Functional MRI of postnatal visual development in normal and hypoxic-ischemic-injured superior colliculi

The superior colliculus (SC) is a laminated subcortical structure in the mammalian midbrain, whose superficial layers receive visual information from the retina and the visual cortex. To date, its functional organization and development in the visual system remain largely unknown. This study employed blood oxygenation level-dependent (BOLD) functional MRI to evaluate the visual responses of the SC in normally developing and severe neonatal hypoxic-ischemic (HI)-injured rat brains from the time of eyelid opening to adulthood. MRI was performed to the normal animals (n = 7) at postnatal days (P) 14, 21, 28 and 60. In the HI-injured group (n = 7), the ipsilesional primary and secondary visual cortices were completely damaged after unilateral ligation of the left common carotid artery at P7 followed by hypoxia for 2 h, and MRI was performed at P60. Upon unilateral flash illumination, the normal contralateral SC underwent a systematic increase in BOLD signal amplitude with age especially after the third postnatal week. However, no significant difference in BOLD signal increase was found between P14 and P21. These findings implied the presence of neurovascular coupling at the time of eyelid opening, and the progressive development of hemodynamic regulation in the subcortical visual system. In the HI-injured group at P60, the BOLD signal increases in both SC remained at the same level as the normal group at P28 though they were significantly lower than the normal group at P60. These observations suggested the residual visual functions on both sides of the subcortical brain, despite the damages to the entire ipsilesional visual cortex. The results of this study constitute important evidence on the progressive maturation of visual functions and hemodynamic responses in the normal subcortical brain, and its functional plasticity upon neonatal HI injury.