Development of sensorimotor-visual connectome gradient at birth predicts neurocognitive outcomes at 2 years of age

Yunman Xia; Jianlong Zhao; Yuehua Xu; Dingna Duan; Mingrui Xia; Tina Jeon; Minhui Ouyang; Lina Chalak; Nancy Rollins; Hao Huang; Yong He

doi:10.1016/j.isci.2024.108981

Development of sensorimotor-visual connectome gradient at birth predicts neurocognitive outcomes at 2 years of age

iScience. 2024 Jan 20;27(2):108981. doi: 10.1016/j.isci.2024.108981. eCollection 2024 Feb 16.

Authors

Yunman Xia^{1

2

3

4}, Jianlong Zhao^{1

2

3}, Yuehua Xu^{1

2

3}, Dingna Duan^{1

2

3}, Mingrui Xia^{1

2

3}, Tina Jeon⁵, Minhui Ouyang^{5

6}, Lina Chalak⁷, Nancy Rollins⁸, Hao Huang^{5

6}, Yong He^{1

2

3

9}

Affiliations

¹ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.
² Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing 100875, China.
³ IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
⁴ Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai 200433, China.
⁵ Department of Radiology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA.
⁶ Department of Radiology, University of Pennsylvania, Philadelphia, PA 19104, USA.
⁷ Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
⁸ Department of Radiology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.
⁹ Chinese Institute for Brain Research, Beijing 102206, China.

Abstract

Functional connectome gradients represent fundamental organizing principles of the brain. Here, we report the development of the connectome gradients in preterm and term babies aged 31-42 postmenstrual weeks using task-free functional MRI and its association with postnatal cognitive growth. We show that the principal sensorimotor-to-visual gradient is present during the late preterm period and continuously evolves toward a term-like pattern. The global measurements of this gradient, characterized by explanation ratio, gradient range, and gradient variation, increased with age (p < 0.05, corrected). Focal gradient development mainly occurs in the sensorimotor, lateral, and medial parietal regions, and visual regions (p < 0.05, corrected). The connectome gradient at birth predicts cognitive and language outcomes at 2-year follow-up (p < 0.005). These results are replicated using an independent dataset from the Developing Human Connectome Project. Our findings highlight early emergent rules of the brain connectome gradient and their implications for later cognitive growth.

Keywords: Cognitive neuroscience;; Developmental neuroscience.

Abstract

Grants and funding