Weakening of Subcortical and Strengthening of Cortical Visual Pathways Across Early Adolescence

Mounting evidence suggests that amygdalar nuclei receive visual information via both a well-characterized cortical pathway through the inferior temporal cortex and a subcortical route through the superior colliculus and pulvinar. This subcortical pathway may facilitate rapid responses to salient visual stimuli and could explain phenomena such as blindsight. However, controversies remain about the organization of the subcortical pathway, its role in visual processing, and how the cortical and subcortical pathways mature across development. To address these questions we used longitudinal, minimally processed multi-shell High Angular Resolution Diffusion Imaging (HARDI) data from 4361 participants in the Adolescent Brain Cognitive Development (ABCD) study, reconstructing every major segment of the cortical and subcortical amygdala pathways. We tested the existence of the subcortical pathway against null tractography models, characterized cortical and subcortical pathways development across early adolescence, and investigated their association with visual processing speed. Diffusion MRI data provide support for the existence of bilateral pulvinar-amygdala pathways against a null model (all p < 0.001, corrected). While cortical tracts involving the primary and extrastriate visual cortex and the inferior-temporal cortex strengthened with chronological age and over pubertal development, we demonstrate that subcortical pulvinar-amygdala connectivity decreased over pubertal development. Greater connectivity strength of the right pulvinar-amygdala tract was associated with faster responses on a visual task for both emotional face and place stimuli, a relationship also seen for cortical tracts. This study provides supporting evidence for the existence of pulvinar to amygdala tracts in the largest sample of adolescent participants studied to date. Greater connectivity in both cortical and subcortical tracts was associated with faster reaction time on a visual task, but further work will be needed to investigate the specificity of this association in terms of both task and tract. In line with the hypothesized importance of the subcortical pathway in early development, we show that the developmental trajectories of cortical and subcortical pathways diverge and highlight the influence of pubertal development, with cortical pathways generally strengthening and subcortical pathways weakening across early adolescence.