MRI reveals differential regulation of retinal and choroidal blood volumes in rat retina

The retina is nourished by two unique (retinal and choroidal) circulations. The lack of depth-resolved blood volume (BV) imaging techniques hampers investigation of vascular-specific regulation of the retina in vivo. This study presents a high-resolution, laminar-specific magnetic resonance imaging (MRI) study to image retinal and choroidal BVs, their responses to physiologic challenges in normal and Royal-College-of-Surgeons (RCS) rats (a model of retinal degeneration). Retinal and choroidal BVs were imaged by MRI (30 × 30 × 800 μm) with intravascular administration of monocrystalline iron oxide nanocolloid (MION) contrast agent. Relative baseline BV and BV changes due to physiologic challenges were calculated in normal and RCS rat retinas. BV-MRI revealed two well-resolved retinal and choroidal vascular layers located on either side of the retina and an intervening avascular layer. The ratio of choroidal:retinal BV in normal rats at baseline was 9.8 ± 3.2 in control rat retinas (N = 7). Hyperoxia decreased retinal BV (− 51 ± 17%, p < 0.05) more than choroidal BV (− 28 ± 14%), and hypercapnia increased retinal BV (52 ± 11%, p < 0.01) more than choroidal BV (12 ± 11%). BV-MRI in degenerated retinas of RCS rats (N = 7) revealed thinning of the avascular layer and an increase in relative baseline retinal and choroidal BVs. Only hypercapnia-induced BV changes in the retinal vasculature of RCS rats were significantly different (smaller) from controls (p < 0.05).These findings suggest that BV in both retinal vasculatures is regulated. The relative baseline BV in both vasculatures increased in retinal degeneration. BV-MRI provides clinically relevant data that may prove useful for early detection and longitudinal probing of retinal diseases, and could complement optical imaging techniques.

Research Highlights►Blood volume MRI revealed two distinct laminar signals that correspond to the retinal and choroid vascular layers bounding the retina. ►Choroid BV was about ten times higher than retinal BV. ►fMRI based on BV changes detects vascular layer-specific responses to physiologic challenges and reveals that the choroid blood vessels were less responsive to physiologic challenge than retinal vessels. ►In an accepted animal model of photoreceptor degeneration, MRI confirmed the disappearance of the outer nuclear layer and photoreceptor segments. ►The baseline BV in the retinal and choroid vasculatures was elevated compared to age-matched controls.