Oxygen-free metabolism in the bird inner retina supported by the pecten.

Abstract

Neural tissues are exceptionally sensitive to oxygen deprivation and rely on a dense network of blood vessels to support their extraordinarily high metabolic demands for oxygen, nutrients and clearance of waste products^1-4. In birds, one of the metabolically most demanding neural tissue-the retina-lacks internal blood vessels^5,6. This raises the question of how such a metabolically demanding neural tissue can function without blood perfusion. Here we show that, while the photoreceptor outer segments in the outer retina have access to oxygen, the inner bird retina operates under chronic anoxia, supported by anaerobic glycolysis in the retinal neurons. We provide evidence that the pecten oculi-a uniquely vascularized structure in the vitreous humour of birds, the function of which has been debated for centuries^5-9-supplies the anoxic inner retina with glucose and removes lactic acid. We suggest that the pecten's metabolic support of the bird retina's anoxia tolerance enabled first the evolution of a thick cell-dense, avascular retina, which secondarily served as an exaptation enabling retinal function during high-altitude migrations.