Dynamic causal modelling of effective connectivity during perspective taking in a communicative task

Previous studies have shown that taking into account another person's perspective to guide decisions is more difficult when their perspective is incongruent from one's own compared to when it is congruent. Here we used dynamic causal modelling (DCM) for functional magnetic resonance imaging (fMRI) to investigate effective connectivity between prefrontal and posterior brain regions in a task that requires participants to take into account another person's perspective in order to guide the selection of an action. Using a new procedure to score model evidence without computationally costly estimation, we conducted an exhaustive search for the best of all possible models. The results elucidate how the activity in the areas from our previously reported analysis (Dumontheil et al., 2010) are causally linked and how the connections are modulated by both the social as well as executive task demands of the task. We find that the social demands modulate the backward connections from the medial prefrontal cortex (MPFC) more strongly than the forward connections from the superior occipital gyrus (SOG) and the medial temporal gyrus (MTG) to the MPFC. This was also the case for the backward connection from the MTG to the SOG. Conversely, the executive task demands modulated the forward connections of the SOG and the MTG to the MPFC more strongly than the backward connections. We interpret the results in terms of hierarchical predictive coding

Neuronal interactions between mentalizing and action systems during indirect request processing

Human communication relies on the ability to process linguistic structure and to map words and utterances onto our environment. Furthermore, as what we communicate is often not directly encoded in our language (e.g., in the case of irony, jokes, or indirect requests), we need to extract additional cues to infer the beliefs and desires of our conversational partners. Although the functional interplay between language and the ability to mentalize has been discussed in theoretical accounts in the past, the neurobiological underpinnings of these dynamics are currently not well understood. Here, we address this issue using functional imaging (fMRI). Participants listened to question-reply dialogues. In these dialogues, a reply is interpreted as a direct reply, an indirect reply, or a request for action, depending on the question. We show that inferring meaning from indirect replies engages parts of the mentalizing network (mPFC) while requests for action also activate the cortical motor system (IPL). Subsequent connectivity analysis using Dynamic Causal Modelling (DCM) revealed that this pattern of activation is best explained by an increase in effective connectivity from the mentalizing network (mPFC) to the action system (IPL). These results are an important step towards a more integrative understanding of the neurobiological basis of indirect speech processing

Bayesian Hierarchical Predictive Coding of Human Social Behaviour

‘Bayesian hierarchical predictive coding of human social behaviour.’ Biological agents are the most complex systems humans encounter in their natural environment and it is critical to model other’s mental states correctly to predict their behaviour. To do this one has to generate a mental representation based on an internal neural model of the other agent (Chapter 1). Here we show, in a series experiments, that people use and update their Bayesian priors in social situations and explain how they create mental representations of others to guide action selection. We investigate the neural mechanisms and the brain connectivity that underlie these social processes and how they develop with age. In chapter 2, we show how experimentally induced prior experience with other people (here social inclusion or exclusion) influences the level of trust towards those people. In chapter 3, we describe an fMRI study using a social perspective-taking task that examines the developmental differences between adolescents and adults in the control of action selection by social information. Using the same task, in chapter 4, we investigate the effective connectivity between the activated regions with Dynamic causal modelling. In Chapter 5, we explore effective connectivity of fMRI data from the Human connectome project (Van Essen et al., 2012). During the task participants viewed animations of triangles moving either randomly or so that they evoke mental state attribution (Castelli et al., 2000). Chapter 6 concludes with a summary of the experiments and integrate them into existing research, as well as provide a critical synthesis of the findings in order to suggest future research directions. We interpret our findings in a hierarchical predictive coding framework, where agents try to create a neural model of the external world to minimize prediction errors, Bayesian surprise and free energy

Effective connectivity gateways to the Theory of Mind network in processing communicative intention

An Intention Processing Network (IPN), involving the medial prefrontal cortex, precuneus, bilateral posterior superior temporal sulcus, and temporoparietal junctions, plays a fundamental role in comprehending intentions underlying action goals. In a previous fMRI study, we showed that, depending on the linguistic or extralinguistic (gestural) modality used to convey the intention, the IPN is complemented by activation of additional brain areas, reflecting distinct modality-specific input gateways to the IPN. These areas involve, for the linguistic modality, the left inferior frontal gyrus (LIFG), and for the extralinguistic modality, the right inferior frontal gyrus (RIFG). Here, we tested the modality-specific gateway hypothesis, by using DCM to measure inter-regional functional integration dynamics between the IPN and LIFG/RIFG gateways. We found strong evidence of a well-defined effective connectivity architecture mediating the functional integration between the IPN and the inferior frontal cortices. The connectivity dynamics indicate a modality-specific propagation of stimulus information from LIFG to IPN for the linguistic modality, and from RIFG to IPN for the extralinguistic modality. Thus, we suggest a functional model in which the modality-specific gateways mediate the structural and semantic decoding of the stimuli, and allow for the modality-specific communicative information to be integrated in Theory of Mind inferences elaborated through the IPN

Developmental changes in effective connectivity associated with relational reasoning

Rostrolateral prefrontal cortex (RLPFC) is part of a frontoparietal network of regions involved in relational reasoning, the mental process of working with relationships between multiple mental representations. RLPFC has shown functional and structural changes with age, with increasing specificity of left RLPFC activation for relational integration during development. Here, we used dynamic causal modeling (DCM) to investigate changes in effective connectivity during a relational reasoning task through the transition from adolescence into adulthood. We examined fMRI data of 37 healthy female participants (11–30 years old) performing a relational reasoning paradigm. Comparing relational integration to the manipulation of single relations revealed activation in five regions: the RLPFC, anterior insula, dorsolateral PFC, inferior parietal lobe, and medial superior frontal gyrus. We used a new exhaustive search approach and identified a full DCM model, which included all reciprocal connections between the five clusters in the left hemisphere, as the optimal model. In line with previous resting state fMRI results, we showed distinct developmental effects on the strength of long-range frontoparietal versus frontoinsular short-range fixed connections. The modulatory connections associated with relational integration increased with age. Gray matter volume in left RLPFC, which decreased with age, partly accounted for changes in fixed PFC connectivity. Finally, improvements in relational integration performance were associated with greater modulatory and weaker fixed PFC connectivity. This pattern provides further evidence of increasing specificity of left PFC function for relational integration compared to the manipulation of single relations, and demonstrates an association between effective connectivity and performance during development. Hum Brain Mapp, 2013

Effective connectivity gateways to the Theory of Mind network in processing communicative intention

An Intention Processing Network (IPN), involving the medial prefrontal cortex, precuneus, bilateral posterior superior temporal sulcus, and temporoparietal junctions, plays a fundamental role in comprehending intentions underlying action goals. In a previous fMRI study, we showed that, depending on the linguistic or extralinguistic (gestural) modality used to convey the intention, the IPN is complemented by activation of additional brain areas, reflecting distinct modality-specific input gateways to the IPN. These areas involve, for the linguistic modality, the left inferior frontal gyrus (LIFG), and for the extralinguistic modality, the right inferior frontal gyrus (RIFG). Here, we tested the modality-specific gateway hypothesis, by using DCM to measure inter-regional functional integration dynamics between the IPN and LIFG/RIFG gateways. We found strong evidence of a well-defined effective connectivity architecture mediating the functional integration between the IPN and the inferior frontal cortices. The connectivity dynamics indicate a modality-specific propagation of stimulus information from LIFG to IPN for the linguistic modality, and from RIFG to IPN for the extralinguistic modality. Thus, we suggest a functional model in which the modality-specific gateways mediate the structural and semantic decoding of the stimuli, and allow for the modality-specific communicative information to be integrated in Theory of Mind inferences elaborated through the IPN

Social perspective taking is associated with self-reported prosocial behavior and regional cortical thickness across adolescence

Basic perspective taking and mentalising abilities develop in childhood, but recent studies indicate that the use of social perspective taking to guide decisions and actions has a prolonged development that continues throughout adolescence. Here, we aimed to replicate this research and investigate the hypotheses that individual differences in social perspective taking in adolescence are associated with real-life prosocial and antisocial behavior and differences in brain structure. We employed an experimental approach and a large cross-sectional sample (n=293) of participants aged 7-26 years old to assess age-related improvement in social perspective taking usage during performance of a version of the Director task. In subsamples, we then tested how individual differences in social perspective taking were related to self-reported prosocial behavior and peer relationship problems on the Strengths and Difficulties Questionnaire (SDQ) (n=184) and to magnetic resonance imaging (MRI) measures of regional cortical thickness and surface area (n=226). The pattern of results in the Director task replicated previous findings by demonstrating continued improvement in use of social perspective taking across adolescence. The study also showed that better social perspective taking usage is associated with more self-reported prosocial behavior, as well as to thinner cerebral cortex in regions in the left hemisphere encompassing parts of the caudal middle frontal and precentral gyri and lateral parietal regions. These associations were observed independently of age, and might partly reflect individual developmental variability. The relevance of cortical development was additionally supported by indirect effects of age on social perspective taking usage via cortical thickness

Effective connectivity during animacy perception - dynamic causal modelling of Human Connectome Project data.

Biological agents are the most complex systems humans have to model and predict. In predictive coding, high-level cortical areas inform sensory cortex about incoming sensory signals, a comparison between the predicted and actual sensory feedback is made, and information about unpredicted sensory information is passed forward to higher-level areas. Predictions about animate motion - relative to inanimate motion - should result in prediction error and increase signal passing from lower level sensory area MT+/V5, which is responsive to all motion, to higher-order posterior superior temporal sulcus (pSTS), which is selectively activated by animate motion. We tested this hypothesis by investigating effective connectivity in a large-scale fMRI dataset from the Human Connectome Project. 132 participants viewed animations of triangles that were designed to move in a way that appeared animate (moving intentionally), or inanimate (moving in a mechanical way). We found that forward connectivity from V5 to the pSTS increased, and inhibitory self-connection in the pSTS decreased, when viewing intentional motion versus inanimate motion. These prediction errors associated with animate motion may be the cause for increased attention to animate stimuli found in previous studies

A Mentalization-Informed Staging Approach to Clinical High Risk for Psychosis

The practice of diagnosis is fundamentally designed to orient treatment. In the case of early diagnosis for schizophrenia spectrum disorders (SSP) risk, the empirical base for such a practice is still young, and many clinical questions arise in the everyday clinical application of risk algorithms and ensuing therapeutic options. One of the key questions that we will focus on is the following: in cases of SSP where symptoms are successfully treated, why does residual social functioning impairment remain the most serious obstacle to remission and reinsertion in society? We will present the evidence suggesting that the roots of residual social functioning impairment may, in many cases, come from thwarted or arrested development in the specialization of social cognition during adolescence and early adulthood. We will review the evidence suggesting that both during the premorbid phase and clinical high-risk phase, attenuated psychotic symptoms may impede the maturation of key social cognitive processes, particularly the suite of reflective thinking processes coming under the term of mentalization. From this evidence base, we will adapt the staging model of SSP progression in function of our mentalization-informed model, tailored to provide a coherent framework of care addressing the key clinical needs at every stage of psychosis progression

Neuronal and behavioral correlates of the influence of contextual cues on value-based decision making = Die neuronalen und behavioralen Korrelate des Einflusses von kontextuellen Reizen auf das wertebasierte Entscheidungsverhalten : Kumulative Arbeit

Value-based decisions are almost omnipresent in life. However, they are not very well understood. Previous research has shown that the decision-making process is dynamic, and can be influenced, for instance, by increasing the saliency of a certain attribute. Therefore, one could hypothesize that it is possible to make decision-makers aware of certain long-term attributes in order to improve decisions. In four main studies published during my doctoral work, I investigated the role of contextual attributes on value-based decision making and how they influence dietary choices. The text presented here puts the published studies into a broader context and reviews various topics, such as the influence of attention on decision making, neuroscientific evidence as well as computational models in decision-making research