A shared neural substrate for mentalizing and the affective component of sentence comprehension

Abstract

Using event-related fMRI in a sample of 42 healthy participants, we compared the cerebral activity maps obtained when classifying spoken sentences based on the mental content of the main character (belief, deception or empathy) or on the emotional tonality of the sentence (happiness, anger or sadness). To control for the effects of different syntactic constructions (such as embedded clauses in belief sentences), we subtracted from each map the BOLD activations obtained during plausibility judgments on structurally matching sentences, devoid of emotions or ToM. The obtained theory of mind (ToM) and emotional speech comprehension networks overlapped in the bilateral temporo-parietal junction, posterior cingulate cortex, right anterior temporal lobe, dorsomedial prefrontal cortex and in the left inferior frontal sulcus. These regions form a ToM network, which contributes to the emotional component of spoken sentence comprehension. Compared with the ToM task, in which the sentences were enounced on a neutral tone, the emotional sentence classification task, in which the sentences were play-acted, was associated with a greater activity in the bilateral superior temporal sulcus, in line with the presence of emotional prosody. Besides, the ventromedial prefrontal cortex was more active during emotional than ToM sentence processing. This region may link mental state representations with verbal and prosodic emotional cues. Compared with emotional sentence classification, ToM was associated with greater activity in the caudate nucleus, paracingulate cortex, and superior frontal and parietal regions, in line with behavioral data showing that ToM sentence comprehension was a more demanding task.

Figure 1. Overlap between emotional and ToM sentence processing (in blue).

Three-plane views and surface renderings of the significant activations during language comprehension (conjunction of PLAUTOM and TOM, in warm colors) and ToM sentence comprehension) as compared with a plausibility judgment task on sentences of comparable complexity (TOM - PLAUTOM, in green). The overlap between the TOM task and the emotional sentence classification task (EMO), relative to their matched plausibility judgment tasks (PLAUTOM and PLAUEMO) is rendered or contoured in blue (conjunction analysis, p<0.05 FWE). The functional data (SPM t-map) are overlaid on the mean grey matter image of the stereotaxic template (T-80TVS, MNI space). The functional activation threshold was set at p<0.05, FWE correction for multiple comparisons. The conjunction was masked so as to include only areas that also differ between the EMO and GRAM tasks (at p<0.0001, uncorrected).

Figure 2. Differences between emotional and ToM sentence processing, as assessed by comparisons between EMO (blue shades) and TOM (green shades), relative to their corresponding plausibility judgment tasks (PLAUEMO and PLAUTOM).

The functional data (SPM t-map) are overlaid on a representative subject in the MNI space, on white matter surface and on axial slices in neurological orientation. The accompanying plots (mean ± SEM) present the SPM contrast values (relative to beep-detection baseline) during the two pairs of sentence comprehension tasks in the regions more active during EMO than TOM (blue lines), and during TOM compared with EMO (green lines), contrasted to the PLAUEMO and PLAUTOM reference tasks. The voxel-wise functional activation threshold was set at p<0.05, corrected for multiple comparisons. The [EMO – PLAUEMO] – [TOM – PLAUTOM] contrast, showing regions more active during emotional than ToM speech processing, was masked inclusively by the EMO – GRAM contrast (at p<0.0001, uncorrected). The reverse contrast ([TOM – PLAUTOM] – [EMO – PLAUEMO]) was masked inclusively by the TOM – PLAUTOM contrast (at p<0.0001, uncorrected).

Figure 3. Response profile of Medial-network nodes (mean ± SEM).

The BOLD contrast values during the EMO, GRAM, and PLAUEMO tasks (blue shades), and TOM and PLAUTOM tasks (green shades), relative to beep-detection baseline, were extracted in the 6 regions of the Medial network defined in a previous study using the EMO and GRAM tasks (dmPFC, vmPFC, pCC and Left TPJ; blue labels, see [5]). The coloured spheres (4 mm radius) indicate the regions-of-interest. We added the two mentalizing regions of the right hemisphere (R TPJ and R MTG; green labels), uncovered by the addition of the TOM, PLAUTOM and PLAUEMO tasks.

Figure 4. Average BOLD response of 3 vmPFC regions-of-interest to the 3 different conditions of EMO or TOM (mean ± SEM).

Left: significant region from the EMO and TOM conjunction (a-vmPFC); Centre: region of the Medial network (m-vmPFC); Right: significant region from the EMO – TOM comparison (p-vmPFC).