A comparative fMRI meta-analysis of altruistic and strategic decisions to give

The decision to share resources is fundamental for cohesive societies. Humans can be motivated to give for many reasons. Some generosity incurs a definite cost, with no extrinsic reward to the act, but instead provides intrinsic satisfaction (labelled here as 'altruistic' giving). Other giving behaviours are done with the prospect of improving one's own situation via reciprocity, reputation, or public good (labelled here as 'strategic' giving). These contexts differ in the source, certainty, and timing of rewards as well as the inferences made about others' mental states. We executed a combined statistical map and coordinate-based fMRI meta-analysis of decisions to give (36 studies, 1150 participants). Methods included a novel approach for accommodating variable signal dropout between studies in meta-analysis. Results reveal consistent, cross-paradigm neural correlates of each decision type, commonalities, and informative differences. Relative to being selfish, altruistic and strategic giving activate overlapping reward networks. However, strategic decisions showed greater activity in striatal regions than altruistic choices. Altruistic giving, more than strategic, activated subgenual anterior cingulate cortex (sgACC). Ventromedial prefrontal cortex (vmPFC) is consistently involved during generous decisions and processing across a posterior to anterior axis differentiates the altruistic/strategic context. Posterior vmPFC was preferentially recruited during altruistic decisions. Regions of the 'social brain' showed distinct patterns of activity between choice types, reflecting the different use of theory of mind in the two contexts. We provide the consistent neural correlates of decisions to give, and show that many will depend on the source of incentives

Independent neural computation of value from other people's confidence

Expectation of reward can be shaped by the observation of actions and expressions of other people in one's environment. A person's apparent confidence in the likely reward of an action, for instance, makes qualities of their evidence, not observed directly, socially accessible. This strategy is computationally distinguished from associative learning methods that rely on direct observation, by its use of inference from indirect evidence. In twenty-three healthy human subjects, we isolated effects of first-hand experience, other people's choices, and the mediating effect of their confidence, on decision-making and neural correlates of value within ventromedial prefrontal cortex (vmPFC). Value derived from first hand experience and other people's choices (regardless of confidence) were indiscriminately represented across vmPFC. However, value computed from agent choices weighted by their associated confidence was represented with specificity for ventromedial area 10. This pattern corresponds to shifts of connectivity and overlapping cognitive processes along a posterior-anterior vmPFC axis. Task behavior and self-reported self-reliance for decision-making in other social contexts correlated. The tendency to conform in other social contexts corresponded to increased activation in cortical regions previously shown to respond to social conflict in proportion to subsequent conformity (Campbell-Meiklejohn et al., 2010). The tendency to self-monitor predicted a selectively enhanced response to accordance with others in the right temporoparietal junction (rTPJ). The findings anatomically decompose vmPFC value representations according to computational requirements and provide biological insight into the social transmission of preference and reassurance gained from the confidence of others. Significance Statement: Decades of research have provided evidence that the ventromedial prefrontal cortex (vmPFC) signals the satisfaction we expect from imminent actions. However, we have a surprisingly modest understanding of the organization of value across this substantial and varied region. This study finds that using cues of the reliability of other peoples'; knowledge to enhance expectation of personal success generates value correlates that are anatomically distinct from those concurrently computed from direct, personal experience. This suggests that representation of decision values in vmPFC is suborganized according to the underlying computation, consistent with what we know about the anatomical heterogeneity of the region. These results also provide insight into the observational learning process by which someone else's confidence can sway and reassure our choices

In for a penny, in for a pound: methylphenidate reduces the inhibitory effect of high stakes on persistent risky choice

Methylphenidate (MPH) is a stimulant that increases extracellular levels of dopamine and noradrenaline. It can diminish risky decision-making tendencies in certain clinical populations. MPH is also used, without license, by healthy adults, but the impact on their decision-making is not well established. Previous work has found that dopamine receptor activity of healthy adults can modulate the influence of stake magnitude on decisions to persistently gamble after incurring a loss. In this study, we tested for modulation of this effect by MPH in 40 healthy human adults. In a double-blind experiment, 20 subjects received 20 mg of MPH, while 20 matched controls received a placebo. All were provided with 30 rounds of opportunities to accept an incurred loss from their assets or opt for a "double-or-nothing" gamble that would either avoid or double it. Rounds began with a variable loss that would double with every failed gamble until it was accepted, recovered, or reached a specified maximum. Probability of recovery on any gamble was low and ambiguous. Subjects receiving placebo gambled less as the magnitude of the stake was raised and as the magnitude of accumulated loss escalated over the course of the task. In contrast, subjects treated with MPH gambled at a consistent rate, well above chance, across all stakes and trials. Trait reward responsiveness also reduced the impact of high stakes. The findings suggest that elevated catecholamine activity by MPH can disrupt inhibitory influences on persistent risky choice in healthy adults

Amygdala structure and the tendency to perceive the social system as legitimate and desirable

Individual variation in preferences to maintain vs. change the societal status quo can play out in the political realm by choosing leaders and policies that reinforce or undermine existing inequalities. We sought to understand which individuals are likely to defend or challenge inequality in society by exploring the neuroanatomical substrates of system justification tendencies. In two independent neuroimaging studies, we observed that larger bilateral amygdala volume was positively correlated with the tendency to believe that the existing social order was legitimate and desirable. These results held for members of advantaged and disadvantaged groups (men and women). Furthermore, individuals with larger amygdala volume were less likely to participate in subsequent protest movements. We ruled out alternative explanations in terms of attitudinal extremity and political orientation per se. Exploratory whole brain analyses suggested that system justification effects may extend to structures adjacent to the amygdala, including parts of the insula and orbitofrontal cortex. These findings suggest that the amygdala may provide a neural substrate for maintaining the status quo, and opens avenues for further investigation linking system justification and other neuroanatomical regions

Hungry for compliments? Ghrelin is not associated with neural responses to social rewards or their pleasantness

The stomach-derived hormone ghrelin motivates food search and stimulates food consumption, with highest plasma concentrations before a meal and lowest shortly after. However, ghrelin also appears to affect the value of non-food rewards such as interaction with rat conspecifics, and monetary rewards in humans. The present pre-registered study investigated how nutritional state and ghrelin concentrations are related to the subjective and neural responses to social and non-social rewards. In a cross-over feed-and-fast design, 67 healthy volunteers (20 women) underwent functional magnetic resonance imaging (fMRI) in a hungry state and after a meal with repeated plasma ghrelin measurements. In task 1, participants received social rewards in the form of approving expert feedback, or non-social computer reward. In task 2, participants rated the pleasantness of compliments and neutral statements. Nutritional state and ghrelin concentrations did not affect the response to social reward in task 1. In contrast, ventromedial prefrontal cortical activation to non-social rewards was reduced when the meal strongly suppressed ghrelin. In task 2, fasting increased activation in the right ventral striatum during all statements, but ghrelin concentrations were neither associated with brain activation nor with experienced pleasantness. Complementary Bayesian analyses provided moderate evidence for a lack of correlation between ghrelin concentrations and behavioral and neural responses to social rewards, but moderate evidence for an association between ghrelin and non-social rewards. This suggests that ghrelin’s influence may be restricted to non-social rewards. Social rewards implemented via social recognition and affirmation may be too abstract and complex to be susceptible to ghrelin’s influence. In contrast, the non-social reward was associated with the expectation of a material object that was handed out after the experiment. This may indicate that ghrelin might be involved in anticipatory rather than consummatory phases of reward.publishedVersio

Enhanced automatic action imitation and intact imitation- inhibition in schizophrenia

Imitation plays a key role in social learning and in facilitating social interactions and likely constitutes a basic building block of social cognition that supports higher-level social abilities. Recent findings suggest that patients with schizophrenia have imitation impairments that could contribute to the social impairments associated with the disorder. However, extant studies have specifically assessed voluntary imitation or automatic imitation of emotional stimuli without controlling for potential confounders. The imitation impairments seen might therefore be secondary to other cognitive, motoric or emotional deficits associated with the disorder. To overcome this issue, we used an automatic imitation paradigm with nonemotional stimuli to assess automatic imitation and the top-down modulation of imitation where participants were required to lift one of two fingers according to a number shown on the screen whilst observing the same or the other finger movement. In addition, we used a control task with a visual cue in place of a moving finger, to isolate the effect of observing finger movement from other visual cueing effects. Data from 33 patients (31 medicated) and 40 matched healthy controls were analyzed. Patients displayed enhanced imitation and intact top-down modulation of imitation. The enhanced imitation seen in patients may have been medication induced as larger effects were seen in patients receiving higher antipsychotic doses. In sum, we did not find an imitation impairment in schizophrenia. The results suggest that previous findings of impaired imitation in schizophrenia might have been due to other cognitive, motoric and/or emotional deficits

Hyper- and hypo-mentalizing in patients with first-episode schizophrenia: fMRI and behavioural studies

Background: Historically, research investigating neural correlates of mentalizing deficits in schizophrenia has focused on patients who have been ill for several years with lengthy exposure to medication. Little is known about the neural and behavioural presentations of theory-of-mind deficits in schizophrenia, shortly after the first episode of psychosis. Methods: We investigated social cognition in seventeen recently diagnosed first-episode schizophrenia (FES) patients with little or no exposure to antipsychotic medication and 1:1 matched healthy controls. We recorded behavioural and neural responses to the Animated Triangles Task (ATT), which is a non-verbal validated mentalizing task that measures the ascription of intentionality to the movements of objects. Results: FES patients under-interpreted social cues and over-interpreted non-social cues. These effects were influenced by current intelligence (IQ). Control group and FES neural responses replicated earlier findings in healthy adults. However, a region of anterior medial prefrontal cortex (amPFC) of FES patients showed a different response pattern to that of controls. Unlike healthy controls, patients increased activity in this social cognition region while studying ‘random’ movements of shapes, as compared to the study of movements normally interpreted as ‘intentional’. Conclusions: Mentalizing deficits in FES consists of hypo- and hyper-mentalizing. The neural pattern of FES patients is consistent with deficits in the ability to switch off mentalizing processes in potentially social contexts, instead increasing them when intentionality is not forthcoming. Overall, results demonstrate complexities of theory of mind deficits in schizophrenia that should be considered when offering social cognitive training programs

Hungry for compliments? Ghrelin is not associated with neural responses to social rewards or their pleasantness

The stomach-derived hormone ghrelin motivates food search and stimulates food consumption, with highest plasma concentrations before a meal and lowest shortly after. However, ghrelin also appears to affect the value of non-food rewards such as interaction with rat conspecifics, and monetary rewards in humans. The present pre-registered study investigated how nutritional state and ghrelin concentrations are related to the subjective and neural responses to social and non-social rewards. In a cross-over feed-and-fast design, 67 healthy volunteers (20 women) underwent functional magnetic resonance imaging (fMRI) in a hungry state and after a meal with repeated plasma ghrelin measurements. In task 1, participants received social rewards in the form of approving expert feedback, or non-social computer reward. In task 2, participants rated the pleasantness of compliments and neutral statements. Nutritional state and ghrelin concentrations did not affect the response to social reward in task 1. In contrast, ventromedial prefrontal cortical activation to non-social rewards was reduced when the meal strongly suppressed ghrelin. In task 2, fasting increased activation in the right ventral striatum during all statements, but ghrelin concentrations were neither associated with brain activation nor with experienced pleasantness. Complementary Bayesian analyses provided moderate evidence for a lack of correlation between ghrelin concentrations and behavioral and neural responses to social rewards, but moderate evidence for an association between ghrelin and non-social rewards. This suggests that ghrelin’s influence may be restricted to non-social rewards. Social rewards implemented via social recognition and affirmation may be too abstract and complex to be susceptible to ghrelin’s influence. In contrast, the non-social reward was associated with the expectation of a material object that was handed out after the experiment. This may indicate that ghrelin might be involved in anticipatory rather than consummatory phases of reward

Selective effects of serotonin on choices to gather more information

Background: Gathering and evaluating information leads to better decisions, but often at cost. The balance between information seeking and exploitation features in neurodevelopmental, mood, psychotic and substance-related disorders. Serotonin’s role has been highlighted by experimental reduction of its precursor, tryptophan. Aims: We tested the boundaries and applicability of this role by asking whether changes to information sampling would be observed following acute doses of serotonergic and catecholaminergic clinical treatments. We used a variant of the Information Sampling Task (IST) to measure how much information a person requires before they make a decision. This task allows participants to sample information until satisfied to make a choice. Methods: In separate double-blind placebo-controlled experiments, we tested 27 healthy participants on/off 20 mg of the serotonin reuptake inhibitor (SRI) citalopram, and 22 participants on/off 40 mg of the noradrenergic reuptake inhibitor atomoxetine. The IST variant minimised effects of temporal impulsivity and loss aversion. Analyses used a variety of participant prior expectations of sampling spaces in the IST, including a new prior that accounts for learning of likely states across trials. We analysed behaviour by a new method that also accounts for baseline individual differences of risk preference. Results: Baseline preferences demonstrated risk aversion. Citalopram decreased the expected utility of choices and probability of being correct based on informational content of samples collected, suggesting participants collected less useful information before making a choice. Atomoxetine did not influence information seeking. Conclusion: Acute changes of serotonin activity by way of a single SRI dose alter information-seeking behaviour

A single oral dose of citalopram increases interoceptive insight in healthy volunteers

Rationale Interoception is the signalling, perception, and interpretation of internal physiological states. Many mental disorders associated with changes of interoception, including depressive and anxiety disorders, are treated with selective serotonin reuptake inhibitors (SSRIs). However, the causative link between SSRIs and interoception is not yet clear. Objectives To ascertain the causal effect of acute changes of serotonin levels on cardiac interoception. Methods Using a within-participant placebo-controlled design, forty-seven healthy human volunteers (31 female, 16 male) were tested on and off a 20 mg oral dose of the commonly prescribed SSRI, citalopram. Participants made judgements on the synchrony between their heartbeat and auditory tones and then expressed confidence in each judgement. We measured three types of interoceptive cognition. Results Citalopram increased cardiac interoceptive insight, measured as correspondence of self-reported confidence to the likelihood that interoceptive judgements were actually correct. This effect was driven by enhanced confidence for correct interoceptive judgements and was independent of measured cardiac and reported subjective effects of the drug. Conclusions An acute change of serotonin levels can increase insight into the reliability of inferences made from cardiac interoceptive sensations