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Functional and morphological assessment of age-related changes in the choroid and outer retina in pigeons
- MALINDA E.C. FITZGERALD, ELIZABETH TOLLEY, SHARON FRASE, YURI ZAGVAZDIN, RONALD F. MILLER, WILLIAM HODOS, ANTON REINER
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- Journal:
- Visual Neuroscience / Volume 18 / Issue 2 / March 2001
- Published online by Cambridge University Press:
- 04 May 2001, pp. 299-317
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We sought to determine if choroidal and outer retinal deterioration occur with age in pigeons, as they do in other species, and investigated the relationship between age-related retinal and choroidal changes. In 64 pigeons ranging in age over the pigeon lifespan (0.5–20 years), we measured some or all among the following parameters: choroidal blood flow (ChBF) by laser Doppler flowmetry, choroidal thickness and choriocapillary vessel abundance by LM histology, choriocapillary endothelial cell transport specializations by EM histology, acuity by behavioral methods, and degenerating photoreceptor abundance and total photoreceptor abundance by LM histology. Regression and Receiver Operator Curve (ROC) analyses were used to characterize the pattern of age-related changes and determine the ages at or by which significant changes occurred. For the 45 birds for which we measured choroidal parameters, choriocapillary vessel abundance showed a curvilinear decline with age and half of this decline occurred by 3.5–4.6 years. The endothelial cell transport specializations called channels also declined curvilinearly with age. Choroidal thickness was slightly increased between the ages of 3–6 years, and thereafter declined steadily so that choroidal thickness in the oldest birds was half that in the youngest. ChBF showed an abrupt decline of about 20% at 4 years and a further 20% decline thereafter. In the 53 birds for which we obtained visual acuity and/or photoreceptor data, we observed a curvilinear decline in acuity (with half the decline having occurred by 8 years) and a prominent stepwise decline of about 20% in photoreceptor abundance at 4.7 years, followed by further decline thereafter. The period of major photoreceptor loss coincided with ages during which about 10% of photoreceptors appeared to show degenerative changes (4–8 years of age). Using partial correlation analysis with the common effect of age held constant, ChBF was found to have a positive correlation with acuity. Our results show that ChBF and choroidal vascularity decline significantly with age in pigeons, as do acuity and photoreceptor abundance. Our statistical analyses suggest that prominent choroidal vascular decline preceded the visual decline, and that there is a positive relationship between choroidal and visual functions. Thus, our findings are consistent with the view that age-related decline in choroidal function might contribute to age-related vision loss in pigeons.
Preganglionic endings from nucleus of Edinger-Westphal in pigeon ciliary ganglion contain neuronal nitric oxide synthase
- SHERRY CUTHBERTSON, YURI S. ZAGVAZDIN, TOYA D.H. KIMBLE, WILLIAM J. LAMOREAUX, BRYAN S. JACKSON, MALINDA E.C. FITZGERALD, ANTON REINER
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- Journal:
- Visual Neuroscience / Volume 16 / Issue 5 / September 1999
- Published online by Cambridge University Press:
- 01 September 1999, pp. 819-834
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The avian ciliary ganglion (CG) controls choroidal blood flow by its choroidal neurons, and pupil constriction and accommodation by its ciliary neurons. It was previously reported that both choroidal and ciliary neurons label positively for NADPH diaphorase (NADPHd), a marker for nitric oxide synthase (NOS). To assess if this labeling is preganglionic or postganglionic and to determine if it is attributable to neuronal NOS (nNOS), we studied pigeon CG using NADPHd histochemistry and nNOS immunohistochemistry (IHC). Short-duration staining times by NADPHd histochemistry yielded intense labeling of structures that appeared to be the cap-like endings on ciliary neurons and the boutonal endings on choroidal neurons that arise from the nucleus of Edinger-Westphal (EW), and light or no postganglionic perikaryal staining. The light postganglionic staining that was observed tended to be localized to ciliary neurons. Consistent with this, NADPHd+ nerve fibers were observed in the postganglionic ciliary nerves but rarely in the postganglionic choroidal nerves. These same staining times yielded robust staining of neurons in the orbital pterygopalatine microganglia network, which are known to be nNOS+. Diffuse staining of CG perikarya was observed with longer staining durations, and this staining tended to mask the preganglionic labeling. Preganglionic NADPHd+ staining in CG with short staining times was blocked by the NOS inhibitors iodonium diphenyl (IDP) and dichlorophenol-indophenol (DPIP), but the diffuse postganglionic staining observed with the longer staining times was not completely blocked. Labeling of CG sections for substance P (SP) by IHC (which labels EW-originating preganglionic endings in CG) and subsequently for NADPHd confirmed that NADPHd was localized to preganglionic endings on CG neurons. Immunohistochemical double labeling for nNOS and SP or enkephalin further confirmed that nNOS is found in boutonal and cap-like endings in the CG. Two studies were then carried out to demonstrate that the nNOS+ preganglionic endings in CG arise from EW. First, NADPHd+ and nNOS+ neurons were observed in EW in pigeons treated with colchicine to enhance perikaryal labeling. Second, NADPHd+ and nNOS+ preganglionic endings were eliminated from CG ipsilateral to an EW lesion. These various results indicate that NOS is present in EW-arising preganglionic endings on choroidal and ciliary neurons in avian CG. NOS also appears to be found in some ciliary neurons, but its presence in choroidal neurons is currently uncertain.
Visual acuity losses in pigeons with lesions of the nucleus of Edinger-Westphal that disrupt the adaptive regulation of choroidal blood flow
- WILLIAM HODOS, RONALD F. MILLER, MIMI M. GHIM, MALINDA E.C. FITZGERALD, CLAUDIO TOLEDO, ANTON REINER
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- Journal:
- Visual Neuroscience / Volume 15 / Issue 2 / February 1998
- Published online by Cambridge University Press:
- 01 February 1998, pp. 273-287
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Choroidal blood flow (ChBF) in birds is regulated by a neural circuit whose components are the retina, the suprachiasmatic nucleus, the medial division of the Edinger-Westphal nucleus (EWM), the ciliary ganglion, and the choriod. We have previously shown that lesions of EWM appear to result in pathological alterations in the retina. To determine whether EWM lesions also lead to altered visual functions, we have examined the effects of EWM lesions on visual acuity in pigeons. Bilateral lesions of EWM were made electrolytically, and visual acuity for high-contrast, square-wave gratings was determined behaviorally about 1 year later and compared to that of a group of pigeons that had received sham lesions of EW about 1 year prior to acuity testing. Because lesions targeting EWM invariably resulted in damage to the adjoining lateral part of the Edinger-Westphal nucleus (EWL), which controls pupillary constriction and accommodation, two additional control groups were studied. In one such control group, bilateral lesions in the area pretectalis (AP), which innervates the pupillary control part of EWL and thereby controls pupillary constriction, were made and the effects on visual acuity determined about 1 year later. In the second such control group, the effects of acute accommodative and pupillary dysfunction on acuity were studied in pigeons made cycloplegic. The accuracy of all lesions was later confirmed histologically. The mean acuities of birds with AP lesions (9.1 ± 1.4 cycles/deg) and sham lesions (7.1 ± 1.5 cycles/deg) were not significantly different from normal, based on published normative data on pigeons. In contrast, pigeons with lesions that completely destroyed EW bilaterally showed visual acuity (2.7 ± 0.1 cycles/deg) that was well below the acuity of the sham and AP-lesion control groups. The acuity of the cycloplegic pigeons (4.8 ± 0.3 cycles/deg) and one pigeon with a nearly complete bilateral EWL but a unilateral EWM lesion (6.4 cycles/deg) indicated that only about half of the loss with a bilateral EW lesion could be attributed to accommodative dysfunction. Thus, bilateral destruction of EWM appears to have led to a loss in visual acuity. This conclusion suggests that disruption of adaptive neural regulation of ChBF may impair visual function. Destruction of EWM was, however, associated with damage to the somatic components of the oculomotor and trochlear nuclei. The possibility cannot be excluded that such damage also contributed to the acuity loss.