Shared and nonshared neural networks of cognitive and affective theory-of-mind: a neuroimaging study using cartoon picture stories

Abstract

Theory of mind (ToM) refers to the ability to represent one's own and others' cognitive and affective mental states. Recent imaging studies have aimed to disentangle the neural networks involved in cognitive as opposed to affective ToM, based on clinical observations that the two can functionally dissociate. Due to large differences in stimulus material and task complexity findings are, however, inconclusive. Here, we investigated the neural correlates of cognitive and affective ToM in psychologically healthy male participants (n = 39) using functional brain imaging, whereby the same set of stimuli was presented for all conditions (affective, cognitive and control), but associated with different questions prompting either a cognitive or affective ToM inference. Direct contrasts of cognitive versus affective ToM showed that cognitive ToM recruited the precuneus and cuneus, as well as regions in the temporal lobes bilaterally. Affective ToM, in contrast, involved a neural network comprising prefrontal cortical structures, as well as smaller regions in the posterior cingulate cortex and the basal ganglia. Notably, these results were complemented by a multivariate pattern analysis (leave one study subject out), yielding a classifier with an accuracy rate of more than 85% in distinguishing between the two ToM-conditions. The regions contributing most to successful classification corresponded to those found in the univariate analyses. The study contributes to the differentiation of neural patterns involved in the representation of cognitive and affective mental states of others.

Keywords: cognitive and affective ToM; functional brain imaging; multivariate analysis; theory of mind.

Figure 1

Example of a cartoon story (cooperation) presented to study subjects. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Schematic representation of the study design. Each of the 12 stories was presented 3 times for each condition, leading to a total of 36 pseudo randomized trials. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 3

Shared and nonshared neural networks of cognitive and affective ToM (Analysis 1). Statistical parameter maps of shared and nonshared neural networks of affective and cognitive theory of mind. Contrast between affective and control condition (affective > control) is shown in blue, contrast between cognitive and control condition (cognitive > control) is shown in green, overlap in turquoise. TPJ = temporoparietal junction. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

Differences in brain activation between cognitive and affective ToM (Analysis 2). Statistical parameter maps of the within subject direct comparisons of the two ToM conditions. Contrast affective > cognitive ToM is shown in red in the top‐panel, contrast cognitive > affective ToM is shown in yellow in the bottom panel.[Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 5

Weighting factors of the SVM (Analysis 3). Coefficients of the weighting vectors of the SVM. In regions shown in blue, a higher activation led to cognitive classification, in regions shown in red, a higher activation led to an affective classification. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]