Network attributes underlying intellectual giftedness in the developing brain

Abstract

Brain network is organized to maximize the efficiency of both segregated and integrated information processing that may be related to human intelligence. However, there have been surprisingly few studies that focus on the topological characteristics of brain network underlying extremely high intelligence that is intellectual giftedness, particularly in adolescents. Here, we examined the network topology in 25 adolescents with superior intelligence (SI-Adol), 25 adolescents with average intelligence (AI-Adol), and 27 young adults with AI (AI-Adult). We found that SI-Adol had network topological properties of high global efficiency as well as high clustering with a low wiring cost, relative to AI-Adol. However, contrary to the suggested role that brain hub regions play in general intelligence, the network efficiency of rich club connection matrix, which represents connections among brain hubs, was low in SI-Adol in comparison to AI-Adol. Rather, a higher level of local connection density was observed in SI-Adol than in AI-Adol. The highly intelligent brain may not follow this efficient yet somewhat stereotypical process of information integration entirely. Taken together, our results suggest that a highly intelligent brain may communicate more extensively, while being less dependent on rich club communications during adolescence.

Figure 1

Group-averaged structural matrices of the SI-Adol (upper left), AI-Adol (upper middle), and AI-Adult (upper right) groups. Rows and columns of matrices (i.e., nodes) are ordered as the rich clubs, non-rich clubs of the left hemisphere, and non-rich clubs of the right hemisphere. For presentation purposes, the bar graphs, which represent the total connection density of rich club connection (blue), feeder connections (green), and local connections (red) of group-averaged matrix for each group, are provided in the lower panel.

Figure 2

Global graph metrics of the study groups. (A) Standardized Z scores of global efficiency, local efficiency, and network cost were calculated using the means and standard deviations of the AI-Adol group and were plotted in the radar chart. Red asterisks indicate permutation-adjusted P values for the comparisons between the SI-Adol (red) and AI-Adol (yellow) groups, whereas green asterisks indicate those between the AI-Adult (green) and AI-Adol (yellow) groups. (B) Three-dimensional illustrations represent the individual plotting of global efficiency, local efficiency, and network cost in relations to age and intellectual quotient. The comparisons between the SI-Adol (red) and AI-Adol (yellow) groups may provide the information regarding the effects of high intelligence on network topology, while those between the AI-Adult (green) and AI-Adol (yellow) groups may represent the effects of age on network topology. *Permutation-adjusted P < 0.05; **permutation-adjusted P < 0.01; ***permutation-adjusted P < 0.001, 10,000 permutations.

Figure 3

(A) Group-averaged reconstructed structural brain network represents rich club members including the bilateral superior frontal, superior parietal, precuneus, hippocampus, putamen, and thalamus (dark blue circles) and non-rich club members (light blue circles). Three-dimensional rendering of the brain network in the MNI space was generated using BrainNet viewer. (B) Standardized Z scores of network density and cost for rich club, feeder, and local connections were calculated using the means and standard deviations of the AI-Adol group and were plotted in the radar chart. Red asterisks indicate permutation-adjusted P values for the comparisons between the SI-Adol (red) and AI-Adol (yellow) and groups, whereas green asterisks indicate those between the AI-Adult (green) and AI-Adol (yellow) groups. *permutation-adjusted P < 0.05; **permutation-adjusted P < 0.01, 10,000 permutations).

Figure 4

Standardized Z scores of network efficiency for feeder connections calculated using the means and standard deviations of the AI-Adol group. Red asterisks indicate permutation-adjusted P values for the comparisons between the SI-Adol (red) and AI-Adol (yellow) groups, whereas green asterisks indicate those between the AI-Adult (green) and AI-Adol (yellow) groups. *FDR-corrected P < 0.05; **FDR-corrected P < 0.01.