Boosting Serotonin Increases Information Gathering by Reducing Subjective Cognitive Costs.

Serotonin is implicated in the valuation of aversive costs, such as delay or physical effort. However, its role in governing sensitivity to cognitive effort, for example, deliberation costs during information gathering, is unclear. We show that treatment with a serotonergic antidepressant in healthy human individuals of either sex enhances a willingness to gather information when trying to maximize reward. Using computational modeling, we show this arises from a diminished sensitivity to subjective deliberation costs during the sampling process. This result is consistent with the notion that serotonin alleviates sensitivity to aversive costs in a domain-general fashion, with implications for its potential contribution to a positive impact on motivational deficits in psychiatric disorders.SIGNIFICANCE STATEMENT Gathering information about the world is essential for successfully navigating it. However, sampling information is costly, and we need to balance between gathering too little and too much information. The neurocomputational mechanisms underlying this arbitration between a putative gain, such as reward, and the associated costs, such as allocation of cognitive resources, remain unclear. In this study, we show that week-long daily treatment with a serotonergic antidepressant enhances a willingness to gather information when trying to maximize reward. Computational modeling indicates this arises from a reduced perception of aversive costs, rendering information gathering less cognitively effortful. This finding points to a candidate mechanism by which serotonergic treatment might help alleviate motivational deficits in a range of mental illnesses.

Consistency within change: Evaluating the psychometric properties of a widely used predictive-inference task.

Rapid adaptation to sudden changes in the environment is a hallmark of flexible human behaviour. Many computational, neuroimaging, and even clinical investigations studying this cognitive process have relied on a behavioural paradigm known as the predictive-inference task. However, the psychometric quality of this task has never been examined, leaving unanswered whether it is indeed suited to capture behavioural variation on a within- and between-subject level. Using a large-scale test-retest design (T1: N = 330; T2: N = 219), we assessed the internal (internal consistency) and temporal (test-retest reliability) stability of the task's most used measures. We show that the main measures capturing flexible belief and behavioural adaptation yield good internal consistency and overall satisfying test-retest reliability. However, some more complex markers of flexible behaviour show lower psychometric quality. Our findings have implications for the large corpus of previous studies using this task and provide clear guidance as to which measures should and should not be used in future studies.

Computational and behavioral markers of model-based decision making in childhood.

Human decision-making is underpinned by distinct systems that differ in flexibility and associated cognitive cost. A widely accepted dichotomy distinguishes between a cheap but rigid model-free system and a flexible but costly model-based system. Typically, humans use a hybrid of both types of decision-making depending on environmental demands. However, children's use of a model-based system during decision-making has not yet been shown. While prior developmental work has identified simple building blocks of model-based reasoning in young children (1-4 years old), there has been little evidence of this complex cognitive system influencing behavior before adolescence. Here, by using a modified task to make engagement in cognitively costly strategies more rewarding, we show that children aged 5-11-years (N = 85), including the youngest children, displayed multiple indicators of model-based decision making, and that the degree of its use increased throughout childhood. Unlike adults (N = 24), however, children did not display adaptive arbitration between model-free and model-based decision-making. Our results demonstrate that throughout childhood, children can engage in highly sophisticated and costly decision-making strategies. However, the flexible arbitration between decision-making strategies might be a critically late-developing component in human development.

Compulsivity is linked to reduced adolescent development of goal-directed control and frontostriatal functional connectivity.

A characteristic of adaptive behavior is its goal-directed nature. An ability to act in a goal-directed manner is progressively refined during development, but this refinement can be impacted by the emergence of psychiatric disorders. Disorders of compulsivity have been framed computationally as a deficit in model-based control, and have been linked also to abnormal frontostriatal connectivity. However, the developmental trajectory of model-based control, including an interplay between its maturation and an emergence of compulsivity, has not been characterized. Availing of a large sample of healthy adolescents (n = 569) aged 14 to 24 y, we show behaviorally that over the course of adolescence there is a within-person increase in model-based control, and this is more pronounced in younger participants. Using a bivariate latent change score model, we provide evidence that the presence of higher compulsivity traits is associated with an atypical profile of this developmental maturation in model-based control. Resting-state fMRI data from a subset of the behaviorally assessed subjects (n = 230) revealed that compulsivity is associated with a less pronounced change of within-subject developmental remodeling of functional connectivity, specifically between the striatum and a frontoparietal network. Thus, in an otherwise clinically healthy population sample, in early development, individual differences in compulsivity are linked to the developmental trajectory of model-based control and a remodeling of frontostriatal connectivity.

Probing apathy in children and adolescents with the Apathy Motivation Index-Child version.

Apathy is linked to mental health and altered neurocognitive functions such as learning and decision-making in healthy adults. Mental health problems typically begin to emerge during adolescence, yet little is known about how apathy develops due to an absence of quantitative measurements specific to young people. Here, we present and evaluate the Apathy Motivation Index-Child Version (AMI-CV) for children and adolescents. We show across two samples of young people (aged 8 to 17 years, total N = 191) tested in schools in the UK and on a smartphone app, that the AMI-CV is a short, psychometrically sound measure to assess levels of apathy and motivation in young people. Similar to adult versions, the AMI-CV captures three distinct apathy domains: Behavioural Activation, Social Motivation and Emotional Sensitivity. The AMI-CV showed excellent construct validity with an alternative measure of apathy and external validity replicating specific links with related mental health traits shown in adults. Our results provide a short measure of self-reported apathy in young people that enables research into apathy development. The AMI-CV can be used in conjunction with the adult version to investigate the impact of levels of apathy across the lifespan.

FENS-Kavli Network of Excellence: Science needs strong European cohesion.

Decades of scientific collaboration have brought innovation, prosperity and wide societal benefit to Europe. However, recent political events have impacted pan-European research and collaborations, and solutions are yet to materialise. Here, we argue that a vibrant, united European Research community led by its members and independent from political bodies is needed for Europe to remain a successful, interconnected scientific hub and keep delivering globally competitive science. The Federation of European Neuroscience Societies (FENS) is in an ideal position to play a paramount role in this endeavour.

Exploration heuristics decrease during youth.

Deciding between exploring new avenues and exploiting known choices is central to learning, and this exploration-exploitation trade-off changes during development. Exploration is not a unitary concept, and humans deploy multiple distinct mechanisms, but little is known about their specific emergence during development. Using a previously validated task in adults, changes in exploration mechanisms were investigated between childhood (8-9 y/o, N = 26; 16 females), early (12-13 y/o, N = 38; 21 females), and late adolescence (16-17 y/o, N = 33; 19 females) in ethnically and socially diverse schools from disadvantaged areas. We find an increased usage of a computationally light exploration heuristic in younger groups, effectively accommodating their limited neurocognitive resources. Moreover, this heuristic was associated with self-reported, attention-deficit/hyperactivity disorder symptoms in this population-based sample. This study enriches our mechanistic understanding about how exploration strategies mature during development.

Endogenous fluctuations in the dopaminergic midbrain drive behavioral choice variability.

Human behavior is surprisingly variable, even when facing the same problem under identical circumstances. A prominent example is risky decision making. Economic theories struggle to explain why humans are so inconsistent. Resting-state studies suggest that ongoing endogenous fluctuations in brain activity can influence low-level perceptual and motor processes, but it remains unknown whether endogenous fluctuations also influence high-level cognitive processes including decision making. Here, using real-time functional magnetic resonance imaging, we tested whether risky decision making is influenced by endogenous fluctuations in blood oxygenation level-dependent (BOLD) activity in the dopaminergic midbrain, encompassing ventral tegmental area and substantia nigra. We show that low prestimulus brain activity leads to increased risky choice in humans. Using computational modeling, we show that increased risk taking is explained by enhanced phasic responses to offers in a decision network. Our findings demonstrate that endogenous brain activity provides a physiological basis for variability in complex human behavior.

Credit assignment to state-independent task representations and its relationship with model-based decision making.

Model-free learning enables an agent to make better decisions based on prior experience while representing only minimal knowledge about an environment's structure. It is generally assumed that model-free state representations are based on outcome-relevant features of the environment. Here, we challenge this assumption by providing evidence that a putative model-free system assigns credit to task representations that are irrelevant to an outcome. We examined data from 769 individuals performing a well-described 2-step reward decision task where stimulus identity but not spatial-motor aspects of the task predicted reward. We show that participants assigned value to spatial-motor representations despite it being outcome irrelevant. Strikingly, spatial-motor value associations affected behavior across all outcome-relevant features and stages of the task, consistent with credit assignment to low-level state-independent task representations. Individual difference analyses suggested that the impact of spatial-motor value formation was attenuated for individuals who showed greater deployment of goal-directed (model-based) strategies. Our findings highlight a need for a reconsideration of how model-free representations are formed and regulated according to the structure of the environment.

Reliability of web-based affective auditory stimulus presentation.

Web-based experimental testing has seen exponential growth in psychology and cognitive neuroscience. However, paradigms involving affective auditory stimuli have yet to adapt to the online approach due to concerns about the lack of experimental control and other technical challenges. In this study, we assessed whether sounds commonly used to evoke affective responses in-lab can be used online. Using recent developments to increase sound presentation quality, we selected 15 commonly used sound stimuli and assessed their impact on valence and arousal states in a web-based experiment. Our results reveal good inter-rater and test-retest reliabilities, with results comparable to in-lab studies. Additionally, we compared a variety of previously used unpleasant stimuli, allowing us to identify the most aversive among these sounds. Our findings demonstrate that affective sounds can be reliably delivered through web-based platforms, which help facilitate the development of new auditory paradigms for affective online experiments.

I know better! Emerging metacognition allows adolescents to ignore false advice.

Adolescents aspire for independence. Successful independence means knowing when to rely on one's own knowledge and when to listen to others. A critical prerequisite thus is a well-developed metacognitive ability to accurately assess the quality of one's own knowledge. Little is known about whether the strive to become an independent decision maker in adolescence is underpinned by the necessary metacognitive skills. Here, we demonstrate that metacognition matures from childhood to adolescence (N = 107) and that this process coincides with greater independent decision-making. We show that adolescents, in contrast to children, take on others' advice less often, but only when the advice is misleading. Finally, we demonstrate that adolescents' reduced reliance on others' advice is explained by their increased metacognitive skills, suggesting that a developing ability to introspect may support independent decision-making in adolescence.

Distinct Roles of Dopamine and Noradrenaline in Incidental Memory.

Episodic memory is sensitive to the influence of neuromodulators, such as dopamine and noradrenaline. These influences are considered important in the expression of several known memory biases, though their specific role in memory remains unclear. Using pharmacological agents with relatively high selectivity for either dopamine (400 mg amisulpride) or noradrenaline (40 mg propranolol) we examined their specific contribution to incidental memory. In a double-blind placebo-controlled human study (30 females, 30 males in total), we show that a memory selectivity bias was insensitive to propranolol but sensitive to amisulpride, consistent with a dominant influence from dopamine. By contrast, a putative arousal-induced memory boosting effect was insensitive to amisulpride but was sensitive to propranolol, consistent with a dominant noradrenaline effect. Thus, our findings highlight specific functional roles for dopamine and noradrenaline neurotransmission in the expression of incidental memory.SIGNIFICANCE STATEMENT Why some information is preferentially encoded into memory while other information is not is a central question in cognitive neuroscience. The neurotransmitters dopamine and noradrenaline are often assumed critical in influencing this selectivity, but their specific contributions remain obscure. In this double-blind, placebo-controlled, between-subjects drug study, we investigate the contributions of noradrenaline and dopamine to episodic memory. Using an incidental memory task, we find that blocking dopamine (400 mg amisulpride) eliminates a neural-gain related memory selectivity bias. Blocking noradrenaline function (40 mg propranolol), in contrast, abolishes an arousal-related memory enhancement. In this assessment of dopamine and noradrenaline neuromodulatory effects we reveal their specific contributions to episodic memory.

Childhood socio-economic disadvantage predicts reduced myelin growth across adolescence and young adulthood.

Socio-economic disadvantage increases exposure to life stressors. Animal research suggests early life stressors impact later neurodevelopment, including myelin developmental growth. To determine how early life disadvantage may affect myelin growth in adolescence and young adulthood, we analysed data from an accelerated longitudinal neuroimaging study measuring magnetisation transfer (MT), a myelin-sensitive marker, in 288 participants (149 female) between 14 and 25 years of age at baseline. We found that early life economic disadvantage before age 12, measured by a neighbourhood poverty index, was associated with slower myelin growth. This association was observed for magnetization transfer in cortical, subcortical and core white matter regions, and also in key subcortical nuclei. Participant IQ at baseline, alcohol use, body mass index, parental occupation and self-reported parenting quality did not account for these effects, but parental education did so partially. Specifically, positive parenting moderated the effect of socio-economic disadvantage in a protective manner. Thus, early socioeconomic disadvantage appears to alter myelin growth across adolescence. This finding has potential translational implications, including clarifying whether reducing socio-economic disadvantage during childhood, and increasing parental education and positive parenting, promote normal trajectories of brain development in economically disadvantaged contexts.

Improving the reliability of model-based decision-making estimates in the two-stage decision task with reaction-times and drift-diffusion modeling.

A well-established notion in cognitive neuroscience proposes that multiple brain systems contribute to choice behaviour. These include: (1) a model-free system that uses values cached from the outcome history of alternative actions, and (2) a model-based system that considers action outcomes and the transition structure of the environment. The widespread use of this distinction, across a range of applications, renders it important to index their distinct influences with high reliability. Here we consider the two-stage task, widely considered as a gold standard measure for the contribution of model-based and model-free systems to human choice. We tested the internal/temporal stability of measures from this task, including those estimated via an established computational model, as well as an extended model using drift-diffusion. Drift-diffusion modeling suggested that both choice in the first stage, and RTs in the second stage, are directly affected by a model-based/free trade-off parameter. Both parameter recovery and the stability of model-based estimates were poor but improved substantially when both choice and RT were used (compared to choice only), and when more trials (than conventionally used in research practice) were included in our analysis. The findings have implications for interpretation of past and future studies based on the use of the two-stage task, as well as for characterising the contribution of model-based processes to choice behaviour.

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals.

Optimal decision making mandates organisms learn the relevant features of choice options. Likewise, knowing how much effort we should expend can assume paramount importance. A mesolimbic network supports reward learning, but it is unclear whether other choice features, such as effort learning, rely on this same network. Using computational fMRI, we show parallel encoding of effort and reward prediction errors (PEs) within distinct brain regions, with effort PEs expressed in dorsomedial prefrontal cortex and reward PEs in ventral striatum. We show a common mesencephalic origin for these signals evident in overlapping, but spatially dissociable, dopaminergic midbrain regions expressing both types of PE. During action anticipation, reward and effort expectations were integrated in ventral striatum, consistent with a computation of an overall net benefit of a stimulus. Thus, we show that motivationally relevant stimulus features are learned in parallel dopaminergic pathways, with formation of an integrated utility signal at choice.

Beta-Blocker Propranolol Modulates Decision Urgency During Sequential Information Gathering.

Arbitrating between timely choice and extended information gathering is critical for effective decision making. Aberrant information gathering behavior is thought to be a feature of psychiatric disorders such as schizophrenia and obsessive-compulsive disorder, but we know little about the underlying neurocognitive control mechanisms. In a double-blind, placebo-controlled drug study involving 60 healthy human subjects (30 female), we examined the effects of noradrenaline and dopamine antagonism on information gathering during performance of an information sampling task. We show that modulating noradrenaline function with 40 mg of the ß-blocker propranolol leads to decreased information gathering behavior. Modulating dopamine function via a single dose of 400 mg of amisulpride revealed some effects that were intermediate between those of propranolol and placebo. Using a Bayesian computational model, we show that sampling behavior is best explained by inclusion of a nonlinear urgency signal that promotes commitment to an early decision. Noradrenaline blockade promotes the expression of this decision-related urgency signal during information gathering. We discuss the findings with respect to psychopathological conditions that are linked to aberrant information gathering.SIGNIFICANCE STATEMENT Knowing when to stop gathering information and commit to a choice option is nontrivial. This is an important element in arbitrating between information gain and energy conservation. In this double-blind, placebo-controlled drug study, we investigated the role of catecholamines noradrenaline and dopamine on sequential information gathering. We found that blockade of noradrenaline led to a decrease in information gathering. Dopamine blockade showed an intermediate, but nonsignificant, effect. Using a Bayesian computational model, we show that this noradrenaline effect is driven by increased decision urgency, a signal that reflects an escalating subjective cost of sampling. The observation that noradrenaline modulates decision urgency suggests new avenues for treating patients that show information gathering deficits.

Annual Research Review: Developmental computational psychiatry.

Most psychiatric disorders emerge during childhood and adolescence. This is also a period that coincides with the brain undergoing substantial growth and reorganisation. However, it remains unclear how a heightened vulnerability to psychiatric disorder relates to this brain maturation. Here, we propose 'developmental computational psychiatry' as a framework for linking brain maturation to cognitive development. We argue that through modelling some of the brain's fundamental cognitive computations, and relating them to brain development, we can bridge the gap between brain and cognitive development. This in turn can lead to a richer understanding of the ontogeny of psychiatric disorders. We illustrate this perspective with examples from reinforcement learning and dopamine function. Specifically, we show how computational modelling deepens an understanding of how cognitive processes, such as reward learning, effort learning, and social learning might go awry in psychiatric disorders. Finally, we sketch the promises and limitations of a developmental computational psychiatry.

Fractionation of impulsive and compulsive trans-diagnostic phenotypes and their longitudinal associations.

OBJECTIVE: Young adulthood is a crucial neurodevelopmental period during which impulsive and compulsive problem behaviours commonly emerge. While traditionally considered diametrically opposed, impulsive and compulsive symptoms tend to co-occur. The objectives of this study were as follows: (a) to identify the optimal trans-diagnostic structural framework for measuring impulsive and compulsive problem behaviours, and (b) to use this optimal framework to identify common/distinct antecedents of these latent phenotypes. METHOD: In total, 654 young adults were recruited as part of the Neuroscience in Psychiatry Network, a population-based cohort in the United Kingdom. The optimal trans-diagnostic structural model capturing 33 types of impulsive and compulsive problem behaviours was identified. Baseline predictors of subsequent impulsive and compulsive trans-diagnostic phenotypes were characterised, along with cross-sectional associations, using partial least squares. RESULTS: Current problem behaviours were optimally explained by a bi-factor model, which yielded dissociable measures of impulsivity and compulsivity, as well as a general disinhibition factor. Impulsive problem behaviours were significantly explained by prior antisocial and impulsive personality traits, male gender, general distress, perceived dysfunctional parenting and teasing/arguments within friendships. Compulsive problem behaviours were significantly explained by prior compulsive traits and female gender. CONCLUSION: This study demonstrates that trans-diagnostic phenotypes of 33 impulsive and compulsive problem behaviours are identifiable in young adults, utilising a bi-factor model based on responses to a single questionnaire. Furthermore, these phenotypes have different antecedents. The findings yield a new framework for fractionating impulsivity and compulsivity, and suggest different early intervention targets to avert emergence of problem behaviours. This framework may be useful for future biological and clinical dissection of impulsivity and compulsivity.

Striatal structure and function predict individual biases in learning to avoid pain.

Pain is an elemental inducer of avoidance. Here, we demonstrate that people differ in how they learn to avoid pain, with some individuals refraining from actions that resulted in painful outcomes, whereas others favor actions that helped prevent pain. These individual biases were best explained by differences in learning from outcome prediction errors and were associated with distinct forms of striatal responses to painful outcomes. Specifically, striatal responses to pain were modulated in a manner consistent with an aversive prediction error in individuals who learned predominantly from pain, whereas in individuals who learned predominantly from success in preventing pain, modulation was consistent with an appetitive prediction error. In contrast, striatal responses to success in preventing pain were consistent with an appetitive prediction error in both groups. Furthermore, variation in striatal structure, encompassing the region where pain prediction errors were expressed, predicted participants' predominant mode of learning, suggesting the observed learning biases may reflect stable individual traits. These results reveal functional and structural neural components underlying individual differences in avoidance learning, which may be important contributors to psychiatric disorders involving pathological harm avoidance behavior.

Increased decision thresholds enhance information gathering performance in juvenile Obsessive-Compulsive Disorder (OCD).

Patients with obsessive-compulsive disorder (OCD) can be described as cautious and hesitant, manifesting an excessive indecisiveness that hinders efficient decision making. However, excess caution in decision making may also lead to better performance in specific situations where the cost of extended deliberation is small. We compared 16 juvenile OCD patients with 16 matched healthy controls whilst they performed a sequential information gathering task under different external cost conditions. We found that patients with OCD outperformed healthy controls, winning significantly more points. The groups also differed in the number of draws required prior to committing to a decision, but not in decision accuracy. A novel Bayesian computational model revealed that subjective sampling costs arose as a non-linear function of sampling, closely resembling an escalating urgency signal. Group difference in performance was best explained by a later emergence of these subjective costs in the OCD group, also evident in an increased decision threshold. Our findings present a novel computational model and suggest that enhanced information gathering in OCD can be accounted for by a higher decision threshold arising out of an altered perception of costs that, in some specific contexts, may be advantageous.