Elsevier

NeuroImage

Volume 55, Issue 4, 15 April 2011, Pages 1899-1911
NeuroImage

Task-specific activity and connectivity within the mentalizing network during emotion and intention mentalizing

https://doi.org/10.1016/j.neuroimage.2010.12.036Get rights and content

Abstract

Mentalizing, i.e. the process of inferring another person's mental state, is thought to be primarily subserved by three brain regions, the VMPFC (ventromedial prefrontal cortex), precuneus and TPJ (temporo-parietal junction). However, it is still unclear what the exact roles of these regions in mentalizing are. Here, we compare activity within, and functional connectivity between, the VMPFC, precuneus and TPJ during two different mentalizing tasks. Specifically, we examine whether inferring another person's emotion (“emotion mentalizing”) and inferring another person's intention (“intention mentalizing”) activate similar or distinct subregions within the VMPFC, precuneus and TPJ, and whether these different kinds of mentalizing are associated with different patterns of functional connectivity between these regions. Our results indicate that emotion mentalizing and intention mentalizing activate partly distinct subregions of the right and left TPJ that can be spatially separated across participants. These subregions also showed different patterns of functional connectivity with the VMPFC: a more anterior region of the right and left TPJ, which was more strongly activated during emotion mentalizing, showed stronger functional connectivity with the VMPFC, particularly during emotion mentalizing, than a more posterior region that was more strongly activated during intention mentalizing. Critically, this double dissociation became evident only when the fine-scale distribution of activity within activated regions was analysed, and despite the fact that there was also a significant overlap of activity during the two tasks. Our findings provide first evidence that different neural modules might have evolved within the TPJ that show distinct patterns of functional connectivity and might subserve slightly different subfunctions of mentalizing.

Research Highlights

► Distinct subregions of the TPJ are recruited during emotion and intention mentalizing. ► These subregions show different patterns of functional connectivity with the VMPFC. ► Dissociable neural modules in the TPJ might serve distinct subfunctions of mentalizing.

Introduction

Social cognition subsumes a number of cognitive processes that allow humans to act successfully in their social environment. One core component of social cognition is mentalizing, i.e. the process of inferring another person's mental state. Mentalizing is thought to permit individuals to understand other individuals, to anticipate their behaviour and to react appropriately. Functional imaging studies have identified a number of brain regions that are thought to participate in mentalizing. These regions include part of the ventral medial prefrontal cortex (VMPFC), the precuneus, the temporal pole (TP), the posterior superior temporal sulcus (STS), and the temporo-parietal junction (TPJ) (Frith and Frith, 2003, Gallagher and Frith, 2003, Blakemore et al., 2004, Mitchell, 2008, Mitchell, 2009). Some of these regions have been associated with particular sub-functions of mentalizing. For example the STS, a region thought to participate in biological motion processing (e.g. Allison et al., 2000), seems to be primarily activated when people infer intentions from movement (Castelli et al., 2000, Schultz et al., 2004, Saxe et al., 2004, Gobbini et al., 2007). Another example are the temporal poles, which have been associated with memory retrieval and seem to be primarily recruited when people infer mental states based on a person's previous behaviour and attitude (Fletcher et al., 1995, Ruby and Decety, 2004). In contrast, the VMPFC, precuneus and TPJ are activated across a wide range of different experimental tasks (for overviews, see Van Overwalle, 2009; Van Overwalle and Baetens, 2009) and might thus be regarded as a “core network for mentalizing”. However, their exact role in mentalizing is still unclear.

One important question regarding the role of the VMPFC, precuneus and TPJ in mentalizing concerns their selective and universal involvement in mentalizing. In other words, it has been asked whether there are regions in the “core network for mentalizing” that contain specific neural modules that are used selectively and universally for mentalizing.

Early neuroimaging studies on mentalizing provided evidence that the VMPFC might contain neural modules that are selectively used for mentalizing. These studies found that the VMPFC is consistently stronger activated during tasks that involve mentalizing than during matched tasks that do not require mentalizing (Fletcher et al., 1995, Brunet et al., 2000, Castelli et al., 2000, Gallagher et al., 2000, Gallagher et al., 2002). However, at the same time other studies reported that the VMPFC is also activated when participants are asked to monitor their own thoughts (McGuire et al., 1996) or emotions (Lane et al., 1997) or when they are asked to memorize autobiographical events (Maguire and Mummery, 1999). This has been supported by more recent studies that found overlapping activity during mentalizing and self-referential processing in the VMPFC (Saxe et al., 2006, Lombardo et al., 2010). In line with this, repetition suppression has been observed across mentalizing and self-referential processing, providing strong evidence that these two tasks indeed activate similar neuronal modules within the VMPFC (Jenkins et al., 2008).

Evidence regarding the selectivity of the TPJ for mentalizing is more contentious. While some studies report selective activation of the TPJ, particularly the right TPJ, during specific mentalizing tasks (Saxe et al., 2006, Saxe and Powell, 2006, Perner et al., 2006, Sommer et al., 2007, Aichhorn et al., 2009), evidence is now accumulating that the TPJ is also activated by non-social tasks that require attention direction towards unexpected but relevant changes (Decety and Lamm, 2007, Mitchell, 2008). Two recent studies (Mitchell, 2008, Scholz et al., 2009) that have directly compared TPJ activity during mentalizing and re-orienting come to somewhat different conclusions: Both studies report overlapping activity during the two tasks, but only the earlier study by Mitchell (2008) interprets this as evidence that the two tasks activate the same subregion. Employing additional fine-scale spatial analyses, Scholz et al. (2009) provide strong evidence that mentalizing and re-orienting in fact recruit neighbouring, but partly spatially distinct regions.

Concerning the second part of the question, the universal involvement in mentalizing, activation of the VMPFC, precuneus and TPJ has been observed across a wide range of mentalizing studies (see Van Overwalle, 2009 and Van Overwalle and Baeten, 2009). Despite this overlap across studies it is still unclear whether different kinds of mentalizing indeed activate similar neural modules within the VMPFC, precuneus and TPJ. This question appears particularly interesting when considering that Mitchell (2008) and Decety and Lamm (2007) have suggested that mentalizing and re-orienting recruit the same subregion within the TPJ.

Another open question concerns the specific contribution of different nodes of the “core ntework” to mentalizing, and how they interact. Different patterns of activity have been observed across the VMPFC, precuneus and TPJ both in single studies that directly compared different kinds of mentalizing (e.g. Saxe and Powell, 2006, Hynes et al., 2006, Voellm et al., 2006, Gobbini et al., 2007, Sommer et al., 2007) and in a meta analysis (Van Overwalle, 2009), but it is largely unknown how these regions interact during different mentalizing tasks. A recent study found that the VMPFC, precuneus and TPJ show highly overlapping patterns of connectivity with somatosensory, sensorimotor and premotor cortices during both mentalizing and self-referential processing (Lombardo et al., 2010). Surprisingly, however, the authors do not report connectivity within the “core mentalizing network”, that is, between the VMPFC, precuneus and TPJ.

As dysfunctions of the mentalizing networks have been discussed to be at the root of many psychiatric illnesses including autism and schizophrenia (Brüne and Brüne-Cohrs, 2006) a deeper understanding of how the nodes of this network contribute to and interact during specific mentalizing tasks might not only broaden our understanding of the healthy human social brain, but also of its psychiatric dysfunction.

The current study aimed to determine whether different kinds of mentalizing indeed recruit similar neural modules within the mentalizing network, and how these subregions interact during different kinds of mentalizing. Specifically, we compared fine-scale distribution of activity within, and functional connectivity between, regions of the mentalizing network during two different kinds of mentalizing, namely inferring another person's affective state (“emotion mentalizing”) and inferring another person's intention (“intention mentalizing”). Both kinds of mentalizing have previously been directly compared (Hynes et al., 2006, Voellm et al., 2006), but not at the level of fine-scale distribution of activity within activated regions. First, we examined whether these two kinds of mentalizing indeed activate similar subregions within the VMPFC, precuneus and TPJ. For this, we combined voxel-wise analyses of group activation maps and analysis of peaks in individual maps. Second, we investigated the functional connectivity between these regions associated with each of the two mentalizing tasks.

Section snippets

Participants

Twenty-four volunteers (11 women and 13 men; age range 22–28 years, mean 23.6 years) with no record of neurological or psychiatric disorders participated in the study. All participants were right-handed, native German speakers and had normal or corrected-to-normal vision. All participants gave informed written consent before scanning, and the study was approved by the local Ethics committee.

Experimental design and stimuli

We used a simple experimental paradigm that had previously been used to study neural correlates of emotion

Task performance

Behavioural data of two participants were lost because of recording errors. Of the remaining participants (N = 22) more than half responded on each trial and only one missed to respond more than once (twice). In each and every participant overall performance was above chance (i.e. p < .05, minimum hit rate 27 out of 40 trials, Table 1). Eighty percent of all participants performed better than chance in each of the four tasks (i.e. p < .05, minimum hit rate 8 out of 10 trials).

Participants made

Discussion

The current study examined neural activity in the right and left TPJ, precuneus and VMPFC. Specifically, we examined the fine-scale distribution of activity within, and functional connectivity between, regions of this network during two different kinds of mentalizing, emotion mentalizing and intention mentalizing. Like previous studies we found that the right and left TPJ and the precuneus were significantly stronger activated when participants were required to infer a character's mental state

Conclusions

The role of the VMPFC, precuneus and, particular, the TPJ in mentalizing are subject of an ongoing debate. By employing a number of advanced analysis techniques the current study provides evidence for the existence of two partly distinct subregions within the TPJ that show distinct patterns of functional connectivity with the VMPFC and precuneus. This provides evidence that different subregions might have evolved within the TPJ that subserve slightly different subfunctions of mentalizing.

Based

Acknowledgments

This work was partly supported by a FORTÜNE grant of the University of Tübingen, by the Deutsche Forschungsgemeinschaft (German Research Association, Grant AN 755/2-1), and by the Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research, Grant 01GW0752). We thank Birgit Voellm for generously providing the stimuli, and Thomas Ethofer for comments on an earlier version of the manuscript.

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