Anterior insula coordinates hierarchical processing of tactile mismatch responses.

The body underlies our sense of self, emotion, and agency. Signals arising from the skin convey warmth, social touch, and the physical characteristics of external stimuli. Surprising or unexpected tactile sensations can herald events of motivational salience, including imminent threats (e.g., an insect bite) and hedonic rewards (e.g., a caressing touch). Awareness of such events is thought to depend upon the hierarchical integration of body-related mismatch responses by the anterior insula. To investigate this possibility, we measured brain activity using functional magnetic resonance imaging, while healthy participants performed a roving tactile oddball task. Mass-univariate analysis demonstrated robust activations in limbic, somatosensory, and prefrontal cortical areas previously implicated in tactile deviancy, body awareness, and cognitive control. Dynamic Causal Modelling revealed that unexpected stimuli increased the strength of forward connections along a caudal to rostral hierarchy-projecting from thalamic and somatosensory regions towards insula, cingulate and prefrontal cortices. Within this ascending flow of sensory information, the AIC was the only region to show increased backwards connectivity to the somatosensory cortex, augmenting a reciprocal exchange of neuronal signals. Further, participants who rated stimulus changes as easier to detect showed stronger modulation of descending PFC to AIC connections by deviance. These results suggest that the AIC coordinates hierarchical processing of tactile prediction error. They are interpreted in support of an embodied predictive coding model where AIC mediated body awareness is involved in anchoring a global neuronal workspace.

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.

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 (11­30 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.

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.

Developmental differences in the control of action selection by social information.

Our everyday actions are often performed in the context of a social interaction. We previously showed that, in adults, selecting an action on the basis of either social or symbolic cues was associated with activations in the fronto-parietal cognitive control network, whereas the presence and use of social versus symbolic cues was in addition associated with activations in the temporal and medial prefrontal cortex (MPFC) social brain network. Here we investigated developmental changes in these two networks. Fourteen adults (21-30 years of age) and 14 adolescents (11-16 years) followed instructions to move objects in a set of shelves. Interpretation of the instructions was conditional on the point of view of a visible "director" or the meaning of a symbolic cue (Director Present vs. Director Absent) and the number of potential referent objects in the shelves (3-object vs. 1-object). 3-object trials elicited increased fronto-parietal and temporal activations, with greater left lateral prefrontal cortex and parietal activations in adults than adolescents. Social versus symbolic information led to activations in superior dorsal MPFC, precuneus, and along the superior/middle temporal sulci. Both dorsal MPFC and left temporal clusters exhibited a Director × Object interaction, with greater activation when participants needed to consider the directors' viewpoints. This effect differed with age in dorsal MPFC. Adolescents showed greater activation whenever social information was present, whereas adults showed greater activation only when the directors' viewpoints were relevant to task performance. This study thus shows developmental differences in domain-general and domain-specific PFC activations associated with action selection in a social interaction context.

Experimentally induced social inclusion influences behavior on trust games.

Being socially excluded is profoundly distressing. It is unknown whether exclusion renders victims vulnerable to manipulation or whether excluded individuals become more cautious about being exploited by, and less trusting of, the person who excluded them. We investigated this by testing how much participants trust people who have socially included or excluded them. Inclusion and exclusion were manipulated using Cyberball (a virtual ball game) and, after playing Cyberball, participants played trust games. In a Reputation group participants played trust games with players from Cyberball; in the No Reputation group, participants played with strangers. Inclusion/exclusion manipulation interacted with Group such that participants in the Reputation group trusted individuals who included them more than those who excluded them, whereas inclusion/exclusion made no difference to trust in the No-Reputation group. Our findings suggest that exclusion does not increase gullibility, but that reputation is transferred from a social to an economic setting so that social inclusion increases trust.