Elsevier

NeuroImage

Volume 58, Issue 2, 15 September 2011, Pages 640-646
NeuroImage

Evaluating the roles of the inferior frontal gyrus and superior parietal lobule in deductive reasoning: An rTMS study

https://doi.org/10.1016/j.neuroimage.2011.06.076Get rights and content

Abstract

This study used off-line repetitive transcranial magnetic stimulation (rTMS) to examine the roles of the superior parietal lobule (SPL) and inferior frontal gyrus (IFG) in a deductive reasoning task. Subjects performed a categorical syllogistic reasoning task involving congruent, incongruent, and abstract trials. Twenty four subjects received magnetic stimulation to the SPL region prior to the task. In the other 24 subjects, TMS was administered to the IFG region before the task. Stimulation lasted for 10 min, with an inter-pulse frequency of 1 Hz. We found that bilateral SPL (Brodmann area (BA) 7) stimulation disrupted performance on abstract and incongruent reasoning. Left IFG (BA 45) stimulation impaired congruent reasoning performance while paradoxically facilitating incongruent reasoning performance. This resulted in the elimination of the belief-bias. In contrast, right IFG stimulation only impaired incongruent reasoning performance, thus enhancing the belief-bias effect. These findings are largely consistent with the dual-process theory of reasoning, which proposes the existence of two different human reasoning systems: a belief-based heuristic system; and a logic-based analytic system. The present findings suggest that the left language-related IFG (BA 45) may correspond to the heuristic system, while bilateral SPL may underlie the analytic system. The right IFG may play a role in blocking the belief-based heuristic system for solving incongruent reasoning trials. This study could offer an insight about functional roles of distributed brain systems in human deductive reasoning by utilizing the rTMS approach.

Highlights

► TMS was administered on SPL and IFG regions during a deductive reasoning task. ► Bilateral SPL stimulation disrupted abstract and incongruent reasoning performance. ► Left IFG stimulation impaired congruent reasoning performance. ► Right IFG stimulation only impaired incongruent reasoning performance

Introduction

Deductive reasoning is the process of drawing valid conclusions from a given set of premises. Many theories have described the neuro-cognitive processes of human deductive reasoning. Among these, the mental model theory proposes that cognitive processes of constructing and manipulating spatially organized mental models are essential for deductive reasoning (Johnson-Laird, 1994, Johnson-Laird, 2001, Johnson-Larid, 2010). This predicts that the neural substrates of spatial processing (e.g., parietal cortex) are critical for human reasoning processes. Other theories have emphasized the role of language processing in deductive reasoning (e.g., Polk and Newell, 1995), predicting that the neural mechanisms of linguistic processing (e.g., left frontotemporal cortex) underwrite human reasoning processes.

Goel et al. (2000) demonstrated that the presence or absence of content words in the argument is an important factor in determining which brain mechanism is engaged. They found that the parietal lobes, including the superior parietal lobules (SPLs), were activated bilaterally during abstract reasoning trials where semantic content was lacking (e.g., “All P are B”), consistent with the mental model theory (but see Prado et al., 2010, Reverberi et al., 2010, as studies showing the absence of SPL activation for abstract reasoning). In contrast, language-related brain regions, such as left-lateralized inferior frontal gyrus (IFG) and superior temporal lobe, were activated for contentful materials (e.g., “All dogs are mammals”), although the left IFG was also activated by abstract reasoning (Monti et al., 2007, Monti et al., 2009, Reverberi et al., 2007, Reverberi et al., 2010).

In addition, recent studies of the belief-bias effect have indicated that the neural correlates of content reasoning vary depending on the consistency between logical validity and belief in the conclusion (De Neys et al., 2008, Goel and Dolan, 2003, Tsujii and Watanabe, 2009, Tsujii and Watanabe, 2010). The belief-bias effect refers to the tendency for subjects to be erroneously biased when logical conclusions are incongruent with beliefs about the world (Evans, 2003). Thus, the belief-bias of semantic processing facilitates logical responses on congruent trials where the logical conclusion is consistent with beliefs about the world (valid–believable, invalid–unbelievable), while inhibiting logically correct responses on incongruent trials (valid–unbelievable, invalid–believable). Recent papers have suggested that activity in the right IFG is associated with incongruent reasoning performance, while left IFG activity (Brodmann area (BA) 45) is associated with congruent reasoning performance (De Neys et al., 2008, Goel and Dolan, 2003, Tsujii and Watanabe, 2009, Tsujii and Watanabe, 2010, Tsujii et al., 2010a, Tsujii et al., 2010b).

Relevant to these neuroimaging findings, the dual-process theory of reasoning proposes that human reasoning could be accomplished by flexible interactions of two different systems (Evans, 2008, Goel, 2007). The first system, often called the heuristic system, relies on prior knowledge and belief. The second, or analytic, system engages in reasoning according to logical standards. The default heuristic system is assumed to operate rapidly and automatically, while the analytic system is believed to be slow and highly demanding of computational resources (De Neys, 2006a, De Neys, 2006b, Tsujii and Watanabe, 2009, Tsujii and Watanabe, 2010). The analytic system is necessary for solving abstract and incongruent reasoning, while the heuristic system is sufficient for performing congruent reasoning.

According to this dual process theory, the left frontotemporal pathway (e.g., left IFG) corresponds to the belief-based heuristic system, whereas the bilateral parietal pathway (e.g., SPL) corresponds to the logic-based analytic system (Goel, 2007). Right IFG may play a functional role as a switching mechanism to inhibit the default heuristic system and thus enable analytic system activity (Tsujii and Watanabe, 2009, Tsujii and Watanabe, 2010). These considerations, although interesting, have only been supported by neuroimaging studies, which can only examine correlations between cortical areas and a type of behavior. The aim of the present study was to examine the roles of the SPL and IFG in a deductive reasoning task using repetitive transcranial magnetic stimulation (rTMS) to establish causal relationships between brain and behavior more directly.

Another recent study examined neural correlates of the deductive reasoning process using an off-line rTMS method (Tsujii et al., 2010a). They adopted an approach in which low-frequency rTMS is delivered to a specific brain area over several minutes to disrupt normal functioning transiently after stimulation (for a review, see Robertson et al., 2003). Tsujii et al. (2010a) examined the role of the IFG in belief-bias reasoning using this temporal lesion approach and found that subjects in whom the right IFG was impaired by rTMS could not inhibit irrelevant semantic processing in incongruent reasoning, resulting in an enhanced belief-bias effect. In contrast, left IFG stimulation significantly impaired congruent reasoning performance while paradoxically facilitating incongruent reasoning performance. Left IFG stimulation removed interference from irrelevant semantic processing, resulting in elimination of the belief-bias effect.

Two shortcomings of this pioneering research must be mentioned: they only examined the region around the IFG; and they did not examine abstract reasoning where semantic-content was lacking. The present study examined the roles of the SPL and IFG in a deductive reasoning task using the same off-line rTMS approach. The task included congruent, incongruent, and abstract reasoning trials (Fig. 1), and our study addressed how these three types of reasoning performance were affected by magnetic stimulation of the SPL and IFG.

Section snippets

Subjects

Twenty four subjects were assigned to the SPL group (13 women, 11 men; 23 were right-handed) and the other 24 were assigned to the IFG group (12 women, 12 men; 22 were right-handed). Mean age was 21.33 ± 1.88 years for the SPL group and 21.54 ± 1.93 years for the IFG group. None had received any formal training in logic. The study was conducted in accordance with the principles of the Declaration of Helsinki and the guidelines from the International Workshop on the Safety of Repetitive Transcranial

Materials

We prepared 144 contentful and 72 no-content abstract syllogisms (Fig. 1). Contentful syllogisms included sentences like “All pigeons are birds”, while no-content abstract sentences were of the form “All S are Z”. For contentful syllogisms, a combination of logical validity and believability yielded two types of trials: 72 congruent (36 valid-believable, 36 invalid-unbelievable) and 72 incongruent (36 valid-unbelievable, 36 invalid-believable). The believability of the conclusion was rated by

SPL

Fig. 2 summarizes accuracy scores from congruent, incongruent, and abstract reasoning trials after the SPL regions were stimulated. Two-way ANOVA revealed a significant hemisphere × reasoning type interaction (F(4,92) = 2.51, p < .05, ηp2 = .10), suggesting that significant hemisphere effects were observed for abstract trials (F(2138) = 6.62, p < .01, ηp2 = .10), and for incongruent trials (F(2138) = 6.18, p < .01, ηp2 = .09), but not for congruent trials (F(2138) = .05, p = .95, ηp2 = .00).

For abstract reasoning

Discussion

The present study examined the role of the SPL and IFG in a deductive reasoning task (Robertson et al., 2003). The rTMS parameters used here are known to transiently disrupt the activity of targeted brain regions in a variety of tasks (Hilgetag et al., 2001, Kosslyn et al., 1999, Miller et al., 2008, Robertson et al., 2003). Subjects performed a categorical syllogistic reasoning task which included congruent, incongruent, and abstract trials. Here we discuss how these three types of reasoning

Conclusions

This study examined the roles of the SPL and IFG in a deductive reasoning task using an off-line rTMS method. The findings are largely consistent with the dual-process theory of reasoning, which proposes the existence of two different reasoning systems in humans: a belief-based heuristic system; and a logic-based analytic system. In the present study, the left IFG appears to correspond to the heuristic system, while bilateral SPLs are part of the analytic system. The right IFG may play a role

Acknowledgments

Funding for this study was provided by the fund of Global COE Program and Grant-in-Aid for Young Scientists (B) from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan. In addition, manuscript preparation was supported by funding from the Center of Developmental Education and Research (CODER) of Japan and by the fund for Japan Science and Technology Agency (JST), under the Strategic Promotion of Innovative Research and Development Program.

References (58)

  • V. Goel et al.

    A role for right ventrolateral prefrontal cortex in reasoning about indeterminate relations

    Neuropsychologia

    (2009)
  • M. Hamidi et al.

    Evaluating the role of prefrontal and parietal cortices in memory-guided response with repetitive transcranial magnetic stimulation

    Neuropsychologia

    (2009)
  • M. Hamidi et al.

    Evaluating frontal and parietal contributions to spatial working memory with repetitive transcranial magnetic stimulation

    Brain Res.

    (2008)
  • P.N. Johnson-Laird

    Mental models and probabilistic thinking

    Cognition

    (1994)
  • P.N. Johnson-Laird

    Mental models and deduction

    Trends Cogn Sci.

    (2001)
  • M. Knauff et al.

    Spatial imagery in deductive reasoning: a functional MRI study

    Cogn. Brain Res.

    (2002)
  • B.T. Miller et al.

    Prefrontal and parietal contributions to refreshing: an rTMS study

    NeuroImage

    (2008)
  • M.M. Monti et al.

    Functional neuroanatomy of deductive inference: a language-independent distributed network

    NeuroImage

    (2007)
  • R.L. Newman et al.

    Modulation of brain regions involved in word recognition by homophonous stimuli: an fMRI study

    Brain Res.

    (2011)
  • J.M. Olichney et al.

    fMRI responses to words repeated in a congruous semantic context are abnormal in mild Alzheimer's disease

    Neuropsychologia

    (2010)
  • J. Prado et al.

    Recomposing a fragmented literature: how conditional and relational arguments engage different neural systems for deductive reasoning

    NeuroImage

    (2010)
  • C. Reverberi et al.

    Neural basis of generation of conclusions in elementary deduction

    NeuroImage

    (2007)
  • A.T. Sack et al.

    The experimental combination of rTMS and fMRI reveals the functional relevance of parietal cortex for visuospatial functions

    Cogn. Brain Res.

    (2002)
  • N. Shinoura et al.

    Damage to the right superior longitudinal fasciculus in the inferior parietal lobe plays a role in spatial neglect

    Neuropsychologia

    (2009)
  • R. Stavy et al.

    Intuitive interference in quantitative reasoning

    Brain Res.

    (2006)
  • S. Takahama et al.

    Neural basis for dynamic updating of object representation in visual working memory

    NeuroImage

    (2010)
  • P.P. Thakral et al.

    The role of parietal cortex during sustained visual spatial attention

    Brain Res.

    (2009)
  • C.K. Thompson et al.

    Neural plasticity and treatment-induced recovery of sentence processing in agrammatism

    Neuropsychologia

    (2010)
  • T. Tsujii et al.

    The role of inferior frontal cortex in belief-bias reasoning: an rTMS study

    Neuropsychologia

    (2010)
  • Cited by (0)

    View full text