Beta and theta oscillations track effort and previous reward in the human basal ganglia and prefrontal cortex during decision making.

Choosing whether to exert effort to obtain rewards is fundamental to human motivated behavior. However, the neural dynamics underlying the evaluation of reward and effort in humans is poorly understood. Here, we report an exploratory investigation into this with chronic intracranial recordings from the prefrontal cortex (PFC) and basal ganglia (BG; subthalamic nuclei and globus pallidus) in people with Parkinson's disease performing a decision-making task with offers that varied in levels of reward and physical effort required. This revealed dissociable neural signatures of reward and effort, with BG beta (12 to 20 Hz) oscillations tracking effort on a single-trial basis and PFC theta (4 to 7 Hz) signaling previous trial reward, with no effects of net subjective value. Stimulation of PFC increased overall acceptance of offers and sensitivity to reward while decreasing the impact of effort on choices. This work uncovers oscillatory mechanisms that guide fundamental decisions to exert effort for reward across BG and PFC, supports a causal role of PFC for such choices, and seeds hypotheses for future studies.

Neural representations of vicarious rewards are linked to interoception and prosocial behaviour.

Every day we constantly observe other people receiving rewards. Theoretical accounts posit that vicarious reward processing might be linked to people's sensitivity to internal body states (interoception) and facilitates a tendency to act prosocially. However, the neural processes underlying the links between vicarious reward processing, interoception, and prosocial behaviour are poorly understood. Previous research has linked vicarious reward processing to the anterior cingulate gyrus (ACCg) and the anterior insula (AI). Can we predict someone's propensity to be prosocial or to be aware of interoceptive signals from variability in how the ACCg and AI process rewards? Here, participants monitored rewards being delivered to themselves or a stranger during functional magnetic resonance imaging. Later, they performed a task measuring their willingness to exert effort to obtain rewards for others, and a task measuring their propensity to be aware and use interoceptive respiratory signals. Using multivariate similarity analysis, we show that people's willingness to be prosocial is predicted by greater similarity between self and other representations in the ACCg. Moreover, greater dissimilarity in self-other representations in the AI is linked to interoceptive propensity. These findings highlight that vicarious reward is linked to bodily signals in AI, and foster prosocial tendencies through the ACCg.

Anterior cingulate cortex: A brain system necessary for learning to reward others?

Helping a friend move house, donating to charity, volunteering assistance during a crisis. Humans and other species alike regularly undertake prosocial behaviors-actions that benefit others without necessarily helping ourselves. But how does the brain learn what acts are prosocial? Basile and colleagues show that removal of the anterior cingulate cortex (ACC) prevents monkeys from learning what actions are prosocial but does not stop them carrying out previously learned prosocial behaviors. This highlights that the ability to learn what actions are prosocial and choosing to perform helpful acts may be distinct cognitive processes, with only the former depending on ACC.

Neural and Cognitive Signatures of Guilt Predict Hypocritical Blame.

A common form of moral hypocrisy occurs when people blame others for moral violations that they themselves commit. It is assumed that hypocritical blamers act in this manner to falsely signal that they hold moral standards that they do not really accept. We tested this assumption by investigating the neurocognitive processes of hypocritical blamers during moral decision-making. Participants (62 adult UK residents; 27 males) underwent functional MRI scanning while deciding whether to profit by inflicting pain on others and then judged the blameworthiness of others' identical decisions. Observers (188 adult U.S. residents; 125 males) judged participants who blamed others for making the same harmful choice to be hypocritical, immoral, and untrustworthy. However, analyzing hypocritical blamers' behaviors and neural responses shows that hypocritical blame was positively correlated with conflicted feelings, neural responses to moral standards, and guilt-related neural responses. These findings demonstrate that hypocritical blamers may hold the moral standards that they apply to others.

Dopamine Modulates Dynamic Decision-Making during Foraging.

The mesolimbic dopaminergic system exerts a crucial influence on incentive processing. However, the contribution of dopamine in dynamic, ecological situations where reward rates vary, and decisions evolve over time, remains unclear. In such circumstances, current (foreground) reward accrual needs to be compared continuously with potential rewards that could be obtained by traveling elsewhere (background reward rate), to determine the opportunity cost of staying versus leaving. We hypothesized that dopamine specifically modulates the influence of background, but not foreground, reward information when making a dynamic comparison of these variables for optimal behavior. On a novel foraging task based on an ecological account of animal behavior (marginal value theorem), human participants of either sex decided when to leave locations in situations where foreground rewards depleted at different rates, either in rich or poor environments with high or low background reward rates. In line with theoretical accounts, people's decisions to move from current locations were independently modulated by changes in both foreground and background reward rates. Pharmacological manipulation of dopamine D2 receptor activity using the agonist cabergoline significantly affected decisions to move on, specifically modulating the effect of background reward rates. In particular, when on cabergoline, people left patches in poor environments much earlier. These results demonstrate a role of dopamine in signaling the opportunity cost of rewards, not value per se. Using this ecologically derived framework, we uncover a specific mechanism by which D2 dopamine receptor activity modulates decision-making when foreground and background reward rates are dynamically compared.SIGNIFICANCE STATEMENT Many decisions, across economic, political, and social spheres, involve choices to "leave". Such decisions depend on a continuous comparison of a current location's value, with that of other locations you could move on to. However, how the brain makes such decisions is poorly understood. Here, we developed a computerized task, based around theories of how animals make decisions to move on when foraging for food. Healthy human participants had to decide when to leave collecting financial rewards in a location, and travel to collect rewards elsewhere. Using a pharmacological manipulation, we show that the activity of dopamine in the brain modulates decisions to move on, with people valuing other locations differently depending on their dopaminergic state.

Aging Increases Prosocial Motivation for Effort.

Social cohesion relies on prosociality in increasingly aging populations. Helping other people requires effort, yet how willing people are to exert effort to benefit themselves and others, and whether such behaviors shift across the life span, is poorly understood. Using computational modeling, we tested the willingness of 95 younger adults (18-36 years old) and 92 older adults (55-84 years old) to put physical effort into self- and other-benefiting acts. Participants chose whether to work and exert force (30%-70% of maximum grip strength) for rewards (2-10 credits) accrued for themselves or, prosocially, for another. Younger adults were somewhat selfish, choosing to work more at higher effort levels for themselves, and exerted less force in prosocial work. Strikingly, compared with younger adults, older people were more willing to put in effort for others and exerted equal force for themselves and others. Increased prosociality in older people has important implications for human behavior and societal structure.

Neurocomputational mechanisms of prosocial learning and links to empathy.

Reinforcement learning theory powerfully characterizes how we learn to benefit ourselves. In this theory, prediction errors-the difference between a predicted and actual outcome of a choice-drive learning. However, we do not operate in a social vacuum. To behave prosocially we must learn the consequences of our actions for other people. Empathy, the ability to vicariously experience and understand the affect of others, is hypothesized to be a critical facilitator of prosocial behaviors, but the link between empathy and prosocial behavior is still unclear. During functional magnetic resonance imaging (fMRI) participants chose between different stimuli that were probabilistically associated with rewards for themselves (self), another person (prosocial), or no one (control). Using computational modeling, we show that people can learn to obtain rewards for others but do so more slowly than when learning to obtain rewards for themselves. fMRI revealed that activity in a posterior portion of the subgenual anterior cingulate cortex/basal forebrain (sgACC) drives learning only when we are acting in a prosocial context and signals a prosocial prediction error conforming to classical principles of reinforcement learning theory. However, there is also substantial variability in the neural and behavioral efficiency of prosocial learning, which is predicted by trait empathy. More empathic people learn more quickly when benefitting others, and their sgACC response is the most selective for prosocial learning. We thus reveal a computational mechanism driving prosocial learning in humans. This framework could provide insights into atypical prosocial behavior in those with disorders of social cognition.

Disrupted prediction errors index social deficits in autism spectrum disorder.

Social deficits are a core symptom of autism spectrum disorder; however, the perturbed neural mechanisms underpinning these deficits remain unclear. It has been suggested that social prediction errors-coding discrepancies between the predicted and actual outcome of another's decisions-might play a crucial role in processing social information. While the gyral surface of the anterior cingulate cortex signalled social prediction errors in typically developing individuals, this crucial social signal was altered in individuals with autism spectrum disorder. Importantly, the degree to which social prediction error signalling was aberrant correlated with diagnostic measures of social deficits. Effective connectivity analyses further revealed that, in typically developing individuals but not in autism spectrum disorder, the magnitude of social prediction errors was driven by input from the ventromedial prefrontal cortex. These data provide a novel insight into the neural substrates underlying autism spectrum disorder social symptom severity, and further research into the gyral surface of the anterior cingulate cortex and ventromedial prefrontal cortex could provide more targeted therapies to help ameliorate social deficits in autism spectrum disorder.

Vicarious reinforcement learning signals when instructing others.

Reinforcement learning (RL) theory posits that learning is driven by discrepancies between the predicted and actual outcomes of actions (prediction errors [PEs]). In social environments, learning is often guided by similar RL mechanisms. For example, teachers monitor the actions of students and provide feedback to them. This feedback evokes PEs in students that guide their learning. We report the first study that investigates the neural mechanisms that underpin RL signals in the brain of a teacher. Neurons in the anterior cingulate cortex (ACC) signal PEs when learning from the outcomes of one's own actions but also signal information when outcomes are received by others. Does a teacher's ACC signal PEs when monitoring a student's learning? Using fMRI, we studied brain activity in human subjects (teachers) as they taught a confederate (student) action-outcome associations by providing positive or negative feedback. We examined activity time-locked to the students' responses, when teachers infer student predictions and know actual outcomes. We fitted a RL-based computational model to the behavior of the student to characterize their learning, and examined whether a teacher's ACC signals when a student's predictions are wrong. In line with our hypothesis, activity in the teacher's ACC covaried with the PE values in the model. Additionally, activity in the teacher's insula and ventromedial prefrontal cortex covaried with the predicted value according to the student. Our findings highlight that the ACC signals PEs vicariously for others' erroneous predictions, when monitoring and instructing their learning. These results suggest that RL mechanisms, processed vicariously, may underpin and facilitate teaching behaviors.

Encoding of Vicarious Reward Prediction in Anterior Cingulate Cortex and Relationship with Trait Empathy.

Empathy--the capacity to understand and resonate with the experiences of others--can depend on the ability to predict when others are likely to receive rewards. However, although a plethora of research has examined the neural basis of predictions about the likelihood of receiving rewards ourselves, very little is known about the mechanisms that underpin variability in vicarious reward prediction. Human neuroimaging and nonhuman primate studies suggest that a subregion of the anterior cingulate cortex in the gyrus (ACCg) is engaged when others receive rewards. Does the ACCg show specialization for processing predictions about others' rewards and not one's own and does this specialization vary with empathic abilities? We examined hemodynamic responses in the human brain time-locked to cues that were predictive of a high or low probability of a reward either for the subject themselves or another person. We found that the ACCg robustly signaled the likelihood of a reward being delivered to another. In addition, ACCg response significantly covaried with trait emotion contagion, a necessary foundation for empathizing with other individuals. In individuals high in emotion contagion, the ACCg was specialized for processing others' rewards exclusively, but for those low in emotion contagion, this region also responded to information about the subject's own rewards. Our results are the first to show that the ACCg signals probabilistic predictions about rewards for other people and that the substantial individual variability in the degree to which the ACCg is specialized for processing others' rewards is related to trait empathy. SIGNIFICANCE STATEMENT: Successfully cooperating, competing, or empathizing with others can depend on our ability to predict when others are going to get something rewarding. Although many studies have examined how the brain processes rewards we will get ourselves, very little is known about vicarious reward processing. Here, we show that a subregion of the anterior cingulate cortex in the gyrus (ACCg) shows a degree of specialization for processing others' versus one's own rewards. However, the degree to which the ACCg is specialized varies with people's ability to empathize with others. This new insight into how vicarious rewards are processed in the brain and vary with empathy may be key for understanding disorders of social behavior, including psychopathy and autism.

Plasticity in unimodal and multimodal brain areas reflects multisensory changes in self-face identification.

Nothing provides as strong a sense of self as seeing one's face. Nevertheless, it remains unknown how the brain processes the sense of self during the multisensory experience of looking at one's face in a mirror. Synchronized visuo-tactile stimulation on one's own and another's face, an experience that is akin to looking in the mirror but seeing another's face, causes the illusory experience of ownership over the other person's face and changes in self-recognition. Here, we investigate the neural correlates of this enfacement illusion using fMRI. We examine activity in the human brain as participants experience tactile stimulation delivered to their face, while observing either temporally synchronous or asynchronous tactile stimulation delivered to another's face on either a specularly congruent or incongruent location. Activity in the multisensory right temporo-parietal junction, intraparietal sulcus, and the unimodal inferior occipital gyrus showed an interaction between the synchronicity and the congruency of the stimulation and varied with the self-reported strength of the illusory experience, which was recorded after each stimulation block. Our results highlight the important interplay between unimodal and multimodal information processing for self-face recognition, and elucidate the neurobiological basis for the plasticity required for identifying with our continuously changing visual appearance.

The anterior cingulate gyrus signals the net value of others' rewards.

Evaluating the costs and benefits of our own choices is central to most forms of decision-making and its mechanisms in the brain are becoming increasingly well understood. To interact successfully in social environments, it is also essential to monitor the rewards that others receive. Previous studies in nonhuman primates have found neurons in the anterior cingulate cortex (ACC) that signal the net value (benefit minus cost) of rewards that will be received oneself and also neurons that signal when a reward will be received by someone else. However, little is understood about the way in which the human brain engages in cost-benefit analyses during social interactions. Does the ACC signal the net value (the benefits minus the costs) of rewards that others will receive? Here, using fMRI, we examined activity time locked to cues that signaled the anticipated reward magnitude (benefit) to be gained and the level of effort (cost) to be incurred either by a subject themselves or by a social confederate. We investigated whether activity in the ACC covaries with the net value of rewards that someone else will receive when that person is required to exert effort for the reward. We show that, although activation in the sulcus of the ACC signaled the costs on all trials, gyral ACC (ACC(g)) activity varied parametrically only with the net value of rewards gained by others. These results suggest that the ACC(g) plays an important role in signaling cost-benefit information by signaling the value of others' rewards during social interactions.

Social environment-based opportunity costs dictate when people leave social interactions.

There is an ever-increasing understanding of the cognitive mechanisms underlying how we process others' behaviours during social interactions. However, little is known about how people decide when to leave an interaction. Are these decisions shaped by alternatives in the environment - the opportunity-costs of connecting to other people? Here, participants chose when to leave partners who treated them with varying degrees of fairness, and connect to others, in social environments with different opportunity-costs. Across four studies we find people leave partners more quickly when opportunity-costs are high, both the average fairness of people in the environment and the effort required to connect to another partner. People's leaving times were accounted for by a fairness-adapted evidence accumulation model, and modulated by depression and loneliness scores. These findings demonstrate the computational processes underlying decisions to leave, and highlight atypical social time allocations as a marker of poor mental health.

Functional Magnetic Resonance Spectroscopy of Prolonged Motor Activation using Conventional and Spectral GLM Analyses.

Background: Functional MRS (fMRS) is a technique used to measure metabolic changes in response to increased neuronal activity, providing unique insights into neurotransmitter dynamics and neuroenergetics. In this study we investigate the response of lactate and glutamate levels in the motor cortex during a sustained motor task using conventional spectral fitting and explore the use of a novel analysis approach based on the application of linear modelling directly to the spectro-temporal fMRS data. Methods: fMRS data were acquired at a field strength of 3 Tesla from 23 healthy participants using a short echo-time (28ms) semi-LASER sequence. The functional task involved rhythmic hand clenching over a duration of 8 minutes and standard MRS preprocessing steps, including frequency and phase alignment, were employed. Both conventional spectral fitting and direct linear modelling were applied, and results from participant-averaged spectra and metabolite-averaged individual analyses were compared. Results: We observed a 20% increase in lactate in response to the motor task, consistent with findings at higher magnetic field strengths. However, statistical testing showed some variability between the two averaging schemes and fitting algorithms. While lactate changes were supported by the direct spectral modelling approach, smaller increases in glutamate (2%) were inconsistent. Exploratory spectral modelling identified a 4% decrease in aspartate, aligning with conventional fitting and observations from prolonged visual stimulation. Conclusion: We demonstrate that lactate dynamics in response to a prolonged motor task are observed using short-echo time semi-LASER at 3 Tesla, and that direct linear modelling of fMRS data is a useful complement to conventional analysis. Future work includes mitigating spectral confounds, such as scalp lipid contamination and lineshape drift, and further validation of our novel direct linear modelling approach through experimental and simulated datasets.

Human ventromedial prefrontal cortex is necessary for prosocial motivation.

Ventromedial prefrontal cortex (vmPFC) is vital for decision-making. Functional neuroimaging links vmPFC to processing rewards and effort, while parallel work suggests vmPFC involvement in prosocial behaviour. However, the necessity of vmPFC for these functions is unknown. Patients with rare focal vmPFC lesions (n = 25), patients with lesions elsewhere (n = 15) and healthy controls (n = 40) chose between rest and exerting effort to earn rewards for themselves or another person. vmPFC damage decreased prosociality across behavioural and computational measures. vmPFC patients earned less, discounted rewards by effort more, and exerted less force when another person benefited, compared to both control groups. Voxel-based lesion mapping revealed dissociations between vmPFC subregions. While medial damage led to antisocial behaviour, lateral damage increased prosocial behaviour relative to patients with damage elsewhere. vmPFC patients also showed reduced effort sensitivity overall, but reward sensitivity was limited to specific subregions. These results reveal multiple causal contributions of vmPFC to prosocial behaviour, effort and reward.

Acute stress reduces effortful prosocial behaviour.

Acute stress can change our cognition and emotions, but what specific consequences this has for human prosocial behaviour is unclear. Previous studies have mainly investigated prosociality with financial transfers in economic games and produced conflicting results. Yet a core feature of many types of prosocial behaviour is that they are effortful. We therefore examined how acute stress changes our willingness to exert effort that benefits others. Healthy male participants - half of whom were put under acute stress - made decisions whether to exert physical effort to gain money for themselves or another person. With this design, we could independently assess the effects of acute stress on prosocial, compared to self-benefitting, effortful behaviour. Compared to controls (n = 45), participants in the stress group (n = 46) chose to exert effort more often for self- than for other-benefitting rewards at a low level of effort. Additionally, the adverse effects of stress on prosocial effort were particularly pronounced in more selfish participants. Neuroimaging combined with computational modelling revealed a putative neural mechanism underlying these effects: more stressed participants showed increased activation to subjective value in the dorsal anterior cingulate cortex and anterior insula when they themselves could benefit from their exerted effort relative to when someone else could. By using an effort-based task that better approximates real-life prosocial behaviour and incorporating trait differences in prosocial tendencies, our study provides important insights into how acute stress affects prosociality and its associated neural mechanisms.

Addressing climate change with behavioral science: A global intervention tournament in 63 countries.

Effectively reducing climate change requires marked, global behavior change. However, it is unclear which strategies are most likely to motivate people to change their climate beliefs and behaviors. Here, we tested 11 expert-crowdsourced interventions on four climate mitigation outcomes: beliefs, policy support, information sharing intention, and an effortful tree-planting behavioral task. Across 59,440 participants from 63 countries, the interventions' effectiveness was small, largely limited to nonclimate skeptics, and differed across outcomes: Beliefs were strengthened mostly by decreasing psychological distance (by 2.3%), policy support by writing a letter to a future-generation member (2.6%), information sharing by negative emotion induction (12.1%), and no intervention increased the more effortful behavior-several interventions even reduced tree planting. Last, the effects of each intervention differed depending on people's initial climate beliefs. These findings suggest that the impact of behavioral climate interventions varies across audiences and target behaviors.

Computational mechanisms underlying the dynamics of physical and cognitive fatigue.

The willingness to exert effort for reward is essential but comes at the cost of fatigue. Theories suggest fatigue increases after both physical and cognitive exertion, subsequently reducing the motivation to exert effort. Yet a mechanistic understanding of how this happens on a moment-to-moment basis, and whether mechanisms are common to both mental and physical effort, is lacking. In two studies, participants reported momentary (trial-by-trial) ratings of fatigue during an effort-based decision-making task requiring either physical (grip-force) or cognitive (mental arithmetic) effort. Using a novel computational model, we show that fatigue fluctuates from trial-to-trial as a function of exerted effort and predicts subsequent choices. This mechanism was shared across the domains. Selective to the cognitive domain, committing errors also induced momentary increases in feelings of fatigue. These findings provide insight into the computations underlying the influence of effortful exertion on fatigue and motivation, in both physical and cognitive domains.

The different faces of one's self: an fMRI study into the recognition of current and past self-facial appearances.

Mirror self-recognition is often considered as an index of self-awareness. Neuroimaging studies have identified a neural circuit specialised for the recognition of one's own current facial appearance. However, faces change considerably over a lifespan, highlighting the necessity for representations of one's face to continually be updated. We used fMRI to investigate the different neural circuits involved in the recognition of the childhood and current, adult, faces of one's self. Participants viewed images of either their own face as it currently looks morphed with the face of a familiar other or their childhood face morphed with the childhood face of the familiar other. Activity in areas which have a generalised selectivity for faces, including the inferior occipital gyrus, the superior parietal lobule and the inferior temporal gyrus, varied with the amount of current self in an image. Activity in areas involved in memory encoding and retrieval, including the hippocampus and the posterior cingulate gyrus, and areas involved in creating a sense of body ownership, including the temporo-parietal junction and the inferior parietal lobule, varied with the amount of childhood self in an image. We suggest that the recognition of one's own past or present face is underpinned by different cognitive processes in distinct neural circuits. Current self-recognition engages areas involved in perceptual face processing, whereas childhood self-recognition recruits networks involved in body ownership and memory processing.