Development of visual cortex in human neonates is selectively modified by postnatal experience

  1. Mingyang Li
  2. Tingting Liu
  3. Xinyi Xu
  4. Qingqing Wen
  5. Zhiyong Zhao
  6. Xixi Dang
  7. Yi Zhang
  8. Dan Wu  Is a corresponding author
  1. Key Laboratory for Biomedical Engineering of Ministry of Education, Department of Biomedical Engineering, College of Biomedical Engineering & Instrument Science, Zhejiang University, China
  2. Department of Psychology, Zhejiang Sci-Tech University, China
  3. Children's Hospital School of Medicine, Zhejiang University, China
  4. Binjiang Institute of Zhejiang University, China
9 figures, 2 tables and 1 additional file

Figures

Figure 1 with 4 supplements
The development of cortical structural properties in human newborns.

(a) The distribution of neonatal postmenstrual age (PMA) at scan in the study population. (b) The averaged cortical thickness (CT) and (c) the averaged cortical myelination (CM) from 38 to 44 weeks …

Figure 1—figure supplement 1
The 34 ROIs of the ventral cortex in the adult and neonatal space.

The ventral cortex was parcellated into 34 regions of interest (ROIs) in HCP-MMP atlas (a), which was projected onto a neonatal template at 40 weeks of postmenstrual age (PMA) (b). White arrows …

Figure 1—figure supplement 2
Spatial variation of cortical structure development in the ventral cortex.

The correlation maps between cortical thickness (CT) or cortical myelination (CM) and postmenstrual age (PMA) in ventral cortex (a). To quantify the spatial variation of the development, we divide …

Figure 1—figure supplement 3
Example segmentations of subjects scanned at 37–44 weeks.

The outlines indicate the boundary between white and gray matter.

Figure 1—figure supplement 4
Comparison of the area V1 created by manual and registered methods.

(a) The gradient map of cortical myelination in the neonates, where the black line depicts the manually delineated V1 contours. (b) Comparison of the V1 area transformed from adult space (yellow) …

Figure 2 with 2 supplements
Contribution of postnatal time and gestational age on the development of cortical thickness and cortical myelination.

The correlation maps between cortical thickness (CT)/cortical myelination (CM) and gestational age (GA) (a, b) or postnatal time (PT) (c, d) in ventral cortex. (e–h) Validation analysis using two …

Figure 2—figure supplement 1
Relationship between gestational age (GA) and postnatal time (PT).

The Pearson correlation between them was not significant (r = –0.08, p>0.1).

Figure 2—figure supplement 2
The correlation coefficient maps between postmenstrual age (PMA) or postnatal time (PT) and the structural measurements (cortical thickness [CT] or cortical myelination [CM]) across the whole brain.

The primary sensory areas such as V1 (visual), primary auditory area (auditory), and central sulcus (sensorimotor) demonstrated the most prominent increase of CT with respect to both PMA and PT, …

The development of cortical thickness (CT) and cortical myelination (CM) in primary visual cortex (V1) and higher-level visual cortex (VOTC) in human newborns.

(a) Definitions of V1 and VOTC. Correlation between CT (b, c) or CM (d, e) and gestational age (GA) or postnatal time (PT) in V1 and VOTC. *p<0.05, ***p<0.001.

Figure 4 with 4 supplements
The innate functional organization of ventral cortex within 1 day after birth and its development in the first month of age in human newborns.

(a) The pairwise correlation matrix describes the functional correlations among 34 regions of interest (ROIs) across hemispheres in ventral cortex. (b) The scatter graph illustrates the correlation …

Figure 4—figure supplement 1
Multidimensional scaling and community groups based on pairwise ipsilateral connections between 34 regions of interest (ROIs) in the left or right ventral cortex.

The results were similar between left and right cortex, and similar in the networks constructed using different thresholds of correlation coefficient r from 0.1 to 0.2. The color of the nodes …

Figure 4—figure supplement 2
Functional networks of right ventral cortex for each postmenstrual age (PMA) week from 38 to 44 weeks based on multidimensional scaling.

We found similar three-cluster network structure in the infants at different PMA (except for 42 weeks), and subtle fluctuation was observed in the boundary between different clusters at different PMA.

Figure 4—figure supplement 3
The correlation between global efficiency or mean cluster coefficient of the right hemisphere and gestational age (GA) or postnatal time (PT).

*p<0.05, ***p<0.001.

Figure 4—figure supplement 4
The correlations between ipsilateral functional connections and postmenstrual age.

The left and right half matrix indicates the connections in the left and right hemispheres, respectively.

The development of the functional connections between bilateral primary visual cortex (V1) and higher-level visual cortex (VOTC) and their cross-correlations.

(a) The connections of interest include the homotopic connection between bilateral V1 (purple), bilateral VOTC (peach), and the averaged ipsilateral connections between V1 and VOTC in each of the …

Mediation analysis between the developmental factors (gestational age [GA] or postnatal time [PT]), homotopic functional connection between bilateral V1, and structural features (cortical thickness [CT] or cortical myelination [CM]).

Homotopic connection between bilateral V1 was set as an independent variate, while the developmental factor was a dependent variate, and the structural features (CT or CM) was the mediated variate. …

Figure 7 with 2 supplements
Comparison of structural and functional features between term- and preterm-born infants.

(a) The comparison of gestational age (GA), postmenstrual age (PMA), and postnatal time (PT) between term-born and preterm-born infants. (b–d) The t maps of cortical thickness (CT), cortical …

Figure 7—figure supplement 1
The mean cortical thickness (CT) and mean cortical myelination (CM) in each of the 34 regions of interest (ROIs) in the ventral visual cortex compared between term and preterm-born infants.

*p<0.05.

Figure 7—figure supplement 2
Functional networks of right ventral cortex in term-born and preterm-born infants, based on multidimensional analysis.
Author response image 1
The distribution of neonates with different PT in the term and preterm infants.
Author response image 2
Mapping of Wang et al.

(2015) atlas on the 40-week neonatal template.

Tables

Table 1
Summary of the effects of gestational age (GA) and postnatal time (PT) on the structural and functional properties of the ventral visual cortex.

The numbers indicate the correlation coefficients of the corresponding measurement and the GA or PT.

PropertiesGAPT
 CT Whole ventral cortex<0.2>0.4
 V10.2–0.4>0.4
 VOTC<0.20.2–0.4
 CM Whole ventral cortex>0.4Nonsignificant
 V1>0.4<0.2
 VOTC>0.4Nonsignificant
 FC network properties in the whole ventral cortex0.2–0.4<0.2
 Homotopic connection V1Nonsignificant<0.2
 VOTCNonsignificant<0.2
 Ipsilateral connection between V1 and VOTC<0.2<0.2
  1. CT, cortical thickness; CM, cortical myelination; VOTC, ventral occipital temporal cortex.

Appendix 1—key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
Software, algorithmMATLABMathWorksRRID:SCR_001622
Software, algorithmSPMFILRRID:SCR_007037
Software, algorithmDPABIdoi:10.1007/s12021-016-9299-4RRID:SCR_010501
Software, algorithmFSLFMRIBRRID:SCR_002823
Software, algorithmMSMdoi:10.1016/j.neuroimage.2017.10.037
Software, algorithmBCTdoi:10.1016/j.neuroimage.2009.10.003RRID:SCR_004841
Software, algorithmConnectome WorkbenchConnectome WorkbenchRRID:SCR_008750

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