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.

Occipital transcranial direct current stimulation in episodic migraine patients: effect on cerebral perfusion.

Cerebral blood flow differs between migraine patients and healthy controls during attack and the interictal period. This study compares the brain perfusion of episodic migraine patients and healthy controls and investigates the influence of anodal transcranial direct current stimulation (tDCS) over the occipital cortex. We included healthy adult controls and episodic migraineurs. After a 28-day baseline period and the baseline visit, migraine patients received daily active or sham anodal tDCS over the occipital lobe for 28 days. All participants underwent a MRI scan at baseline; migraineurs were also scanned shortly after the stimulation period and about five months later. At baseline, brain perfusion of migraine patients and controls differed in several areas; among the stimulated areas, perfusion was increased in the cuneus of healthy controls. At the first visit, the active tDCS group had an increased blood flow in regions processing visual stimuli and a decreased perfusion in other areas. Perfusion did not differ at the second follow-up visit. The lower perfusion level in migraineurs in the cuneus indicates a lower preactivation level. Anodal tDCS over the occipital cortex increases perfusion of several areas shortly after the stimulation period, but not 5 months later. An increase in the cortical preactivation level could mediate the transient reduction of the migraine frequency.Trial registration: NCT03237754 (registered at clincicaltrials.gov; full date of first trial registration: 03/08/2017).

Individual risk attitudes arise from noise in neurocognitive magnitude representations.

Humans are generally risk averse, preferring smaller certain over larger uncertain outcomes. Economic theories usually explain this by assuming concave utility functions. Here, we provide evidence that risk aversion can also arise from relative underestimation of larger monetary payoffs, a perceptual bias rooted in the noisy logarithmic coding of numerical magnitudes. We confirmed this with psychophysics and functional magnetic resonance imaging, by measuring behavioural and neural acuity of magnitude representations during a magnitude perception task and relating these measures to risk attitudes during separate risky financial decisions. Computational modelling indicated that participants use similar mental magnitude representations in both tasks, with correlated precision across perceptual and risky choices. Participants with more precise magnitude representations in parietal cortex showed less variable behaviour and less risk aversion. Our results highlight that at least some individual characteristics of economic behaviour can reflect capacity limitations in perceptual processing rather than processes that assign subjective values to monetary outcomes.

A unified neural account of contextual and individual differences in altruism.

Altruism is critical for cooperation and productivity in human societies but is known to vary strongly across contexts and individuals. The origin of these differences is largely unknown, but may in principle reflect variations in different neurocognitive processes that temporally unfold during altruistic decision making (ranging from initial perceptual processing via value computations to final integrative choice mechanisms). Here, we elucidate the neural origins of individual and contextual differences in altruism by examining altruistic choices in different inequality contexts with computational modeling and electroencephalography (EEG). Our results show that across all contexts and individuals, wealth distribution choices recruit a similar late decision process evident in model-predicted evidence accumulation signals over parietal regions. Contextual and individual differences in behavior related instead to initial processing of stimulus-locked inequality-related value information in centroparietal and centrofrontal sensors, as well as to gamma-band synchronization of these value-related signals with parietal response-locked evidence-accumulation signals. Our findings suggest separable biological bases for individual and contextual differences in altruism that relate to differences in the initial processing of choice-relevant information.

Neurocomputational evidence that conflicting prosocial motives guide distributive justice.

In the history of humanity, most conflicts within and between societies have originated from perceived inequality in resource distribution. How humans achieve and maintain distributive justice has therefore been an intensely studied issue. However, most research on the corresponding psychological processes has focused on inequality aversion and has been largely agnostic of other motives that may either align or oppose this behavioral tendency. Here we provide behavioral, computational, and neuroimaging evidence that distribution decisions are guided by three distinct motives-inequality aversion, harm aversion, and rank reversal aversion-that interact with each other and can also deter individuals from pursuing equality. At the neural level, we show that these three motives are encoded by separate neural systems, compete for representation in various brain areas processing equality and harm signals, and are integrated in the striatum, which functions as a crucial hub for translating the motives to behavior. Our findings provide a comprehensive framework for understanding the cognitive and biological processes by which multiple prosocial motives are coordinated in the brain to guide redistribution behaviors. This framework enhances our understanding of the brain mechanisms underlying equality-related behavior, suggests possible neural origins of individual differences in social preferences, and provides a new pathway to understand the cognitive and neural basis of clinical disorders with impaired social functions.

Human brain anatomy reflects separable genetic and environmental components of socioeconomic status.

Socioeconomic status (SES) correlates with brain structure, a relation of interest given the long-observed relations of SES to cognitive abilities and health. Yet, major questions remain open, in particular, the pattern of causality that underlies this relation. In an unprecedently large study, here, we assess genetic and environmental contributions to SES differences in neuroanatomy. We first establish robust SES-gray matter relations across a number of brain regions, cortical and subcortical. These regional correlates are parsed into predominantly genetic factors and those potentially due to the environment. We show that genetic effects are stronger in some areas (prefrontal cortex, insula) than others. In areas showing less genetic effect (cerebellum, lateral temporal), environmental factors are likely to be influential. Our results imply a complex interplay of genetic and environmental factors that influence the SES-brain relation and may eventually provide insights relevant to policy.

Inhibiting Human Aversive Memory by Transcranial Theta-Burst Stimulation to the Primary Sensory Cortex.

BACKGROUND: Predicting adverse events from past experience is fundamental for many biological organisms. However, some individuals suffer from maladaptive memories that impair behavioral control and well-being, e.g., after psychological trauma. Inhibiting the formation and maintenance of such memories would have high clinical relevance. Previous preclinical research has focused on systemically administered pharmacological interventions, which cannot be targeted to specific neural circuits in humans. Here, we investigated the potential of noninvasive neural stimulation on the human sensory cortex in inhibiting aversive memory in a laboratory threat conditioning model. METHODS: We build on an emerging nonhuman literature suggesting that primary sensory cortices may be crucially required for threat memory formation and consolidation. Immediately before conditioning innocuous somatosensory stimuli (conditioned stimuli [CS]) to aversive electric stimulation, healthy human participants received continuous theta-burst transcranial magnetic stimulation (cTBS) to individually localized primary somatosensory cortex in either the CS-contralateral (experimental) or CS-ipsilateral (control) hemisphere. We measured fear-potentiated startle to infer threat memory retention on the next day, as well as skin conductance and pupil size during learning. RESULTS: After overnight consolidation, threat memory was attenuated in the experimental group compared with the control cTBS group. There was no evidence that this differed between simple and complex CS or that CS identification or initial learning were affected by cTBS. CONCLUSIONS: Our results suggest that cTBS to the primary sensory cortex inhibits threat memory, likely by an impact on postlearning consolidation. We propose that noninvasive targeted stimulation of the sensory cortex may provide a new avenue for interfering with aversive memories in humans.

Enhancing models of social and strategic decision making with process tracing and neural data.

Every decision we take is accompanied by a characteristic pattern of response delay, gaze position, pupil dilation, and neural activity. Nevertheless, many models of social decision making neglect the corresponding process tracing data and focus exclusively on the final choice outcome. Here, we argue that this is a mistake, as the use of process data can help to build better models of human behavior, create better experiments, and improve policy interventions. Specifically, such data allow us to unlock the "black box" of the decision process and evaluate the mechanisms underlying our social choices. Using these data, we can directly validate latent model variables, arbitrate between competing personal motives, and capture information processing strategies. These benefits are especially valuable in social science, where models must predict multi-faceted decisions that are taken in varying contexts and are based on many different types of information. This article is categorized under: Economics > Interactive Decision-Making Neuroscience > Cognition Psychology > Reasoning and Decision Making.

A causal role for the right frontal eye fields in value comparison.

Recent studies have suggested close functional links between overt visual attention and decision making. This suggests that the corresponding mechanisms may interface in brain regions known to be crucial for guiding visual attention - such as the frontal eye field (FEF). Here, we combined brain stimulation, eye tracking, and computational approaches to explore this possibility. We show that inhibitory transcranial magnetic stimulation (TMS) over the right FEF has a causal impact on decision making, reducing the effect of gaze dwell time on choice while also increasing reaction times. We computationally characterize this putative mechanism by using the attentional drift diffusion model (aDDM), which reveals that FEF inhibition reduces the relative discounting of the non-fixated option in the comparison process. Our findings establish an important causal role of the right FEF in choice, elucidate the underlying mechanism, and provide support for one of the key causal hypotheses associated with the aDDM.

Dissecting functional contributions of the social brain to strategic behavior.

Social interactions routinely lead to neural activity in a "social brain network" comprising, among other regions, the temporoparietal junction (TPJ) and the dorsomedial prefrontal cortex (dmPFC). But what is the function of these areas? Are they specialized for behavior in social contexts or do they implement computations required for dealing with any reactive process, even non-living entities? Here, we use fMRI and a game paradigm separating the need for these two aspects of cognition. We find that most social-brain areas respond to both social and non-social reactivity rather than just to human opponents. However, the TPJ shows a dissociation from the dmPFC: its activity and connectivity primarily reflect context-dependent outcome processing and reactivity detection, while dmPFC engagement is linked to implementation of a behavioral strategy. Our results characterize an overarching computational property of the social brain but also suggest specialized roles for subregions of this network.

Enhancing reappraisal of negative emotional memories with transcranial direct current stimulation.

Reappraisal of negative memories and experiences is central for mental health and well-being. Deficiency of reappraisal lies at the core of many psychiatric disorders and is a key target for treatment. Here we apply transcranial direct current stimulation (tDCS) to enhance reappraisal of negative emotional memories. In a randomised, sham-controlled, 2 × 2 between-subject and double-blinded study, we applied single sessions of anodal and sham tDCS over the right dorsolateral prefrontal cortex (dlPFC) of 101 healthy participants while reappraising a personal negative memory or engaging in a control task. We hypothesised that (i) reappraisal decreases negative valence, arousal and evaluations of the memory and leads to improved decision making, and (ii) tDCS leads to additional changes in these reappraisal outcomes. In line with these hypotheses, participants' personal memories were rated as less negative and less arousing following reappraisal. Anodal tDCS during reappraisal was associated with significant short-term reductions in negative valence compared to sham stimulation. Our results indicate that tDCS may enhance some of the effects of reappraisal. If replicated, our findings suggest potential benefits elicited by tDCS stimulation that may help optimise current treatment approaches for psychiatric disorders.

Anticipatory energization revealed by pupil and brain activity guides human effort-based decision making.

An organism's fitness is determined by how it chooses to adapt to effort in response to challenges. Exertion of effort correlates with activity in dorsomedial prefrontal cortex (dmPFC) and noradrenergic pupil dilation, but little is known about the role of these neurophysiological processes for decisions about future efforts - they may provide anticipatory energization to help us accept the challenge or a cost representation that is weighted against the expected rewards. Here we provide evidence for the former, by measuring pupil and fMRI brain responses while 52 human participants (29 females) chose whether to exert efforts to obtain rewards. Both pupil-dilation rate and dMPFC fMRI activity increased with anticipated effort level, and these increases differ depending on the choice outcome: They were stronger when participants chose to accept the challenge compared to when the challenge was declined. Crucially, the choice-dependent modulation of pupil and brain-activity effort representations were stronger in participants whose behavioral choices were more sensitive to effort. Our results identify a process involving the peripheral and central human nervous system that simulates the required energization prior to overt response, suggesting a role in guiding effort-based decisions.SIGNIFICANCE STATEMENT:The brain's arousal system tracks the effort we engage in during strenuous activity. But much less is known about what role this effort signaling may play when we decide whether to exert effort in the future. Here we characterize pupil-linked arousal and brain signals that guide decisions whether to engage in effort to gain money. During such choices, increases in brain activity and pupil dilation correlated with the effort involved in the chosen option, and these increases were stronger when people decided to accept the effort compared to when they rejected it. These results suggest that the brain arousal system guides decisions by energizing the organism for the prospective challenge.

Frontopolar theta oscillations link metacognition with prospective decision making.

Prospective decision making considers the future consequences of actions and therefore requires agents to represent their present subjective preferences reliably across time. Here, we test the link of frontopolar theta oscillations to both metacognitive ability and prospective choice behavior. We target these oscillations with transcranial alternating current stimulation while participants make decisions between smaller-sooner and larger-later monetary rewards and rate their choice confidence after each decision. Stimulation designed to enhance frontopolar theta oscillations increases metacognitive accuracy in reports of subjective uncertainty in intertemporal decisions. Moreover, the stimulation also enhances the willingness of participants to restrict their future access to short-term gratification by strengthening the awareness of potential preference reversals. Our results suggest a mechanistic link between frontopolar theta oscillations and metacognitive knowledge about the stability of subjective value representations, providing a potential explanation for why frontopolar cortex also shields prospective decision making against future temptation.

Real-world stress resilience is associated with the responsivity of the locus coeruleus.

Individuals may show different responses to stressful events. Here, we investigate the neurobiological basis of stress resilience, by showing that neural responsitivity of the noradrenergic locus coeruleus (LC-NE) and associated pupil responses are related to the subsequent change in measures of anxiety and depression in response to prolonged real-life stress. We acquired fMRI and pupillometry data during an emotional-conflict task in medical residents before they underwent stressful emergency-room internships known to be a risk factor for anxiety and depression. The LC-NE conflict response and its functional coupling with the amygdala was associated with stress-related symptom changes in response to the internship. A similar relationship was found for pupil-dilation, a potential marker of LC-NE firing. Our results provide insights into the noradrenergic basis of conflict generation, adaptation and stress resilience.

Genetic underpinnings of risky behaviour relate to altered neuroanatomy.

Previous research points to the heritability of risk-taking behaviour. However, evidence on how genetic dispositions are translated into risky behaviour is scarce. Here, we report a genetically informed neuroimaging study of real-world risky behaviour across the domains of drinking, smoking, driving and sexual behaviour in a European sample from the UK Biobank (N = 12,675). We find negative associations between risky behaviour and grey-matter volume in distinct brain regions, including amygdala, ventral striatum, hypothalamus and dorsolateral prefrontal cortex (dlPFC). These effects are replicated in an independent sample recruited from the same population (N = 13,004). Polygenic risk scores for risky behaviour, derived from a genome-wide association study in an independent sample (N = 297,025), are inversely associated with grey-matter volume in dlPFC, putamen and hypothalamus. This relation mediates roughly 2.2% of the association between genes and behaviour. Our results highlight distinct heritable neuroanatomical features as manifestations of the genetic propensity for risk taking.

Long-Term Effects of Self-Administered Transcranial Direct Current Stimulation in Episodic Migraine Prevention: Results of a Randomized Controlled Trial.

BACKGROUND: Migraine is a multifactorial neurovascular disorder, which affects about 12% of the general population. In episodic migraine, the visual cortex revealed abnormal processing, most likely due to decreased preactivation level. Transcranial direct current stimulation (tDCS) is able to modify cortical excitability and might result in an alleviation of migraine occurrence if used repetitively. OBJECTIVE: To test the hypothesis that self-administered anodal tDCS over the visual cortex significantly decreases the number of monthly migraine days in episodic migraine. MATERIALS AND METHODS: The study was single-blind, randomized, and sham-controlled. Inclusion criteria were age 18-80 years and an ICHD-3 diagnosis of episodic migraine. Exclusion criteria were pregnancy, presence of a neurodegenerative disorder, a contraindication against MRI examinations, and less than two migraine days during the 28-day baseline period. Patients in whom the baseline period suggested chronic migraine were excluded. After baseline, participants applied daily either verum (anodal-1 mA to 20 min) or sham tDCS (anodal-1 mA to 30 sec) at Oz (reference Cz electrode) for 28 days. Headache diaries were used to record the number of migraine days at baseline, during the stimulation period, and during four subsequent 28-day periods. RESULTS: Twenty-eight patients were included; two were excluded after the baseline period because less than two migraine days occurred; three were excluded because their headache diaries suggested the diagnosis of chronic migraine. Twenty-three datasets were taken for further analysis. Compared to sham tDCS (n = 12), verum tDCS (n = 11) resulted in a lower number of migraine days (p = 0.010) across all follow-up periods. We found no significant change in total headache days (p = 0.165), anxiety (p = 0.884), or depression scores (p = 0.535). No serious adverse events occurred; minor side effects were similar in both groups. CONCLUSIONS: This study provides Class II evidence that self-administered anodal tDCS over the visual cortex in episodic migraine results in a significantly lower number of monthly migraine days. However, it has neither an immediate nor a long-term effect.

Effect of an Educational Intervention on Therapeutic Inertia in Neurologists With Expertise in Multiple Sclerosis: A Randomized Clinical Trial.

Importance: Therapeutic inertia (TI) is the failure to escalate therapy when treatment goals are unmet and is associated with low tolerance to uncertainty and aversion to ambiguity in physician decision-making. Limited information is available on how physicians handle therapeutic decision-making in the context of uncertainty. Objective: To evaluate whether an educational intervention decreases TI by reducing autonomic arousal response (pupil dilation), a proxy measure of how physicians respond to uncertainty during treatment decisions. Design, Setting, and Participants: In this randomized clinical trial, 34 neurologists with expertise in multiple sclerosis (MS) practicing at 15 outpatient MS clinics in academic and community institutions from across Canada were enrolled. Participants were randomly assigned to receive an educational intervention that facilitates treatment decisions (active group) or to receive no exposure to the intervention (usual care [control group]) from December 2017 to March 2018. Participants listened to 20 audio-recorded simulated case scenarios as pupil responses were assessed by eye trackers. Autonomic arousal was assessed as pupil dilation in periods in which critical information was provided (first period [T1]: clinical data, second period [T2]: neurologic status, and third period [T3]: magnetic resonance imaging data). Data were analyzed from September 2018 to March 2020. Interventions: The traffic light system (TLS)-based educational intervention vs usual care (unexposed). The TLS (use of established associations between traffic light colors and actions to stop or proceed) assists participants in identifying factors associated with worse prognosis in MS care, thereby facilitating the treatment decision-making process by use of established associations between red, green, and yellow colors and risk levels, and actions (treatment decisions). Main Outcomes and Measures: Pupil assessment was the primary autonomic outcome. To test the treatment effect of the educational intervention (TLS), difference-in-differences models (also called untreated control group design with pretest and posttest) were used. Results: Of 38 eligible participants, 34 (89.4%) neurologists completed the study. The mean (SD) age was 44.6 (11.6) years; 38.3% were female and 20 (58.8%) were MS specialists. Therapeutic inertia was present in 50.0% (17 of 34) of all participants and was associated with greater pupil dilation. For every additional SD of pupil dilation, the odds of TI increased by 51% for T1 (odds ratio, 1.51; 95% CI, 1.12-2.03), by 31% for T2 (odds ratio, 1.31; 95% CI, 1.08-1.59), and by 49% for T3 (odds ratio, 1.49; 95% CI, 1.13-1.97). The intervention significantly reduced TI (risk reduction, 31.5%; 95% CI, 16.1%-47.0%). Autonomic arousal responses mediated 29.0% of the effect of the educational intervention on TI. Conclusions and Relevance: In this randomized clinical trial, the TLS intervention decreased TI as measured by pupil dilation, which suggests that individual autonomic arousal is an indicator of how physicians handle uncertainty when making live therapeutic decisions. Pupil response, a biomarker of TI, may eventually be useful in medical education. Trial Registration: ClinicalTrials.gov Identifier: NCT03134794.

Role of the locus coeruleus arousal system in cognitive control.

Cognitive control lies at the core of human adaptive behaviour. Humans vary substantially in their ability to execute cognitive control with respect to optimally facing environmental challenges, although the neural origins of this heterogeneity are currently not well understood. Recent theoretical frameworks implicate the locus coeruleus noradrenergic arousal system (LC-NE) in that process. Invasive neurophysiological work in rodents has shown that the LC-NE is an important homeostatic control centre of the body. LC-NE innervates the entire neocortex and has particularly strong connections with the cingulate gyrus. In the present study, using a response conflict task, functional magnetic resonance imaging and concurrent pupil dilation measures (a proxy for LC-NE firing), we provide empirical evidence for a decisive role of the LC-NE in cognitive control in humans. We show that the level of individual behavioural adjustment in cognitive control relates to the level of functional coupling between LC-NE and the dorsomedial prefrontal cortex, as well as dorsolateral prefrontal cortex. Moreover, we show that the pupil is substantially more dilated during conflict trials requiring behavioural adjustment than during no conflict trials. In addition, we explore a potential relationship between pupil dilation and neural activity during choice conflict adjustments. Our data provide novel insight into arousal-related influences on cognitive control and suggest pupil dilation as a potential external marker for endogenous neural processes involved in optimising behavioural control. Our results may also be clinically relevant for a variety of pathologies where cognitive control is compromised, such as anxiety, depression, addiction and post-traumatic stress disorder.

The right temporoparietal junction enables delay of gratification by allowing decision makers to focus on future events.

Studies of neural processes underlying delay of gratification usually focus on prefrontal networks related to curbing affective impulses. Here, we provide evidence for an alternative mechanism that facilitates delaying gratification by mental orientation towards the future. Combining continuous theta-burst stimulation (cTBS) with functional neuroimaging, we tested how the right temporoparietal junction (rTPJ) facilitates processing of future events and thereby promotes delay of gratification. Participants performed an intertemporal decision task and a mental time-travel task in the MRI scanner before and after receiving cTBS over the rTPJ or the vertex (control site). rTPJ cTBS led to both stronger temporal discounting for longer delays and reduced processing of future relative to past events in the mental time-travel task. This finding suggests that the rTPJ contributes to the ability to delay gratification by facilitating mental representation of outcomes in the future. On the neural level, rTPJ cTBS led to a reduction in the extent to which connectivity of rTPJ with striatum reflected the value of delayed rewards, indicating a role of rTPJ-striatum connectivity in constructing neural representations of future rewards. Together, our findings provide evidence that the rTPJ is an integral part of a brain network that promotes delay of gratification by facilitating mental orientation to future rewards.

Dissociable mechanisms govern when and how strongly reward attributes affect decisions.

Theories and computational models of decision-making usually focus on how strongly different attributes are weighted in choice, for example, as a function of their importance or salience to the decision-maker. However, when different attributes affect the decision process is a question that has received far less attention. Here, we investigated whether the timing of attribute consideration has a unique influence on decision-making by using a time-varying drift diffusion model and data from four separate experiments. Experimental manipulations of attention and neural activity demonstrated that we can dissociate the processes that determine the relative weighting strength and timing of attribute consideration. Thus, the processes determining either the weighting strengths or the timing of attributes in decision-making can independently adapt to changes in the environment or goals. Quantifying these separate influences of timing and weighting on choice improves our understanding and predictions of individual differences in decision behaviour.