Dorsal anterior cingulate cortex in typically developing children: Laterality analysis

Jue Wang, Ning Yang, Wei Liao, Han Zhang, Chao-Gan Yan, Yu-Feng Zang, Xi-Nian Zuo, Jue Wang, Ning Yang, Wei Liao, Han Zhang, Chao-Gan Yan, Yu-Feng Zang, Xi-Nian Zuo

Abstract

We aimed to elucidate the dACC laterality in typically developing children and their sex/age-related differences with a sample of 84 right-handed children (6-16 years, 42 boys). We first replicated the previous finding observed in adults that gray matter density asymmetry in the dACC was region-specific: leftward (left > right) in its superior part, rightward (left < right) in its inferior part. Intrinsic connectivity analysis of these regions further revealed region-specific asymmetric connectivity profiles in dACC as well as their sex and age differences. Specifically, the superior dACC connectivity with frontoparietal network and the inferior dACC connectivity with visual network are rightward. The superior dACC connectivity with the default network (lateral temporal cortex) was more involved in the left hemisphere. In contrast, the inferior dACC connectivity with the default network (anterior medial prefrontal cortex) was more lateralized towards the right hemisphere. The superior dACC connectivity with lateral visual cortex was more distinct across two hemispheres in girls than that in boys. This connection in boys changed with age from right-prominent to left-prominent asymmetry whereas girls developed the connection from left-prominent to no asymmetry. These findings not only highlight the complexity and laterality of the dACC but also provided insights into dynamical structure-function relationships during the development.

Figures

Fig. 1
Fig. 1
Illustration of the overall procedure of image analysis. (A) Structural image analysis. Individual raw gray matter density (GMD) images are first normalized to a symmetric gray matter template in the standard brain space and then spatially smoothed. Paired t-tests were performed on smoothed GMD images and their left–right flipped (LR-flipped) versions to achieve a T-map for GMD differences between the left hemisphere (LH) and the right hemisphere (RH). This laterality map derives seeds of regions of interests for superior and inferior subdivisions of the dorsal cingulate cortex (dACC) for next steps of functional image analysis (B). In this second stage, individual raw BOLD images are first normalized to the symmetric standard brain template and then seed-based functional connectivity maps are estimated by using the dACC seeds in both hemispheres, and quantified with their Fisher's z-maps. Flexible factor analysis is employed to detect laterality effects on both ipsilateral (L-L versus R-R) and contralateral (L-R versus R-L) functional connectivity of the dACC using the left dACC (L.dACC) seeded z-maps and the LR-flipped versions (LR-flipped R.dACC) of the right dACC (R.dACC) seeded z-maps as inputs.
Fig. 2
Fig. 2
Laterality of gray matter density (GMD) and its regional difference in dACC. T-maps of the paired t-tests on GMD between the left and the right hemisphere are overlaid onto the symmetric structural template. The warm colors indicate a leftward (left > right) laterality whereas the cool colors represents degree of a rightward (right > left) laterality of GMD. Region-specific asymmetry of GMD is detected in dACC where (A) inferior dACC seeds (±5, 17, 22) were rightward and (B) superior dACC seeds (±6, 19, 31) showed leftward asymmetry.
Fig. 3
Fig. 3
Intrinsic functional connectivity (iFC) of the dorsal anterior cingulate cortex (dACC). Mean Fisher-z maps of all individual iFC of the four seeds for the superior (A: left hemisphere; B: right hemisphere) and inferior (C: left hemisphere; D: right hemisphere) dACC are rendered onto the Conte69_32k surfaces. All the maps displayed for lateral and medial views of both hemispheres. Gray curves indicate the boundaries between the seven networks in Yeo et al. (2011). The locations of the dACC seeds are labeled as a green circle on the surfaces.
Fig. 4
Fig. 4
Laterality of superior dACC's functional connectivity and its network distribution. T-value maps of the flexible factor analysis (see in Section 2) are rendered onto the Conte69_32k surfaces. Maps of the seven networks including visual (Visual), somatomotor (SomMot), dorsal attention (DorsAttn), ventral attention (VentAttn), limbic (Limbic), frontoparietal (Control) and default (Default) networks are also displayed on these surfaces. All the maps displayed for multiple views of both the ipsilateral hemisphere (A, B) and the contralateral hemisphere (C, D) in Conte69_32k space: A, anterior; P, posterior; D, dorsal; V, ventral. The functional network organization of the human cerebral cortex is derived from Yeo et al. (2011). Colors reflect regions estimated to be within the same network. Black curves indicate the boundaries between the networks. The locations of the superior dACC seeds are labeled as a green circle on the surfaces for laterality of (A) the ipsilateral functional connectivity (LL versus RR: warm colors for LL > RR, cool colors for LL < RR) and the contralateral functional connectivity (LR versus RL: warm colors for LR > RL, cool colors for LR < RL).
Fig. 5
Fig. 5
Laterality of inferior dACC's functional connectivity and its network distribution. T-value maps of the flexible factor analysis (see in Section 2) are rendered onto the Conte69_32k surfaces. Maps of the seven networks including visual (Visual), somatomotor (SomMot), dorsal attention (DorsAttn), ventral attention (VentAttn), limbic (Limbic), frontoparietal (Control) and default (Default) networks are also displayed on these surfaces. All the maps displayed for multiple views of both the ipsilateral hemisphere (A, B) and the contralateral hemisphere (C, D) in Conte69_32k space: A, anterior; P, posterior; D, dorsal; V, ventral. The functional network organization of the human cerebral cortex is derived from Yeo et al. (2011). Colors reflect regions estimated to be within the same network. Black curves indicate the boundaries between the networks. The locations of the inferior dACC seeds are labeled as a green circle on the surfaces for laterality of (A) the ipsilateral functional connectivity (LL versus RR: warm colors for LL > RR, cool colors for LL < RR) and the contralateral functional connectivity (LR versus RL: warm colors for LR > RL, cool colors for LR < RL).
Fig. 6
Fig. 6
Interaction between the laterality of superior dACC's ipsilateral functional connectivity and sex. (A) T-value maps of the flexible factor analysis (see in Section 2) are rendered onto the Conte69_32k surfaces. The maps displayed for multiple views of the ipsilateral hemisphere in Conte69_32k space: A, anterior; P, posterior; D, dorsal; V, ventral. Black curves indicate the boundaries between the seven neural networks. The location of the superior dACC seed is labeled as a green circle on the surfaces for laterality of the ipsilateral functional connectivity. The colorbar indicates different directions of the interaction: warm colors for female and cool colors for male. (B) Scatter bar plots are displayed for an intuitive illustration on the laterality–sex interaction in the region cluster as shown in (A). The laterality index is quantified with LL-RR adjusted for head motion and global mean connectivity.
Fig. 7
Fig. 7
Interactions among the laterality of dACC's functional connectivity, sex and age. T-value maps of the three-way interaction derived from the flexible factor analysis (see in Section 2) are rendered onto the Conte69_32k surfaces for (A) the superior dACC ipsilateral functional connectivity and (C) the inferior dACC contralateral functional connectivity. The maps displayed for multiple views of the ipsilateral hemisphere in Conte69_32k space: A, anterior; P, posterior; D, dorsal; V, ventral. Black curves indicate the boundaries between the seven neural networks. The locations of the superior and inferior dACC seeds are labeled as a green circle on the surfaces. The colorbar indicates different directions of the interaction. Scatter bar plots are displayed in (B) for an intuitive illustration on the three-way interaction in the region cluster as shown in (A), and in (D) for an intuitive illustration on the three-way interaction in the region cluster as shown in (C). The laterality index is quantified with LL-RR and LR-RL adjusted for head motion and global mean connectivity, respectively. Dashed curves indicate the 95% confidence intervals of the linear regression of the connectivity laterality on age.

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Source: PubMed

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