Children's intellectual ability is associated with structural network integrity
Introduction
The inter-relationship among localized and distributed brain regions has been conceptualized as an integrated network organized into many segregated subregions linked by axonal white matter tracts (Sporns et al., 2005). A robust finding from the network perspective is that the human brain is organized in a highly efficient way for integrated information transfer, in so called small-world topology (for a review, see Bullmore and Sporns, 2009). Moreover, recent neuroimaging studies have suggested that some brain regions including the precuneus, posterior cingulate, and medial prefrontal cortex play a pivotal role as hubs or part of a structural core in the brain (Hagmann et al., 2008, Sporns et al., 2007) supporting fast communication between distributed regions. These key cortical hubs also are likely to be preferentially connected to each other forming a rich club (van den Heuvel and Sporns, 2011). Network organization undergoes rapid alterations in development with changes in axonal synaptic connectivity, white matter volume, and the thickness of corresponding cortical regions; see Vertes and Bullmore (2015) for a summary of developmental changes in network organization. In particular, structural maturation of white matter as well as cortical and subcortical areas is strongly associated with intellectual abilities from early childhood throughout adolescence (Shaw et al., 2006, Tamnes et al., 2010). However, the relationship of network properties derived from axonal white matter tracts such as network efficiency with intelligence during childhood has received little investigation.
Intelligence can be defined as the individual's capacity for mental functioning across a variety of domains including reasoning, executive function, information processing speed, memory and spatial manipulation — so called, general intelligence (g). Efficient and economical information processing among the distributed brain regions along white matter fibers is thought to contribute to general intelligence capacity (Deary et al., 2010, Gray and Thompson, 2004). The parieto-frontal integration theory (P-FIT) postulates that the dorsolateral prefrontal cortex and the parietal cortex, including the arcuate fasciculus connecting those two regions, comprise an important neuronal network associated with efficient intellectual functioning (Jung and Haier, 2007). The P-FIT of intelligence has been supported by neuroimaging findings including studies of gray matter volumes (Colom et al., 2009), cortical thickness (Narr et al., 2007) and white matter tracts (Van Beek et al., 2014). A brain network perspective provides a quantitative model for elucidating the association between the efficiency of brain networks and intelligence (Cole et al., 2012, van den Heuvel et al., 2009). Network approaches to understanding adult intelligence reveal consistent positive associations between intellectual performance and network integrity characterized by diffusion tensor imaging (DTI; Fischer et al., 2014, Li et al., 2009), resting-state functional MRI (van den Heuvel et al., 2009), and the electroencephalogram (EEG; Langer et al., 2012). Since brain development in childhood is associated with large-scale changes in synaptic connectivity, gray matter thickness and myelination, these relationships could be quite different than those observed in the adult brain. For example, there is evidence that the association between cortical regions and intelligence must include consideration of the trajectory of brain development, in which the relations between brain systems and function are dynamic and are altered as a function of age (Shaw et al., 2006). While one imaging study for children showed no relation of functional brain networks with IQ (Wu et al., 2013), no neuroimaging studies have been performed to date to investigate the relations between children's intellectual ability and whole-brain structural network properties.
In this study, we applied a graph theoretic network analysis to structural neuroimaging data acquired in typically developing children. This approach enabled characterization of global network associations with children's intelligence scores, including the role of hub regions and specific local regions in brain network architecture. We tested the hypothesis that the perceptual reasoning index (PRI), representing individual's nonverbal fluid reasoning skills, was associated with individual's structural network organization. Based on network studies on adults, higher structural network integration was predicted to be significantly associated with higher perceptual reasoning abilities. In addition to this, we particularly focused on domain-specific associations derived from three PRI subtests (Block Design, Picture Concepts, and Matrix Reasoning), and examined the association between cortical network architecture and specific intellectual performance of preadolescent children.
Section snippets
Participants
The dataset of 99 typically developing healthy preadolescent children was collected from a subset of children participating in longitudinal developmental studies who were born at one of two hospitals in the greater Los Angeles area (UC Irvine Medical Center or Long Beach Memorial Medical Center) — Table 1. All children were between 6 and 11 years old (mean ± SD: 7.80 ± 1.22 years), right-handed (defined by the modified version of the Edinburgh Handedness Inventory; Oldfield, 1971), and were the
Global network measures
Consistent with previous studies on the global network organization of children (Cao et al., 2013, Kim et al., 2014), the structural brain networks of children showed a small-world organization — i.e., σ > 1 (mean ± SD = 1.42 ± 0.13) resulting from higher network clustering (γ > 1; 1.53 ± 0.15) and relatively shorter path length (λ ≈ 1; 1.08 ± 0.02) compared to the random networks (all p < 0.05; one-sample t-test). The association between brain network organization and children's perceptual intelligence was
Discussion
The main finding of this study was a strong association between specific intellectual abilities of children and the level of integration of their structural network organization. Our results showed that children with high scores on measures of perceptual reasoning, especially Block Design (BD) and Matrix Reasoning (MR), exhibited significantly greater global efficiency of structural brain networks (Fig. 1). This finding supports the notion that superior performance of children on a test of
Conclusion
The findings in this study indicate that typically developing preadolescent children with higher intellectual ability as measured by the Perceptual Reasoning Index have brain networks that are more highly integrated at both global and local levels. Moreover, a subtest for visuo-spatial motor processing (i.e., Block Design), which is strongly associated with general intelligence (g), was most robustly correlated with global network structure as well as local brain regions and brain's rich club.
Acknowledgment
This work was supported by the NIH R01 HD 50662 (EPD), R01 HD 51852 (CAS), P50 MH 096889 (CAS, EPD), James S McDonnell Foundation (OS), 1R21 DA 035493 (BFO), and NIMH Grant 5R01 MH 074983-09 (WPH). We are grateful to the families who have participated in these longitudinal studies.
References (59)
- et al.
Where smart brains are different: a quantitative meta-analysis of functional and structural brain imaging studies on intelligence
Intelligence
(2015) - et al.
Large-scale brain networks in cognition: emerging methods and principles
Trends Cogn. Sci.
(2010) - et al.
Optimization of seed density in DTI tractography for structural networks
J. Neurosci. Methods
(2012) - et al.
Gray matter correlates of fluid, crystallized, and spatial intelligence: testing the P-FIT model
Intelligence
(2009) - et al.
The parcellation-based connectome: limitations and extensions
Neuroimage
(2013) - et al.
Cortical thickness correlates of specific cognitive performance accounted for by the general factor of intelligence in healthy children aged 6 to 18
Neuroimage
(2011) - et al.
Longer gestation is associated with more efficient brain networks in preadolescent children
Neuroimage
(2014) - et al.
Visuospatial construction
Am. J. Hum. Genet.
(1999) - et al.
Complex network measures of brain connectivity: uses and interpretations
Neuroimage
(2010) Developmental sex differences in the relation of neuroanatomical connectivity to intelligence
Intelligence
(2009)
Functional MRI evidence for disparate developmental processes underlying intelligence in boys and girls
Neuroimage
Sex differences in the development of neuroanatomical functional connectivity underlying intelligence found using Bayesian connectivity analysis
Neuroimage
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain
Neuroimage
Left fronto-parietal white matter correlates with individual differences in children's ability to solve additions and multiplications: a tractography study
Neuroimage
Network hubs in the human brain
Trends Cogn. Sci.
Differential recruitment of the sensorimotor putamen and frontoparietal cortex during motor chunking in humans
Neuron
Efficiency and cost of economical brain functional networks
PLoS Comput. Biol.
Manual for the MacArthur Health and Behavior Questionnaire (HBQ 1.0)
Rich-club organization of the newborn human brain
Proc. Natl. Acad. Sci. U. S. A.
Neuropsychological Evaluation of the Child
Complex brain networks: graph theoretical analysis of structural and functional systems
Nat. Rev. Neurosci.
Probabilistic diffusion tractography and graph theory analysis reveal abnormal white matter structural connectivity networks in drug-naive boys with attention deficit/hyperactivity disorder
J. Neurosci.
Global connectivity of prefrontal cortex predicts cognitive control and intelligence
J. Neurosci.
The neuroscience of human intelligence differences
Nat. Rev. Neurosci.
Association of structural global brain network properties with intelligence in normal aging
PLoS One
The role of the human motor cortex in the control of complex and simple finger movement sequences
Brain
Distributed neural system for general intelligence revealed by lesion mapping
Proc. Natl. Acad. Sci. U. S. A.
Neurobiology of intelligence: science and ethics
Nat. Rev. Neurosci.
Structural and functional rich club organization of the brain in children and adults
PLoS One
Cited by (60)
Early Childhood Development of Node Centrality in the White Matter Connectome and Its Relationship to IQ at Age 6 Years
2023, Biological Psychiatry: Cognitive Neuroscience and NeuroimagingStructural connectivity and intelligence in brain-injured children
2022, NeuropsychologiaThe maturation and cognitive relevance of structural brain network organization from early infancy to childhood
2021, NeuroImageCitation Excerpt :However, two previous cross-sectional studies have observed on the group level that children and adolescents (aged 6–18) with higher intelligence quotient (IQ) had more integrated SCN organization (i.e., higher global efficiency) as compared to those with lower IQ (Khundrakpam et al., 2017; Solé-Casals et al., 2019), although results were inconsistent regarding whether the higher IQ group was more modular (Khundrakpam et al., 2017) or less modular (Solé-Casals et al., 2019). This is mostly consistent with studies observing that both greater integration and greater segregation of resting state (Sherman et al., 2014; Wu et al., 2013) and tractography networks (Keunen et al., 2017; Kim et al., 2016) are related to higher IQ in children. A recent methodological advancement allows for subject-level analysis of change across time in structural brain features, such as cortical thickness, to quantify how pairs of brain regions mature in tandem within an individual.