Layer-specific Loss and Compensation of Parvocellular Response in Subcortical Pathways of Adult Human Amblyopia

Abnormal visual experience in critical period causes amblyopia or lazy eye, reducing visual abilities even with corrected optics. A long-standing question is where in the human visual system does the amblyopic deficit arise. In particular, whether amblyopia induces selective deficits of the magnocellular (M) or the parvocellular (P) geniculostriate pathways, and whether the more ancient retinotectal pathway is also affected. Technical limitations to non-invasively measure layer-specific activity in human lateral geniculate nucleus (LGN) and superior colliculus (SC) hampered efforts in addressing these questions. In the current study, using lamina-resolved 3T and 7T fMRI and visual stimuli selectively activating the M and P pathways, we investigated layer-specific response properties of the LGN and the SC of amblyopia patients and normal controls. With stimuli presented to the amblyopic eye, there was a stronger response loss in the P layers than in the M layers of the LGN. Compared to normal controls, amblyopic eyes response to the P stimulus was selectively reduced in the superficial SC, while the fellow eyes response was robustly increased in the deep SC. Selective P response deficits of amblyopia were also observed in the visual pulvinar, early visual cortex, and ventral but not dorsal visual streams. These results provide strong in vivo evidence in adult amblyopic patients for selective deficits of parvocellular functions in the visual thalamus, and additionally reveal response deficits to the amblyopic eye and neural compensation to the fellow eye in the retinotectal pathway. HighlightsO_LIParvocellular response loss in the LGN P layers, visual pulvinar and ventral visual stream C_LIO_LISelective amblyopic deficits of the parvocellular pathway C_LIO_LIAmblyopic eyes response decreased in the superficial SC C_LIO_LIFellow eyes response increased in the deep SC C_LIO_LIAmblyopic deficits and neural compensation in the retinotectal pathway C_LI