Elsevier

NeuroImage

Volume 41, Issue 3, 1 July 2008, Pages 1168-1176
NeuroImage

Brain spontaneous functional connectivity and intelligence

https://doi.org/10.1016/j.neuroimage.2008.02.036Get rights and content

Abstract

Many functional imaging studies have been performed to explore the neural basis of intelligence by detecting brain activity changes induced by intelligence-related tasks, such as reasoning or working memory. However, little is known about whether the spontaneous brain activity at rest is relevant to the differences in intelligence. Here, 59 healthy adult subjects (Wechsler Adult Intelligence Scale score, 90ā€“138) were studied with resting state fMRI. We took the bilateral dorsolateral prefrontal cortices (DLPFC) as the seed regions and investigated the correlations across subjects between individual intelligence scores and the strength of the functional connectivity (FC) between the seed regions and other brain regions. We found that the brain regions in which the strength of the FC significantly correlated with intelligence scores were distributed in the frontal, parietal, occipital and limbic lobes. Stepwise linear regression analysis also revealed that the FCs within the frontal lobe and between the frontal and posterior brain regions were both important predictive factors for the differences in intelligence. These findings support a network view of intelligence, as suggested in previous studies. More importantly, our findings suggest that brain activity may be relevant to the differences in intelligence even in the resting state and in the absence of an explicit cognitive demand. This could provide a new perspective for understanding the neural basis of intelligence.

Introduction

The neural basis of intelligence has been investigated for many years. Researchers have found, using various neuroimaging paradigms that have ranged from the structural (Colom et al., 2006, Gong et al., 2005, Haier et al., 2004, Shaw et al., 2006) to functional imaging (Boivin et al., 1992, Esposito et al., 1999, Fangmeier et al., 2006, Gray et al., 2003, Haier, 2003, Haier et al., 1988, Lee et al., 2006, Prabhakaran et al., 1997), that both frontal and posterior brain regions are associated with intelligence. As a result, it is widely believed that a brain network characterized by interactions between multiple brain regions is likely to be the neural basis of intelligence.

Most of the brain's energy consumption is devoted to ongoing metabolic activity, namely spontaneous neuronal activity not clearly associated with any particular stimulus or task (Raichle, 2006). Although the neurobiological implications of the spontaneous neuronal activity are not very clear, researchers have found that spontaneous fluctuations in the blood oxygenation level-dependent (BOLD) signal are coherent within a variety of brain systems, such as the somatomotor (Biswal et al., 1995); visual (Lowe et al., 1998); language processing (Hampson et al., 2002); auditory (van de Ven et al., 2004); attention (Fox et al., 2006), memory (Vincent et al., 2006) and default mode networks (Greicius et al., 2003). Moreover, a recent study reported that coherent BOLD spontaneous fluctuations were present even in anaesthetized monkey brains, which indicates that the functional architecture of the brain may be intrinsic, rather than limited to any particular stimulus (Vincent et al., 2007). Previous functional studies (for review, see Jung and Haier, (2007)) have strongly shown that the brain activity associated with a specific cognitive task was distinct among subjects with different levels of intelligence. This raises the question whether the spontaneous brain activity at rest, that is, without any particular task, is related to individual differences in intelligence.

Functional connectivity (FC), which studies temporal correlations between BOLD signals in different brain regions, has been widely used in fMRI studies. These temporal correlations suggest direct or indirect interactions between brain regions (Friston et al., 1993). The behavioral significance of BOLD FC has recently been investigated in studies not only associated with specific task (Hampson et al., 2006b, He et al., 2007) but also at rest (Hampson et al., 2006a, Liu et al., 2007, Seeley et al., 2007). The connectivity-behavior analysis is a technology for analysis of the correlations between the strength of FC and behavioral performance (Hampson et al., 2006b). The present study investigates the correlations between individual intelligence scores and the strength of the FC at rest.

The lateral prefrontal cortex has been found to be one of the most important brain regions supporting intelligent behavior (Gray and Thompson, 2004). In the present study, we took the bilateral dorsolateral prefrontal cortices (left and right DLPFC) as seed regions and separately measured the interregional FC between these seed regions and each voxel that we identified in all parts of the brain. Then we correlated the Wechsler full-scale intelligence quotient (FSIQ) scores with the strength of FC across subjects to search for the brain regions in which the strength of FC significantly correlated with FSIQ scores separately in the composite functional connectivity map and throughout the entire brain. Finally, stepwise linear regression was performed to predict FSIQ scores with the FC obtained from the searches.

Section snippets

Subjects

Fifty-nine healthy right-handed subjects were included in this study. All subjects (29 males and 30 females; mean ageĀ =Ā 24.6Ā years, SDĀ =Ā 3.5Ā years, rangeĀ =Ā 18.5ā€“33.3Ā years) were recruited by advertisement. All subjects gave written informed consent, and this study was approved by the ethical committee of Xuanwu Hospital of Capital Medical University.

Intelligence testing

In the present study, the FSIQ score was used to assess individual intelligence using the Chinese Revised Wechsler Adult Intelligence Scale (WAIS-RC),

Results

The composite functional connectivity maps for the left and right seed regions are shown in Fig. S1 in the Supplementary materials. As shown in Fig. S1, positive correlations were apparent in the bilateral frontal lobe and the superior parietal lobe, while negative correlations were apparent in the anterior and posterior cingulate cortices and the angular gyrus. These results were consistent with those reported in previous studies (Fox et al., 2005, Greicius et al., 2003).

Results from the

Discussion

To our knowledge, this is the first study to investigate the relationship between spontaneous BOLD signal fluctuations and intelligence differences. A prominent difference between the present study and previous functional studies on the neural basis of intelligence was that the present study was conducted at rest and in the absence of any explicit memory, reasoning or problem solving demand. Using connectivity-behavior analysis, we found that the strength of some specific FCs was significantly

Acknowledgments

This work was partially supported by the Natural Science Foundation of China, Grant Nos. 60675033, 30425004, and 30730035, the National Key Basic Research and Development Program (973), Grant No. 2004CB318107, and Beijing Scientific and Technological New Star Program Grant No. 2005B21. The authors appreciate the help of Drs. Rhoda E. and Edmund F. Perozzi with the use of the English in this paper. The authors are grateful to two anonymous reviewers, who gave some suggestions that improved the

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