Elsevier

NeuroImage

Volume 57, Issue 4, 15 August 2011, Pages 1624-1629
NeuroImage

Ventromedial prefrontal volume predicts understanding of others and social network size

https://doi.org/10.1016/j.neuroimage.2011.05.030Get rights and content

Abstract

Cognitive abilities such as Theory of Mind (ToM), and more generally mentalizing competences, are central to human sociality. Neuroimaging has associated these abilities with specific brain regions including temporo-parietal junction, superior temporal sulcus, frontal pole, and ventromedial prefrontal cortex. Previous studies have shown both that mentalizing competence, indexed as the ability to correctly understand others' belief states, is associated with social network size and that social group size is correlated with frontal lobe volume across primate species (the social brain hypothesis). Given this, we predicted that both mentalizing competences and the number of social relationships a person can maintain simultaneously will be a function of gray matter volume in these regions associated with conventional Theory of Mind. We used voxel-based morphometry of Magnetic Resonance Images (MRIs) to test this hypothesis in humans. Specifically, we regressed individuals' mentalizing competences and social network sizes against gray matter volume. This revealed that gray matter volume in bilateral posterior frontal pole and left temporoparietal junction and superior temporal sucus varies parametrically with mentalizing competence. Furthermore, gray matter volume in the medial orbitofrontal cortex and the ventral portion of medial frontal gyrus, varied parametrically with both mentalizing competence and social network size, demonstrating a shared neural basis for these very different facets of sociality. These findings provide the first fine-grained anatomical support for the social brain hypothesis. As such, they have important implications for our understanding of the constraints limiting social cognition and social network size in humans, as well as for our understanding of how such abilities evolved across primates.

Research highlights

►We regressed gray matter volume in human brains against two behavioral measures. ►These were high-level intentionality ability and social network size. ►In temporoparietal junction, gray matter volume predicted intentionality ability. ►In the ventromedial prefrontal cortex, gray matter volume predicted both measures.

Introduction

The ability to infer the mental states of other individuals, commonly known as Theory of Mind, is widely accepted as a crucial cognitive basis for sociality in humans (Frith and Frith, 2003, Leslie, 1987, Leslie, 1994, Wimmer and Perner, 1983). The neural basis of Theory of Mind (ToM) has received considerable attention in recent years and a number of core brain structures have been implicated in solving false belief tasks, the generally accepted benchmark for Theory of Mind (Wimmer and Perner, 1983). These include regions of the medial prefrontal cortex (mPFC) (Gallagher and Frith, 2003), temporo-parietal junction (TPJ) (Saxe and Kanwisher, 2003), superior temporal sulcus (STS) (Frith and Frith, 2003), and frontal pole (FP) (Decety and Lamm, 2007, Gallagher et al., 2000, Saxe, 2006, Saxe et al., 2004, Spreng et al., 2009). ToM is functionally equivalent to second order intentionality (“I believe that you suppose…”), and is acquired by the age of about 4–5 years (Astington, 1993, Leslie, 1987). As such, ToM poses no challenges for normal adult humans, who are usually able to cope with mentalizing tasks up to 4th or 5th order intentionality (Kinderman et al., 1998, Stiller and Dunbar, 2007), with only rare individuals performing well at 6th order. Performance at these higher orders of intentionality has recently been shown to predict prefrontal volume (Powell et al. 2010). However, this work used large regions of interest encompassing the entire dorsal and orbital prefrontal cortices and thus provides little information as to the specific subregions in which these quantitative differences in neurobiology may occur (Dunbar, 2009, Dunbar, 2011).

At the other end of the scale, the well-documented cross-species positive correlation between social group size and neocortex volume in primates, otherwise known as the social brain hypothesis (Dunbar, 1998, Dunbar and Shultz, 2007, Pérez-Barbería et al., 2007, Shultz and Dunbar, 2007, Shultz and Dunbar, 2010), implies that the social cognitive skills underpinning this relationship must have some kind of neurophysiological representation (Shultz and Dunbar, 2010). To date, it has proved difficult to integrate the social brain hypothesis with any underlying cognitive and neurophysiological substrates, and this weakness has attracted some criticism (Healy and Rowe, 2007). Nonetheless, at least in humans, individual competences on high order intentionality tasks correlate positively with the size of personal social networks (Stiller and Dunbar, 2007), and there is strong circumstantial evidence to suggest that social cognitive competences might correlate positively with some aspects of brain size (notably frontal lobe volume) across primate species (Dunbar, 2003).

These observations raise two obvious questions. First, do those who can compute higher levels of intentionality have access to greater processing power in the brain networks required for mentalizing? In other words, is there a quantitative relationship between the level of intentionality at which a healthy individual can habitually work and the volume of neural matter in the classic Theory of Mind regions that the individual can bring to bear on the problem? Second, do either of these correlate with the size of the person's social network (i.e. the number of individuals they list as personal friends)?

Here, we used voxel-based morphometry (VBM) of high resolution magnetic resonance imaging (MRI) brain scans to test these hypotheses. On the basis of several recent meta-analyses (Frith and Frith, 2003, Spreng et al., 2009, Van Overwalle, 2009), we identified four principal regions of the brain that are commonly associated with conventional Theory of Mind: mPFC, TPJ, STS, and FP. We first tested for a quantitative relationship between individuals' social cognitive competences (indexed as the intentionality fail level) and the volume of gray matter in these four regions. We then tested for a relationship between the size of each individual's personal social network and gray matter volume in these same regions. Finally, we tested for areas correlating with both high order intentionality abilities and social network size. We chose the fine-grained analysis offered by VBM in order to determine whether or not those regions known to be involved in Theory of Mind (i.e. conventional second order intentionality) exhibit a parametric relationship with individual differences in mentalizing competences (higher order intentional competences) and/or network size. Such a relationship would imply that higher order intentionality is computationally more demanding, and that social competence is linked to neural recruitment within quite tightly defined brain regions. Since we aimed to test the role of information processing, rather than information exchange between processing units, we focus explicitly on gray matter volume rather than white matter volume.

Section snippets

Materials and methods

We sampled 45 individuals, 26 females and 19 males aged between 18 and 50 years (mean 25.6 years for both females and males, SEM 2 and 1 years respectively). We used subjects who: (1) reported no history of neurological problems, (2) were native English speakers, and (3) had not previously been involved in research on Theory of Mind. All subjects gave written fully informed consent of their willingness to participate. The study was approved by the appropriate local ethics committee.

We determined

Results

The mean number of social contacts reported was 36.7 ± SEM 2.7. As found by Stiller and Dunbar (2007), there was a significant Pearson correlation (r = 0.254, N = 45, p < 0.05) between social network size and intentionality fail point. In order to control for the potential contribution of memory abilities, we also ran this analysis as a partial correlation with memory fail point partialed out. This showed that the relationship between network size and intentionality remained significant and was, if

Discussion

Our data support a previous finding that there is a significant correlation between the size of an individual's social network and their level of social cognitive competence (indexed as their ability to correctly understand others' belief states). We extend this by showing that these measures predict the gray matter volume of brain regions used in mentalizing and emotional processing. The quantitative relationship that we demonstrate between the levels of intentionality at which an individual

Acknowledgments

This research was funded by the University of Liverpool, and MRI scans were paid for by a Wellcome VIP award to PAL. PAL is currently supported by the University of Manchester, and by a BBSRC New Investigator Award [BB/F003048/1] to PAL. RIMD is supported by the University of Oxford and the British Academy Centenary Research Project and, at the time the experiments were carried out, by a British Academy Research Professorship. We are grateful to the staff at MARIARC for technical support, to

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