 TD adults and 56 adults with ASD provided arousal ratings (sensation of being energized varying along a dimension from calm to excited) and valence ratings (emotionality varying along dimension of approach to withdrawal) for a series of 114 images derived from previous research on CI. The groups did not differ on arousal ratings for any image type, but ASD adults provided higher valence ratings than TD adults for CI-related images, and lower valence ratings for social images. Even after co-varying the effects of sex, the ASD group, but not the TD group, gave higher valence ratings to CI images than social images. These findings provide additional evidence that ASD is characterized by a preference for certain categories of non-social objects and a reduced preference for social stimuli, and support the dissemination of this image set for examining aspects of the circumscribed interest phenotype in ASD.
The human striatum is integral for reward-processing and supports learning by linking experienced outcomes with prior expectations. Recent endeavors implicate the striatum in processing outcomes of social interactions, such as social approval/rejection, as well as in learning reputations of others. Interestingly, social impressions often influence our behavior with others during interactions. Information about an interaction partner’s moral character acquired from biographical information hinders updating of expectations after interactions via top down modulation of reward circuitry. An outstanding question is whether initial impressions formed through experience similarly modulate the ability to update social impressions at the behavioral and neural level. We investigated the role of experienced social information on trust behavior and reward-related BOLD activity. Participants played a computerized ball-tossing game with three fictional partners manipulated to be perceived as good, bad, or neutral. Participants then played an iterated trust game as investors with these same partners while undergoing fMRI. Unbeknownst to participants, partner behavior in the trust game was random and unrelated to their ball-tossing behavior. Participants’ trust decisions were influenced by their prior experience in the ball-tossing game, investing less often with the bad partner compared to the good and neutral. Reinforcement learning models revealed that participants were more sensitive to updating their beliefs about good and bad partners when experiencing outcomes consistent with initial experience. Increased striatal and anterior cingulate BOLD activity for positive versus negative trust game outcomes emerged, which further correlated with model-derived prediction error learning signals. These results suggest that initial impressions formed from direct social experience can be continually shaped by consistent information through reward learning mechanisms.
trust; learning; social experience; reward; striatum; prediction error
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.
Autism spectrum disorders; Reward; Social motivation; Ventral striatum; Ventromedial prefrontal cortex; Amygdala; Dopamine; Oxytocin; Opioids; Treatment
The human reward system is sensitive to both social (e.g., validation) and non-social rewards (e.g., money) and is likely integral for relationship development and reputation building. However, data is sparse on the question of whether implicit social reward processing meaningfully contributes to explicit social representations such as trust and attachment security in pre-existing relationships. This event-related fMRI experiment examined reward system prediction-error activity in response to a potent social reward—social validation—and this activity's relation to both attachment security and trust in the context of real romantic relationships. During the experiment, participants' expectations for their romantic partners' positive regard of them were confirmed (validated) or violated, in either positive or negative directions. Primary analyses were conducted using predefined regions of interest, the locations of which were taken from previously published research. Results indicate that activity for mid-brain and striatal reward system regions of interest was modulated by social reward expectation violation in ways consistent with prior research on reward prediction-error. Additionally, activity in the striatum during viewing of disconfirmatory information was associated with both increases in post-scan reports of attachment anxiety and decreases in post-scan trust, a finding that follows directly from representational models of attachment and trust.
reward system; prediction-error; social reward; attachment; love; striatum; trust; fMRI
Inhibitory control allows for the regulation of thought and action, and interacts with motivational variables, such as reward, to modify behavior adaptively as environments change. We examined the effects of reward on two distinct forms of inhibitory control, cancellation and restraint. Typically developing children and adolescents completed two versions of the stop signal task (cancellation and restraint) under three reward conditions (neutral, low reward, and high reward), where rewards were earned for successful inhibitory control. Rewards improved both cancellation and restraint inhibition, with similar effects of reward on each form of inhibitory control. Rewards did not alter the speed of response execution in either task, suggesting that rewards specifically altered inhibition processes without influencing processes related to response execution. Adolescents were faster and less variable than children when executing and inhibiting their responses. There were similar developmental effects of reward on the speed of inhibitory control, but group differences were found in terms of accuracy of inhibition in the restraint task. These results clarify how reward modulates two different forms of regulatory behavior in children and adolescents.
Inhibition; reward; cancellation; restraint; development
Dysfunctional social reward and social attention are present in a variety of neuropsychiatric disorders including autism, schizophrenia, and social anxiety. Here we show that similar social reward and attention dysfunction are present in anorexia nervosa (AN), a disorder defined by avoidance of food and extreme weight loss. We measured the implicit reward value of social stimuli for female participants with (n = 11) and without (n = 11) AN using an econometric choice task and also tracked gaze patterns during free viewing of images of female faces and bodies. As predicted, the reward value of viewing bodies varied inversely with observed body weight for women with anorexia but not control women, in contrast with their explicit ratings of attractiveness. Surprisingly, women with AN, unlike control women, did not find female faces rewarding and avoided looking at both the face and eyes – independent of observed body weight. These findings suggest comorbid dysfunction in the neural circuits mediating gustatory and social reward in anorexia nervosa.
eating disorders; social; bulimia
Primary sensory cortices have been assumed to serve as stimulus analyzers while cognitive functions such as learning and memory have been allocated to “higher” cortical areas. However, the primary auditory cortex (A1) is now known to encode the acquired significance of sound as indicated by associatively-induced specific shifts of tuning to the frequencies of conditioned stimuli (CS) and gains in area of CS representations. Rewarding brain stimulation can be a very powerful motivator and brain reward systems have been implicated in addictive behavior. Therefore, it is possible that a cue for brain reward will gain cortical territory and perhaps thereby increase its control of subsequent behavior. To investigate the effect of brain reward on cortical organization, adult male rats (n = 11) were first tested with varying amounts of stimulation of the ventral tegmental area (VTAstm) to generate sigmoidal psychometric functions of nose poke (NP) rates as a function of reward magnitude (duration). Next, we attempted to accomplish tone control of NPs by maintaining intertrial NPs using a low reward duration and presenting a 20 s tone (2.0 kHz, 70 dB) which signaled an increase in reward to a high magnitude 10 s after tone onset. Tone control was demonstrated by a significant increase in the rate of NPs during the first 10 s of tone presentation, which anticipated the delivery of the high magnitude of reward. Tone control was achieved in seven of 11 subjects. This was accompanied by a highly specific and significant gain in representational area, specifically for the half-octave range centered on the CS frequency. However, this plasticity developed only in tone-controlled (TC) animals. The auditory cortex of non-tone-controlled subjects (n = 4) did not differ from that of naïve controls (n = 9) although their VTAstm was as rewarding as for the TC group. These findings reveal that auditory instrumental behavior can be controlled by rewarding VTAstm and that such control appears necessary for the highly specific recruitment of cortical cells to increase the representation of a sound that acquires behavioral importance.
Association; Frequency; Plasticity; Tonotopic map; Ventral tegmental area
This study used eye-tracking to examine how 20-month old toddlers with autism spectrum disorder (ASD) (N=28), typical development (TD) (N=34), and non-autistic developmental delays (DD) (N=16) monitored the activities occurring in a context of an adult-child play interaction. Toddlers with ASD, in comparison to control groups, showed less attention to the activities of others and focused more on background objects (e.g. toys). In addition, while all groups spent the same time overall looking at people, toddlers with ASD looked less at people's heads and more at their bodies. In ASD, these patterns were associated with cognitive deficits and greater autism severity. These results suggest that the monitoring of the social activities of others is disrupted early in the developmental progression of autism, limiting future avenues for observational learning.
activity monitoring; autism; eye-tracking; joint attention; social learning; observational learning
Individuals with autism spectrum disorders (ASD) tend to make inadequate social judgments, particularly when the nonverbal and verbal emotional expressions of other people are incongruent. Although previous behavioral studies have suggested that ASD individuals have difficulty in using nonverbal cues when presented with incongruent verbal-nonverbal information, the neural mechanisms underlying this symptom of ASD remain unclear. In the present functional magnetic resonance imaging study, we compared brain activity in 15 non-medicated adult males with high-functioning ASD to that of 17 age-, parental-background-, socioeconomic-, and intelligence-quotient-matched typically-developed (TD) male participants. Brain activity was measured while each participant made friend or foe judgments of realistic movies in which professional actors spoke with conflicting nonverbal facial expressions and voice prosody. We found that the ASD group made significantly less judgments primarily based on the nonverbal information than the TD group, and they exhibited significantly less brain activity in the right inferior frontal gyrus, bilateral anterior insula, anterior cingulate cortex/ventral medial prefrontal cortex (ACC/vmPFC), and dorsal medial prefrontal cortex (dmPFC) than the TD group. Among these five regions, the ACC/vmPFC and dmPFC were most involved in nonverbal-information-biased judgments in the TD group. Furthermore, the degree of decrease of the brain activity in these two brain regions predicted the severity of autistic communication deficits. The findings indicate that diminished activity in the ACC/vmPFC and dmPFC underlies the impaired abilities of individuals with ASD to use nonverbal content when making judgments regarding other people based on incongruent social information.