Type-specific photoreceptor loss in pigeons after disruption of parasympathetic control of choroidal blood flow by the medial subdivision of the nucleus of Edinger–Westphal

Abstract

The medial part of the nucleus of Edinger–Westphal (EWM) in birds mediates light-regulated adaptive increases in choroidal blood flow (ChBF). We sought to characterize the effect of loss of EWM-mediated ChBF regulation on photoreceptor health in pigeons housed in either moderate intensity diurnal or constant light (CL). Photoreceptor abundance following complete EWM destruction was compared to that following a lesion in the pupil control circuit (as a control for spread of EWM lesions to the nearby pupil-controlling lateral EW) or following no EW damage. Birds were housed post-lesion in a 12 h 400 lux light/12 h dark light cycle for up to 16.5 months, or in constant 400 lux light for up to 3 weeks. Paraformaldehyde–glutaraldehyde fixed eyes were embedded in plastic, sectioned, slide-mounted, and stained with toluidine blue/azure II. Blinded analysis of photoreceptor outer segment abundance was performed, with outer segment types distinguished by oil droplet tint and laminar position. Brains were examined histologically to assess lesion accuracy. Disruption of pupil control had no adverse effect on photoreceptor outer segment abundance in either diurnal light or CL, but EWM destruction led to 50–60% loss of blue/violet cone outer segments in both light conditions, and a 42% loss of principal cone outer segments in CL. The findings indicate that adaptive regulation of ChBF by the EWM circuit plays a role in maintaining photoreceptor health and mitigates the harmful effect of light on photoreceptors, especially short wavelength-sensitive cone photoreceptors.

Neural control of choroidal blood flow

“…light-mediated ChBF increases) (Fitzgerald et al, 1996). In pigeon eyes affected by EWM lesions, we have found evidence of retinal functional disturbance and pathology, including: 1) increased glial fibrillary acidic protein (GFAP) in retinal Müller cells (Fitzgerald et al, 1990a; Kimble et al, 2006); 2) losses in behaviorally assessed visual acuity (Hodos et al, 1998); and photoreceptor loss (Reiner et al, 2016). In the former studies, we examined the effects of EWM lesions on retinal GFAP immunolabeling in birds housed under normal circadian lighting conditions (Kimble et al, 2006).…”

“…More recently, we characterized the effect of loss of EWM-mediated ChBF regulation on photoreceptor health in pigeons housed in either moderate intensity diurnal or constant light (Reiner et al, 2016). Photoreceptor abundance following complete EWM destruction was compared to that following a lesion in the pupil control circuit (as a control for spread of EWM lesions to the nearby pupil-controlling lateral EW) or following no EW damage.…”

Ocular Autonomic Nervous System: An Update from Anatomy to Physiological Functions

“…If SCN was activated by retinal illumination of the contralateral eye, the choroidal volume appeared to increase (vasodilation) corresponding to a similar increase in systemic blood pressure [ 168 ]. This complex parasympathetic reflex response might be adaptive and is involved in maintaining the health of photoreceptor cells [ 169 ]. Cholinergic fibers of the CG are widely distributed in the choroid of avians.…”