Serotonin.

Serotonin, also known as 5-hydroxytryptamine or 5-HT, is a neuromodulator widely recognized for its role in various psychoactive drugs. These drugs can exhibit antidepressant, antipsychotic, anxiolytic, empathogenic, or psychedelic effects, depending on their specific interactions with the serotonin system as well as other neuromodulators such as noradrenaline, dopamine, and oxytocin. This has led to a widespread belief that the neurochemical processes taking place deep inside our brains affect our subjective experiences and mental health. However, a scientific understanding of how neuromodulators' functions relate to drug effects remains elusive.

Regulation of social hierarchy learning by serotonin transporter availability.

Learning one's status in a group is a fundamental process in building social hierarchies. Although animal studies suggest that serotonin (5-HT) signaling modulates learning social hierarchies, direct evidence in humans is lacking. Here we determined the relationship between serotonin transporter (SERT) availability and brain systems engaged in learning social ranks combining computational approaches with simultaneous PET-fMRI acquisition in healthy males. We also investigated the link between SERT availability and brain activity in a non-social control condition involving learning the payoffs of slot machines. Learning social ranks was modulated by the dorsal raphe nucleus (DRN) 5-HT function. BOLD ventral striatal response, tracking the rank of opponents, decreased with DRN SERT levels. Moreover, this link was specific to the social learning task. These findings demonstrate that 5-HT plays an influence on the computations required to learn social ranks.

Developmental shifts in computations used to detect environmental controllability.

Accurate assessment of environmental controllability enables individuals to adaptively adjust their behavior-exploiting rewards when desirable outcomes are contingent upon their actions and minimizing costly deliberation when their actions are inconsequential. However, it remains unclear how estimation of environmental controllability changes from childhood to adulthood. Ninety participants (ages 8-25) completed a task that covertly alternated between controllable and uncontrollable conditions, requiring them to explore different actions to discover the current degree of environmental controllability. We found that while children were able to distinguish controllable and uncontrollable conditions, accuracy of controllability assessments improved with age. Computational modeling revealed that whereas younger participants' controllability assessments relied on evidence gleaned through random exploration, older participants more effectively recruited their task structure knowledge to make highly informative interventions. Age-related improvements in working memory mediated this qualitative shift toward increased use of an inferential strategy. Collectively, these findings reveal an age-related shift in the cognitive processes engaged to assess environmental controllability. Improved detection of environmental controllability may foster increasingly adaptive behavior over development by revealing when actions can be leveraged for one's benefit.

Stress-sensitive inference of task controllability.

Estimating the controllability of the environment enables agents to better predict upcoming events and decide when to engage controlled action selection. How does the human brain estimate controllability? Trial-by-trial analysis of choices, decision times and neural activity in an explore-and-predict task demonstrate that humans solve this problem by comparing the predictions of an 'actor' model with those of a reduced 'spectator' model of their environment. Neural blood oxygen level-dependent responses within striatal and medial prefrontal areas tracked the instantaneous difference in the prediction errors generated by these two statistical learning models. Blood oxygen level-dependent activity in the posterior cingulate, temporoparietal and prefrontal cortices covaried with changes in estimated controllability. Exposure to inescapable stressors biased controllability estimates downward and increased reliance on the spectator model in an anxiety-dependent fashion. Taken together, these findings provide a mechanistic account of controllability inference and its distortion by stress exposure.

Prediction or Causation? Towards a Redefinition of Task Controllability.

As research investigating controllability perception gains momentum, the algorithmic definition of controllability must be updated to avoid confusion between controllability and predictability. Reframing controllable environments as environments that allow agents to exert causal influences over state transitions can circumvent the confounding influence of predictability when designing cognitive tasks.

A Causal Role for the Right Dorsolateral Prefrontal Cortex in Avoidance of Risky Choices and Making Advantageous Selections.

In everyday life, risky decision-making relies on multiple cognitive processes including sensitivity to reinforcers, exploration, learning, and forgetting. Neuroimaging evidence suggests that the dorsolateral prefrontal cortex (DLPFC) is involved in exploration and risky decision-making, but the nature of its computations and its causal role remain uncertain. We provide evidence for the role of the DLPFC in value-independent, directed exploration on the Iowa Gambling Task (IGT) and we describe a new computational model to account for the competition of directed exploration and exploitation in guiding decisions. Forty-two healthy human participants were included in a right DLPFC, left DLPFC or sham stimulation groups using continuous theta-burst stimulation (cTBS). Immediately after cTBS, the IGT was completed. Computational modelling was used to account for exploration and exploitation with different combinations with value-based and sensitivity to reinforcers for each group. Applying cTBS to the left and right DLPFC selectively decreased directed exploration on the IGT compared to sham stimulation. Model-based analyses further indicated that the right (but not the left) DLPFC stimulation increased sensitivity to reinforcers, leading to avoidance of risky choices and promoting advantageous choices during the task. Although these findings are based on small sample sizes per group, they nevertheless elucidate the causal role of the right DLPFC in governing the exploration-exploitation tradeoff during decision-making in uncertain and ambiguous contexts.

Relevance of working memory for reinforcement learning in older adults varies with timescale of learning.

In young adults, individual differences in working memory (WM) contribute to reinforcement learning (RL). Age-related RL changes, however, are mostly attributed to decreased reward prediction-error (RPE) signaling. Here, we investigated the contribution of WM to RL in young (18-35) and older (≥65) adults. Because WM supports maintenance across a limited timescale, we only expected a relation between RL and WM with short delays between stimulus repetitions. Our results demonstrated better learning with short than long delays. A week later, however, long-delay associations were remembered better. Computational modeling corroborated that during learning, WM was more engaged by young adults in the short-delay condition than in any other age-condition combination. Crucially, both model-derived and neuropsychological assessments of WM predicted short-delay learning in older adults, who further benefitted from using self-conceived learning strategies. Thus, depending on the timescale of learning, age-related RL changes may not only reflect decreased RPE signaling but also WM decline.

Sequential exploration in the Iowa gambling task: Validation of a new computational model in a large dataset of young and old healthy participants.

The Iowa Gambling Task (IGT) is one of the most common paradigms used to assess decision-making and executive functioning in neurological and psychiatric disorders. Several reinforcement-learning (RL) models were recently proposed to refine the qualitative and quantitative inferences that can be made about these processes based on IGT data. Yet, these models do not account for the complex exploratory patterns which characterize participants' behavior in the task. Using a dataset of more than 500 subjects, we demonstrate the existence of sequential exploration in the IGT and we describe a new computational architecture disentangling exploitation, random exploration and sequential exploration in this large population of participants. The new Value plus Sequential Exploration (VSE) architecture provided a better fit than previous models. Parameter recovery, model recovery and simulation analyses confirmed the superiority of the VSE scheme. Furthermore, using the VSE model, we confirmed the existence of a significant reduction in directed exploration across lifespan in the IGT, as previously reported with other paradigms. Finally, we provide a user-friendly toolbox enabling researchers to easily and flexibly fit computational models on the IGT data, hence promoting reanalysis of the numerous datasets acquired in various populations of patients and contributing to the development of computational psychiatry.

How occupational status influences the processing of faces: An EEG study.

This study examines the influence of social hierarchy on the neural electrophysiological responses to faces. In contrast with earlier EEG studies that typically manipulate social rank through competitive situations, we implemented hierarchy through occupational status and thus contrasted faces associated with high- vs. low-status (e.g. lawyer vs. waiter). Since social hierarchies are largely intertwined with gender, both female and male faces were used as stimuli, and both female and male participants were tested. The procedure consisted in presenting a status label before the face it was associated with. The analyses focused mainly on two components that have been shown to be modulated by competitive hierarchies and other social contexts, namely the N170 and the Late Positive Potential (LPP). The results indicated that gender, but not status, modulated the N170 amplitude. Moreover, high-status faces elicited larger LPP amplitude than low-status faces but this difference was driven by female participants. This gender effect is discussed in line with research showing that women and men are sensitive to different kinds of hierarchy. Methodological differences are considered to account for the discrepancy between studies that find an effect of hierarchy on the N170 and those that do not.

From relief to surprise: Dual control of epistemic curiosity in the human brain.

Epistemic curiosity (EC) is a cornerstone of human cognition that contributes to the actualization of our cognitive potential by stimulating a myriad of information-seeking behaviors. Yet, its fundamental relationship with uncertainty remains poorly understood, which limits our ability to predict within- and between-individual variability in the willingness to acquire knowledge. Here, a two-step stochastic trivia quiz designed to induce curiosity and manipulate answer uncertainty provided behavioral and neural evidence for an integrative model of EC inspired from predictive coding. More precisely, our behavioral data indicated an inverse relationship between average surprise elicited by previous trivia items and EC levels, which depended upon hemodynamic activity in the rostrolateral prefrontal cortex from one trial to another and from one individual to another. Complementary, the relief of acute curiosity recruited the ventral striatum when knowledge delivery was unpredictable. Taken together, our results account for the temporal evolution of EC over time, as well as for the interplay of EC, prior knowledge and surprise in controlling memory gain.

Spontaneous eye blink rate and dopamine synthesis capacity: preliminary evidence for an absence of positive correlation.

Dopamine is central to a number of cognitive functions and brain disorders. Given the cost of neurochemical imaging in humans, behavioural proxy measures of dopamine have gained in popularity in the past decade, such as spontaneous eye blink rate (sEBR). Increased sEBR is commonly associated with increased dopamine function based on pharmacological evidence and patient studies. Yet, this hypothesis has not been validated using in vivo measures of dopamine function in humans. To fill this gap, we measured sEBR and striatal dopamine synthesis capacity using [18 F]DOPA PET in 20 participants (nine healthy individuals and 11 pathological gamblers). Our results, based on frequentist and Bayesian statistics, as well as region-of-interest and voxel-wise analyses, argue against a positive relationship between sEBR and striatal dopamine synthesis capacity. They show that, if anything, the evidence is in favour of a negative relationship. These results, which complement findings from a recent study that failed to observe a relationship between sEBR and dopamine D2 receptor availability, suggest that caution and nuance are warranted when interpreting sEBR in terms of a proxy measure of striatal dopamine.

An Integrative Interdisciplinary Perspective on Social Dominance Hierarchies.

In the course of evolution, social dominance has been a strong force shaping the organization of social systems in many species. Individuals with a better ability to represent social dominance relationships and to adapt their behavior accordingly usually achieve better access to resources, hence providing benefits in terms of reproduction, health, and wellbeing. Understanding how and to what extent our brains are affected by social dominance requires interdisciplinary efforts. Here, we integrate findings from social neuroscience, evolutionary biology, and developmental psychology to highlight how social hierarchies are learned and represented in primates. We also review neuropharmacological findings showing how dopamine, serotonin, and testosterone influence social hierarchies and we emphasize their key clinical implications on vulnerabilities to neuropsychiatric disorders.

Embodied emotion impairment in Huntington's Disease.

Theories of embodied cognition suggest that perceiving an emotion involves somatovisceral and motoric re-experiencing. Here we suggest taking such an embodied stance when looking at emotion processing deficits in patients with Huntington's Disease (HD), a neurodegenerative motor disorder. The literature on these patients' emotion recognition deficit has recently been enriched by some reports of impaired emotion expression. The goal of the study was to find out if expression deficits might be linked to a more motoric level of impairment. We used electromyography (EMG) to compare voluntary emotion expression from words to emotion imitation from static face images, and spontaneous emotion mimicry in 28 HD patients and 24 matched controls. For the latter two imitation conditions, an underlying emotion understanding is not imperative (even though performance might be helped by it). EMG measures were compared to emotion recognition and to the capacity to identify and describe emotions using alexithymia questionnaires. Alexithymia questionnaires tap into the more somato-visceral or interoceptive aspects of emotion perception. Furthermore, we correlated patients' expression and recognition scores to cerebral grey matter volume using voxel-based morphometry (VBM). EMG results replicated impaired voluntary emotion expression in HD. Critically, voluntary imitation and spontaneous mimicry were equally impaired and correlated with impaired recognition. By contrast, alexithymia scores were normal, suggesting that emotion representations on the level of internal experience might be spared. Recognition correlated with brain volume in the caudate as well as in areas previously associated with shared action representations, namely somatosensory, posterior parietal, posterior superior temporal sulcus (pSTS) and subcentral sulcus. Together, these findings indicate that in these patients emotion deficits might be tied to the "motoric level" of emotion expression. Such a double-sided recognition and expression impairment may have important consequences, interrupting empathy in nonverbal communication both ways (understanding and being understood), independently of intact internal experience of emotion.

Social brains and divides: the interplay between social dominance orientation and the neural sensitivity to hierarchical ranks.

Ubiquitous in the animal kingdom, dominance hierarchies emerge through social competition and underlie the control of resources. Confronting the disruptive influence of socioeconomic inequalities, human populations tend to split into groups who legitimize existing dominance hierarchies and groups who condemn them. Here, we hypothesized that variations in the neural sensitivity to dominance ranks partly underpins this ideological split, as measured by the social dominance orientation scale (SDO). Following a competitive task used to induce dominance representations about three opponents (superior, equal and inferior), subjects were passively presented the faces of these opponents while undergoing fMRI. Analyses demonstrated that two key brain regions, the superior temporal sulcus (STS) and anterior dorsolateral prefrontal cortex (aDLPFC) were sensitive to social ranks. Confirming our hypothesis, the sensitivity of the right aDLPFC to social ranks correlated positively with the SDO scale, which is known to predict behaviors and political attitudes associated with the legitimization of dominance hierarchies. This study opens new perspectives for the neurosciences of political orientation and social dominance.

Dynamical Representation of Dominance Relationships in the Human Rostromedial Prefrontal Cortex.

Humans and other primates have evolved the ability to represent their status in the group's social hierarchy, which is essential for avoiding harm and accessing resources. Yet it remains unclear how the human brain learns dominance status and adjusts behavior accordingly during dynamic social interactions. Here we address this issue with a combination of fMRI and transcranial direct current stimulation (tDCS). In a first fMRI experiment, participants learned an implicit dominance hierarchy while playing a competitive game against three opponents of different skills. Neural activity in the rostromedial PFC (rmPFC) dynamically tracked and updated the dominance status of the opponents, whereas the ventromedial PFC and ventral striatum reacted specifically to competitive victories and defeats. In a second experiment, we applied anodal tDCS over the rmPFC to enhance neural excitability while subjects performed a similar competitive task. The stimulation enhanced the relative weight of victories over defeats in learning social dominance relationships and exacerbated the influence of one's own dominance over competitive strategies. Importantly, these tDCS effects were specific to trials in which subjects learned about dominance relationships, as they were not present for control choices associated with monetary incentives but no competitive feedback. Taken together, our findings elucidate the role of rmPFC computations in dominance learning and unravel a fundamental mechanism that governs the emergence and maintenance of social dominance relationships in humans.