Elsevier

NeuroImage

Volume 56, Issue 3, 1 June 2011, Pages 1705-1713
NeuroImage

Common and distinct neural networks for false-belief reasoning and inhibitory control

https://doi.org/10.1016/j.neuroimage.2010.12.052Get rights and content

Abstract

Ample behavioral evidence has shown that the ability to attribute false beliefs as part of a Theory of Mind (ToM) and the ability to inhibit a prepotent response are strongly correlated in both children and adults. Frequently reported areas associated with both processes are the right temporo-parietal junction (TPJ) and the medial prefrontal cortex (MPFC). Nevertheless, the exact nature of the relationship between belief-reasoning and inhibitory control at the neural level remains unclear.

A functional magnetic resonance imaging (fMRI) study was conducted to investigate the neural correlates of belief-reasoning and inhibitory control in a within-subjects design using virtually identical visual stimuli. A false-belief task was used to investigate belief-attribution. The neural correlates of response inhibition were measured using a Go/No-Go task.

Besides distinct activation for belief-reasoning and inhibitory control, the results also showed a substantial overlap for both processes in the right superior dorsal MPFC, the right TPJ, the dorsal part of the left TPJ, and lateral prefrontal areas. These findings suggest that the previously described behavioral link between belief attribution and inhibitory control may be explained by a common recruitment of brain areas related to domain-general cognitive processes. Also, the results indicate that neither the right TPJ nor MPFC is specific to the attribution of false beliefs.

Research Highlights

►Bilateral TPJ and right MPFC are active during inhibition and belief-reasoning. ►This common activity may explain a frequently described behavioral connection. ►Reorienting of attention may underlie both processes. ►Neither the MPFC nor the right TPJ may be specific to the attribution of beliefs.

Introduction

The neural underpinnings of social cognition have become a growing area of research in recent years. One crucial aspect of social cognition is the understanding of mental states that has been given the term “mentalizing” or “Theory of Mind” (ToM). This ability enables us to attribute mental states such as intentions, desires and beliefs to the self and others and allows us to predict and explain our own and others' behavior.

In cognitive development it has been shown that a ToM emerges within the first years of life with an understanding of desires preceding an understanding of beliefs. The ability to differentiate beliefs from reality is the cornerstone of a Theory of Mind and evolves between the ages of 3 1/2 and 4 1/2 years (e.g., Baron-Cohen et al., 1985, Wellman et al., 2001). Developmental progress in false-belief understanding in young children concurs with fundamental advances in children's executive functioning (EF). A meta-analysis by Perner and Lang (1999) showed a strong effect size of d = 1.08 in 11 studies investigating correlations between EF and false-belief reasoning. These studies also show that among EF, inhibitory control performance shows the strongest correlations with false-belief reasoning. Other abilities such as working memory, general intelligence or language skills are correlated with belief-reasoning to a much lesser extent. Furthermore, the strong relationship between inhibitory control and belief-reasoning persists even when age and general intelligence are controlled for (Carlson et al., 2002, Perner and Lang, 1999, Sabbagh et al., 2006). Empirical evidence from training studies indicates that the correlation between ToM and EF development is not spurious. In an ingenious experiment, Kloo and Perner (2003) were able to show that training in the Dimensional Card Sorting Task, a measure of inhibitory control, improved results in false-belief performance and vice versa.

A close relationship between false-belief reasoning and inhibitory control has not only been revealed on a behavioral level but also on a neural level.

Studies investigating inhibitory control by using response inhibition tasks such as the Go/No-go task have revealed a largely right-hemispheric fronto-subthalamic network consisting of the middle and inferior frontal gyrus (IFG), subthalamic-nucleus (STN) and dorso-medial frontal gyrus (e.g., Aron, 2007, Chambers et al., 2007, Garavan et al., 2006). Besides this neural circuit which may exert a global inhibitory response, several studies have also revealed activity related to inhibitory control in areas such as inferior parietal lobe, superior occipital gyrus, and the bilateral TPJ (Buchsbaum et al., 2005, Simmonds et al., 2008). The temporo-parietal junction and the dorsal medial prefrontal cortex (dMPFC) also seem to play an important role in false-belief reasoning (e.g. Aichhorn et al., 2009, Fletcher et al., 1995, Gallagher et al., 2000, Gobbini et al., 2007, Grezes et al., 2004, Perner et al., 2006, Saxe and Kanwisher, 2003, Sommer et al., 2007, Vogeley et al., 2001).

Taken together, results from studies investigating false-belief reasoning and studies investigating inhibitory control indicate that there may be brain areas such as the right TPJ and parts of the MPFC that are engaged in both processes. In addition to behavioral findings, which show a strong correlation between performance in false-belief understanding and performance in tasks involving inhibitory control processes, this overlap may serve as another indicator that both processes are indeed closely related. However, the fact that a common brain region is found in studies investigating different cognitive concepts is not sufficient to make reliable inferences about that specific region. Studies are difficult to compare due to crucial factors such as differing subjects, differing imaging methods and scanners, differing paradigms, differing analyses, and differing stimuli.

Three imaging studies have so far attempted to investigate belief-reasoning and inhibitory control within a single within-subjects paradigm (Mitchell, 2008, Saxe et al., 2006, Scholz et al., 2009). These studies focused especially on the role of the right TPJ in both processes.

Saxe et al. (2006) presented subjects with an unexpected-transfer false-belief task and an algorithm task which required subjects to apply one of two algorithms to the same stimulus material as used for the false-belief task. Common neural activity for the algorithm task and belief-reasoning was revealed in MPFC, bilateral parietal sulcus, the anterior cingulate cortex (ACC) and the left TPJ. Only the right TPJ showed significantly higher activation in the false-belief condition compared to the algorithm task. Based on the overlap between the algorithm and the false-belief task, the authors claim that belief-reasoning may recruit domain-general resources also implicated in other tasks including executive demands. According to the authors, activity of the right TPJ, which was exclusively correlated with false-belief reasoning, may indicate activity of domain-specific cognitive processes.

Based on the observation that activity of the right TPJ is not only observed in studies investigating belief attribution but also when subjects are required to break their current attentional set to reorient to task-relevant stimuli (Corbetta et al., 2000, Corbetta and Shulman, 2002, Kincade et al., 2005, Serences et al., 2005), Mitchell (2008) examined the role of the right TPJ in both processes in more detail. A study was therefore conducted that investigated both attentional reorienting and belief-reasoning in a single experimental session. The “Posner cueing task” was used to study attentional reorienting. To study belief-reasoning, a false-belief condition was compared to a false-photo condition. Belief-reasoning was associated with activity in the right TPJ, MPFC, and the precuneus. Attentional reorienting revealed activity only in the same right TPJ region as belief-reasoning. Based on these results, Mitchell argues that the right TPJ is not specific to ToM reasoning but that both attentional reorienting and belief-reasoning rely on common processes that need to be further investigated.

This finding was further investigated in a recent study conducted by Scholz et al. (2009) This study investigated belief-reasoning and attentional reorienting using the belief-reasoning task and the attentional reorienting task utilized in Mitchell's study described above (Mitchell, 2008). Of the 21 subjects investigated, 11 showed activity in the right TPJ for both attentional reorienting and belief-reasoning. The subsequent ROI-analysis focused only on the right TPJ region of these subjects. This analysis revealed only a minor spatial overlap for attentional reorienting and belief-reasoning. In these 11 subjects, the average peak for attentional reorienting in the right TPJ was 9 mm superior to the corresponding average peak for belief-attribution. Based on their findings, Scholz et al. (2009) argue that belief-reasoning and inhibitory control recruit neighbouring but distinct regions within the right TPJ.

To conclude, developmental studies using different tasks show a strong correlation between belief-reasoning and executive tasks involving inhibitory control (Carlson and Moses, 2001, Flynn, 2007, Kloo and Perner, 2003). Some imaging studies show that the right inferior parietal lobe/right TPJ may be engaged during response inhibition (Buchsbaum et al., 2005, Hester et al., 2004, Simmonds et al., 2008) and also during false-belief attribution (Saxe and Kanwisher, 2003, Sommer et al., 2007), suggesting that this area may support processes necessary in both functions. However, the extent of the overlap in the rTPJ region remains disputed (Mitchell, 2008, Scholz et al., 2009).

The exact role of the various parts of the MPFC in both processes has not been studied as thoroughly and remains vague. Of the three studies attempting to investigate common neural correlates of belief-reasoning and inhibitory control by means of a within-subjects design, only two may have actually tapped inhibitory control (Mitchell, 2008, Scholz et al., 2009). However, both studies used paradigms that differed largely in terms of visual stimulation (stories versus attentional cueing task) and focused primarily on the right TPJ, although previous studies suggest that the dorsal MPFC may also be centrally involved in false-belief reasoning and inhibitory control alike (e.g., Frith and Frith, 2003, Simmonds et al., 2008).

Here we carried out a high-field fMRI study that uses a simple Go/No-go task to study inhibitory control. We also used a well-established belief-reasoning task (“Sally-Anne paradigm”; Baron-Cohen et al., 1985, Wimmer and Perner, 1983) to identify the neural correlates of false-belief reasoning. All subjects had to complete both tasks in one session, the visual stimuli used in both tasks were virtually identical, and both tasks were non-verbal. Functional data were introduced into a whole brain analysis, thus yielding conclusions not only about the right TPJ but also about the role of the MPFC and other areas possibly implicated in both cognitive concepts. By this approach we attempt to investigate the relationship between false-belief reasoning and inhibitory control on a neural level and to further clarify the role of the dMPFC and rTPJ in both processes.

Section snippets

Subjects

Twelve right-handed subjects (mean age 23.7 years, range 23–24; 5 male) with no history of neurological or psychiatric problems participated in the study. All participants gave their written informed consent. The procedures followed were in accordance with the standards of the University Medical Center Regensburg ethics committee.

Belief-reasoning task

We presented non-verbal cartoon stories modeled according to the Sally-Anne paradigm (Baron-Cohen et al., 1985). A total of 10 different story plots (consisting of

Behavioral results

Subject gave a correct response in 95.5% (SD = 3.3%) of the false-belief trials and in 96.4% (SD = 2.1%) of the true-belief trials. In the Go condition, average accuracy was 96.3% (SD = 2.1%). In the No-go condition, subjects showed a mean accuracy (i.e. refraining from pressing a button) of 89.8% (SD = 12.0%). There was no statistically significant difference in accuracy between false- and true-belief conditions (t (11) = .979; p = .349, n.s.) or between the Go and No-go conditions (t (11) = 1.997; p = .071,

Discussion

Developmental studies indicate that in young children the developmental progress in understanding false beliefs is strongly correlated with performance in inhibitory control tasks (e.g., Carlson et al., 2002, Perner and Lang, 1999, Sabbagh et al., 2006). Additionally, imaging studies investigating belief reasoning (e.g., Aichhorn et al., 2009, Perner et al., 2006, Saxe and Kanwisher, 2003, Sommer et al., 2007) and studies investigating inhibitory control (Aron, 2007, Buchsbaum et al., 2005,

Acknowledgments

We thank Sarah-Jayne Blakemore for helpful comments on an earlier draft of this article. We are also grateful to Philipp Holter for his help with subject recruitment and data acquisition.

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