Layer-dependent loss and enhancement of geniculostriate and retinotectal pathways in adult human amblyopia

Abstract

Abnormal visual experience during critical period leads to reorganization of neuroarchitectures in primate visual cortex. However, developmental plasticity of human subcortical visual pathways remains elusive. Using high-resolution fMRI and pathway-selective visual stimuli, we investigated layer-dependent response properties and connectivity of subcortical visual pathways of adult human amblyopia. Stimuli presented to the amblyopic eye showed selective response loss in the parvocellular layers of the lateral geniculate nucleus, and also reduced the connectivity to V1. Amblyopic eyes response to isoluminant chromatic stimulus was significantly reduced in the superficial layers of the superior colliculus, while the fellow eyes response robustly increased in the deeper layers associated with increased cortical feedbacks. Therefore, amblyopia led to selective reduction of parvocellular feedforward signals in the geniculostriate pathway, whereas loss and enhancement of parvocellular feedback signals in the retinotectal pathway. These findings shed light for future development of new tools for treating amblyopia and tracking the prognosis. HighlightsO_LIAmblyopia impairs feedforward processing in the P layers of the LGN C_LIO_LILayer-dependent loss and enhancement of cortical feedback signals in the SC C_LIO_LIPathway-specific abnormalities explain amblyopic deficits in visual acuity and attention C_LI Significance statementHow abnormal visual experiences during critical period shape the function and wire the neural circuits of human subcortex remains largely unknown. With high-resolution fMRI and visual stimuli to preferentially activate layer-dependent response in human subcortical pathways, the current study clearly demonstrates that amblyopia shifts the homeostatic interocular balance of human subcortex in a pathway-specific manner. Amblyopia led to selective loss of parvocellular feedforward signals in the geniculostriate pathway, whereas deficit and enhancement of parvocellular feedback signals in the retinotectal pathway. These pathwayspecific functional abnormalities provide the neural basis for amblyopic deficits in visual acuity, control of eye movement and attention. It sheds light for future development of new tools for treating amblyopia and tracking the prognosis.