Early Developmental Trajectories of Functional Connectivity Along the Visual Pathways in Rhesus Monkeys

Abstract

Early social interactions shape the development of social behavior, although the critical periods or the underlying neurodevelopmental processes are not completely understood. Here, we studied the developmental changes in neural pathways underlying visual social engagement in the translational rhesus monkey model. Changes in functional connectivity (FC) along the ventral object and motion pathways and the dorsal attention/visuo-spatial pathways were studied longitudinally using resting-state functional MRI in infant rhesus monkeys, from birth through early weaning (3 months), given the socioemotional changes experienced during this period. Our results revealed that (1) maturation along the visual pathways proceeds in a caudo-rostral progression with primary visual areas (V1-V3) showing strong FC as early as 2 weeks of age, whereas higher-order visual and attentional areas (e.g., MT-AST, LIP-FEF) show weak FC; (2) functional changes were pathway-specific (e.g., robust FC increases detected in the most anterior aspect of the object pathway (TE-AMY), but FC remained weak in the other pathways (e.g., AST-AMY)); (3) FC matures similarly in both right and left hemispheres. Our findings suggest that visual pathways in infant macaques undergo selective remodeling during the first 3 months of life, likely regulated by early social interactions and supporting the transition to independence from the mother.

Keywords: macaque; neurodevelopment; resting state functional MRI; social visual engagement.

Figure 1.

Functional connectivity (FC) within the ventral object pathway. (A) FC between the analyzed regions of interest (ROIs) in the two hemispheres separately. Blue shaded areas indicate ROIs analyzed along the ventral object pathway (V1–V3-TEO–TE–AMY), displayed on the Caret F99 macaque template (Van Essen 2002). TEO–TE: decreased FC from week 2 to 12, week 4 to 12 and week 8 to 12; TE–AMY: increased FC from week 2 to week 8 and 12; and from week 4 to week 12. (B) FC matrices showing every possible ROI–ROI connectivity used for the network analysis within the ventral object pathway at each age point.

Figure 2.

Functional connectivity (FC) within the ventral motion pathway. (A) FC between the analyzed regions of interest (ROIs) in the two hemispheres separately. Green shaded areas indicate ROIs analyzed along the ventral motion pathway, displayed on the Caret F99 macaque template (Van Essen 2002). From dark to light green: V1 – V3 – MT – AST – AMY. V3–MT: higher FC over the left hemisphere compared with the right; unchanged FC between MT–AST and AST–AMY during infancy. (B) FC matrices showing every possible ROI–ROI connectivity used for the network analysis within the ventral motion pathway at each age point.

Figure 3.

Functional connectivity (FC) within the dorsal attention/visuo-spatial pathways. (A) FC between the analyzed regions of interest (ROIs) in the two hemispheres separately. Pink shaded areas indicate ROIs analyzed along the dorsal visual-spatial pathway, displayed on the Caret F99 macaque template (Van Essen 2002). From dark to light pink: V1 – V3 – LIP – BA46 or FEF. V3–LIP: decreased FC from week 4 to week 12; LIP–BA46: uncoupled ROIs during infancy. (B) FC matrices showing every possible ROI–ROI connectivity used for the network analysis within the dorsal attention/visuo-spatial pathways at each age point.