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

Abstract

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. Highlights-We investigated effective connectivity with dynamic causal modelling for fMRI -We used a new exhaustive search procedure to find the best of all possible models -Social demands modulate the backward and lateral connections most strongly -Conversely, executive task demands modulated the forward connections most strongly -We interpret the results in terms of Bayesian hierarchical predictive coding Graphical abstractEffective connectivity analysis shows that backward and lateral connections are modulated more strongly by social task demands (A); whereas forward connections are modulated more strongly by executive task demands (B). AbstractPrevious 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 deman...

Getting on the same page: The neural basis for social coordination deficits in behavioral variant frontotemporal degeneration

“…Only a limited number of studies to date have examined perspective-taking in a communicative context (Dumontheil et al, 2010; Hillebrandt et al, 2013; Wardlow, 2013; Wardlow et al, 2014). For example, in an fMRI study of healthy volunteers, Dumontheil et al, (2010) used a variant of the director task, originally described by Keysar and colleagues (Keysar et al, 2000, 2003).…”

“…The authors report activation in mPFC and left temporal pole for the critical condition (director present, 3-objects), which partially overlaps with our findings. In a follow-up study, Hillebrandt et al, (2013) used dynamic causal modeling to show that the social demands of the task modulate backward connections from mPFC. The paradigm in both studies, however, is comprehension-based and requires subjects to identify the target object via a motor response.…”

“…Previous studies examining perspective-taking (Dumontheil et al, 2010; Hillebrandt et al, 2013; Wardlow, 2013; Wardlow et al, 2014) used stimuli that physically obstruct one partner’s view, much like our privileged ground condition. However, the perspective-taking required during most conversations involves not necessarily the alignment of visuospatial references, but rather the alignment of mental representations and situation models.…”

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

“…To identify and summarise regional responses for further dynamic causal modelling we used standard procedures37. Timeseries from VOIs associated with the above contrasts were summarised using the SPM12b Eigenvariate toolbox: we extracted each participant's principal eigenvariate around the participant-specific local maxima activations nearest to the peak voxel of the group (between subject) GLM analysis (see Table 1 and 2).…”

Differential responses of the dorsomedial prefrontal cortex and right posterior superior temporal sulcus to spontaneous mentalizing

“…As reasoned above, one possible explanation might be that of a qualitative difference between individuals with and without ASD. For instance, as the processing of socially relevant information might be less efficient in subjects with high autism traits [Frith, ], our observation of increased dmPFC‐pSTS connectivity during mentalizing might reflect a compensatory mechanism in nonclinical groups for enhanced detection and inference of social meaning [Hillebrandt et al, ; Nummenmaa et al, ]. Finally, previous studies in ASD patients have reported altered connectivity of temporal areas with lower level sensory brain regions during animated shapes tasks, such as visual area V3 [Castelli et al, ] and lateral fusiform gyrus [Weisberg et al, ].…”