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Fluid intelligence is associated with gray matter volume and white matter tract integrity within multiple-demand network across adult lifespan
PIN-YU CHEN1,2, Chang-Le Chen2, Yung-Chin Hsu3, Tao-Han Hung2, Cam CAN4, Ming-Jang Chiu1,5, and Wen-Yih I. Tseng1,2

1Molecular Imaging Center, National Taiwan University, Taipei, Taiwan, Taipei City, Taiwan, 2Institute of Medical Device and Imaging, National Taiwan University College of Medicine, Taipei, Taiwan, Taipei, Taiwan, 3AcroViz Technology Inc., Taipei, Taiwan, Taipei, Taiwan, 4Cambridge Center for Ageing and Neuroscience (Cam-CAN),University of Cambridge and MRC Cognition and Brain Sciences Unit, Cambridge CB2 3EB, UK., Cambridge, United Kingdom, 5Department of Neurology, National Taiwan University Hospital, College of Medicine, National Taiwan University, Taipei, Taiwan, Taipei, Taiwan

Synopsis

In human brain, there are many cognitive demands sharing similar brain regions including working memory, attention, mathematical calculation and reasoning, and problem solving. These multiple-demand (MD) brain regions mainly involve the frontal and parietal lobes including the posterior-lateral frontal, dorso-medial frontal, and mid-parietal cortices. Previous studies with limited age ranges of the participant population reported the total brain volume was highly correlated with Gf and inconsistent findings of white matter tracts related with Gf. Fewer research explores the life-span patterns of Gf with gray and white matter and no previous study investigated the relationship of left and right hemispheres with Gf. The present study aimed to probe the life-span relationship between gray matter volume and white matter tracts connecting the MD regions and Gf in an adult life span large cohort of 603 normal participants from 18 to 88 years old. We also further compared the contributions of the left and right hemispheres to Gf. We hypothesized that gray matter volume and white matter tracts connecting the MD network may reflect age-related changes of Gf, and that Gf is a lateralized complex function. The novelty of our findings is that we examined larger normal adult population across 18 to 88 years old and found that both gray matter volume and white matter tract integrity in the MD regions are the neural substrates of Gf, reflecting the life-span aging patterns of Gf. We further examined the relationship of left and right hemispheres with Gf and found that left and right MD regions showed similar patterns of correlations with Gf scores. The age-related decrease of gray matter volume and tract integrity in the MD network is associated with the reduced functions of multiple-demand cognitive abilities reflected by Gf scores.

Introduction

In human brain, there are many cognitive demands sharing similar brain regions including working memory, attention, mathematical calculation and reasoning, and problem solving. These multiple-demand (MD) brain regions1.2, mainly involve the frontal and parietal lobes including the posterior-lateral frontal, dorso-medial frontal, and mid-parietal cortices. Previous studies with limited age ranges of the study population reported the total brain volume was highly correlated with Gf 3,4,5 and inconsistent findings of white matter tracts in relation with Gf 4,6. Few studies have explored the relationships of Gf with gray and white matter across adult lifespan, and no studies have investigated the relationships of left and right hemispheres with Gf. Therefore, the present study aimed to probe the life-span relationships between gray matter volume and white matter tracts of the MD networks and Gf in a large cohort of 603 healthy participants from 18 to 88 years old. We also further compared the contributions of the left and right hemispheres to Gf.

Material & Method

Participants 603 cognitively normal adults (age range from 18-88 years old) were recruited from the population–based sample of the Cambridge Centre for Ageing and Neuroscience (Cam-CAN) project7,8 (www.cam-can.com). Ethical approval for the study was obtained from the Cambridgeshire 2 (now East of England-Cambridge Central) Research Ethics Committee. Participants gave full informed consent. Participants were screened and underwent a diverse set of neuropsychological testing, cognitive tasks, and MRI scans. Demographic information of the current sample is provided in Table 1. Cognitive task The Gf task using the classification subtests of the standard Cattell Culture Fair Gf test evaluated the central cognitive process of fluid reasoning, which was believed to underlie the complex cognitive abilities1. Image Acquisition MRI scanning was performed on a 3T MRI system (TIM, Trio, Siemens) at the MRC Cognition Brain and Sciences Unit, Cambridge, UK. Volume-Based Morphological Analysis The morphological analysis of the cortical regions segmented on T1W images was performed by a computational anatomy toolbox CAT12 (http://www.neuro.uni-jena.de/cat/). The cortical volume index was calculated and the MD regions were masked by LONI LPBA40 atlas (http://www.loni.usc.edu/research/atlases). Mean Apparent Propagator (MAP)-MRI analysis and template-based analytical analysis for Diffusion Images MAP-MRI is a robust method to convert the diffusion signal attenuation S(q) to the diffusion propagator P(r) through a well-known Fourier transform relationship between them9. Figure 2 illustrates MAP-MRI-TBAA analyses of DTI images and the computation process generating the general fractional anisotropy (GFA) index. We applied the automatic whole brain tract-based analysis using the predefined tracts in a diffusion spectrum imaging template and an accurate registration strategy11 to sample the GFA values along the five pairs of white matter tracts connecting the MD network across a total of 603 datasets and formed a series of GFA values in 100 steps as the GFA profiles. All the diffusion images underwent image quality assurance during the preprocessing stage. Our assessment showed that the DTI data with more than 90 images of signal dropout caused an error of 6% in GFA estimation. Therefore, we discarded the DTI dataset if it had more than 90 images of signal dropout. Statistical Analyses The mean GFA profiles from the GFA profiles of 5 pairs of tracts connecting the MD network as a general representative profile of the tracts connecting the MD network and those from each hemisphere and from each tract were calculated for further partial correlation analysis. The partial correlation analysis controlling for age and gender was performed to assess the relationships between Gf scores and the volume of left and right MD regions as well as the tract integrity of left and right MD regions.

Results

Figure 3 and Table 2 show significant positive partial correlations were found between Gf scores and the volume of left and right MD regions as well as the tract integrity of left and right MD regions. All volumes of left and right MD regions displayed significant positive partial correlations with Gf scores. The volume and tract integrity of left and right MD regions are similar in the correlation patterns with fluid intelligence.

Discussion

The significance of our study is that we examined a large adult population across a wide age range, and found that both gray matter volume and white matter tract integrity in the MD regions were consistently correlated with Gf across lifespan. We further examined the relationships of left and right hemispheres with Gf and found that left and right MD regions showed similar patterns of correlations with Gf scores. The age-related decrease of gray matter volume and tract integrity in the MD network is associated with reduced functions of multiple-demand cognitive abilities reflected by the Gf scores.

Acknowledgements

Cam-CAN research was supported by the Biotechnology and Biological Sciences Research Council (Grant #BB/H008217/1).This project has also received funding from the European Union’s Horizon2020 research and innovation programme (Grant agreement #732592). R.N.A.H. was supported by MRC Programme Grant #MC-A060-5PR10. R.A.K. is supported by the Sir Henry Wellcome Trust (Grant #107392/Z/15/Z) and MRC Programme Grant#MC-A060-5PR60.We thank the Cam-CAN team (see http://www.cam-can.org/index.php?content=people), which was crucial in recruiting participants, developing the protocol, conducting the testing, and overseeing data management. We also thank the Cam-CAN respondents and their primary care team in Cambridge for their participation in this study.

References

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Figures

Figure 1: Schematic diagram of white matter tracts connecting the multiple-demand gray matter regions in the right hemisphere.

Figure 2: MRI imaging processing pipeline illustrating MAP-MRI-TBAA analyses of Diffusion Tensor Images and generation of the general fractional anisotropy (GFA) index.

Figure 3: Significant positive partial correlations controlling age and gender between Gf total scores and the volume of left and right multiple-demand (MD) regions as well as the tract integrity of left and right MD regions.

Table 1: Demographics of the 603 normal adults life span cohort.

Table 2: Partial correlation analysis controlling for age and gender to assess the relationships between mean generalized fractional anisotropy (GFA) in left and right multiple-demand (MD) regions and Gf scores as well as between volumes in left and right MD regions and Gf scores.

Proc. Intl. Soc. Mag. Reson. Med. 27 (2019)
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