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Oxygen Distribution in the Macaque Retina

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Oxygen Distribution in the Macaque Retina Oxygen Distribution in the Macaque Retina Jameel Ahmed* Rod D. Braun,^ Robert Dunn, Jr. * and Robert A. Linsenmeier*X Purpose. Oxygen distribution was characterized in the macaque retina, which is more like the human retina than others studied previously. Methods. Profiles of oxygen tension (Po2) as a function of distance were recorded in a parafo- veal region about halfway between the fovea and optic disk, and from the fovea in one animal. A one-dimensional diffusion model was used to determine photoreceptor oxygen consump- tion (QO2). Results. In the parafovea, the Po2 decreased as the electrode was withdrawn from the choroid toward the inner retina, reaching a minimum value during dark adaptation of about 9 mmHg at about 70% retinal depth, and then increasing more proximally. Approximately 90% of the oxygen requirement of the photoreceptors was supplied by the choroidal circulation and 10% by the retinal circulation. In light adaptation, there was a monotonic Po2 gradient from the choroid to the inner retina, indicating that all of the oxygen used by photoreceptors was supplied by the choroid. In the fovea, the choroid supplied almost all the oxygen in both dark and light adaptation, with a minor supply from the vitreous humor. Dark-adapted foveal oxy- gen consumption was lower than parafoveal oxygen consumption. Light reduced the oxygen consumption of the photoreceptors, in both regions studied, by 16-; Conclusions. The results show that oxygenation of the parafoveal monkey retina is similar to that previously observed in the cat area centralis. In the fovea, the oxygen distribution differs as expected considering the thinner retina and the absence of inner retinal neurons and retinal circulation. Invest Ophthalmol Vis Sci. 1993;34:516-521. Intensive measurements of oxygen distribution and serves as a good model for oxygenation of the parafo- photoreceptor oxygen consumption have been made veal primate retina. In one monkey, we were able to in the retina of the cat1"3 and miniature pig;4 however, obtain measurements from the fovea. These measure- no intraretinal measurements, and only a small num- ments showed differences that were consistent with ber of vitreal measurements, have been made in pri- the decreased retinal thickness and the absence of reti- mates. In this paper, we report intraretinal measure- nal circulation in this region. ments from two monkeys, and show that the cat retina MATERIALS AND METHODS From the Departments of *Biomedical and ~\Chemical Engineering and %Neurobiology and Physiology, Northwestern University, Evanston, Measurements were made from two monkeys using Illinois. techniques that were similar to those used previously This work was supported by NEl grant EY05034 to RAL and a student in studies on the cat.25 One monkey was a cynomolgus fellowship (toJ.A.) in memory of Herman Shane from the Fight for Sight Research Division of the National Society to Prevent Blindness. macaque (M. fascicularis) weighing 3.3 kg and the Submitted for publication: July 6, 1992; accepted November 10, 1992. other was a pig-tailed macaque (M. nemestrina) weigh- Proprietary interest category: N. ing 4.8 kg. We adhered to the ARVO Statement for Reprint requests: Dr. Robert A. Linsenmeier, Biomedical Engineering Department, Northwestern University, 2145 Sheridan Road, Evanston, the Use of Animals in Ophthalmic and Vision Re- IL 60208-3107. search. Animals were initially anesthetized with keta- Investigative Ophthalmology & Visual Science, March 1993, Vol. 34, No. 3 516 Copyright © Association for Research in Vision and Ophthalmology Downloaded from iovs.arvojournals.org on 09/30/2021 Oxygen Distribution in the Macaque Retina 517 mine (22 mg/kg) plus acepromazine (0.15 mg/kg) IM, arrive at Q. We used previously determined values for and anesthesia was maintained during surgery with so- D of 1.97 X 10"5 cm2/sec and for k of 2.4 X 10"5 ml 3 dium thiamylal (5 wt%). Long-term anesthesia was O2/ml tissue-mmHg. The only values reported here provided by urethane (375-425 mg/kg loading dose that were obtained from the model are for: (1) photor- and 100-200 mg/hr thereafter). After surgery, ani- eceptor QO2; (2) the percentage of photoreceptor mals were paralyzed with pancuronium bromide (0.2- QO2 that was obtained from the retinal circulation; 0.3 mg/kg/hr) and artificially respirated. The eye was and (3) the size of the consuming layer. Values are attached to a stabilizing ring, and hypodermic needles given as mean ± SD. were inserted into the eye to carry the oxygen micro- electrode, an Ag/AgCl vitreal reference electrode for RESULTS the oxygen measurement, and an Ag/AgCl vitreal electrode for recording the electroretinogram (ERG). Figure 1 shows examples of profiles of Po2 as a func- An Ag/AgCl reference electrode for the ERG was tion of depth from the parafoveal retina of both mon- sewn into tissue outside the orbit. Arterial blood pa- rameters were measured and controlled by adjust- ments of the respirator and composition of the in- spired air. During data collection, PaO2 was in the A range of 94 to 120 mmHg; PaCO2 was in the range of 19-38 mmHg and pHa was between 7.37 and 7.45. Oxygen tension (Po2) was measured with double- barreled oxygen microelectrodes constructed and cali- brated as previously described.6 Microelectrode pene- trations of the retina were made in both animals be- tween the fovea and the optic disk (parafoveal), using changes in the local ERG recorded by the second barrel of the electrode as an index of penetration. In M. nemestrina, recordings were also made in the fovea. Zero percent depth was taken to be the point at which the retina was first touched, indicated by a transient deflection in the signal from the voltage barrel, and 100% depth was indicated by the transepithelial po- tential across the retinal pigment epithelium. The data shown and the analysis of oxygen consumption are based on continuous withdrawals of the electrode from the choroid to the vitreous in l-/*m steps at 2 jtim/sec. Electrode penetrations were always made under dark-adapted conditions. Electrode with- drawals were done either in dark adaptation or when the retina was adapted to a steady light sufficient to saturate the b-wave of the vitreal ERG (7.9 log equiva- lent quanta (555 nm)/deg2-sec). All distances have been corrected for a penetration angle that was as- sumed to be 45 deg with respect to the retinal surface, and are therefore approximately radial distances. For both animals, we used the special three-layer model of oxygen consumption developed for the cat retina and described previously.3>5>7 In this model, profiles of Po2 as a function of distance in the outer half of the retina are fitted to a one-dimensional diffu- 100 90 B0 70 60 50 40 30 20 10 0 sion equation in which oxygen consumption (Q) is confined to a single small region between two non- Percent retinal depth consuming regions. For the foveal data, in which there FIGURE l. Profiles of oxygen tension as a function of depth is no retinal circulation, the entire thickness of the obtained during electrode withdrawals from the parafoveal retina was modelled. Because the model yields values monkey retina. (A) Profiles from the light- and dark-adapted for Q/Dk, values for D (diffusivity of oxygen in the retina of M. fascicularis. (B) Profiles from M. nemestrina. Dots retina) and k (oxygen solubility) must be assumed to indicate dark-adapted profiles. Downloaded from iovs.arvojournals.org on 09/30/2021 518 Investigative Ophthalmology & Visual Science, March 1993, Vol. 34, No. 3 keys in light and dark adaptation. In general, these to the fovea in terms of retinal thickness or domina- were similar to those recorded in the cat. The choroi- tion by cones, we wanted to record from this area in dal Po2 was 53.4 ± 5.4 mmHg (n = 10 profiles) in one the primate. The electrode was positioned in the avas- animal and 83.6 ± 6.5 mmHg (n = 19) in the other. A cular part of the fovea under ophthalmoscopic obser- gradient of Po2 was observed as the electrode was vation, with the local ERG being used to confirm its withdrawn from the choroid, with the slope being position. In the fovea, the receptor potential has a greater when the retina was dark-adapted. The direc- greater influence on the shape of the local ERG than tion of the gradients indicated that the choroidal cir- in other regions.8 Examples of the dark-adapted local culation supplied the oxygen for the entire outer half ERG in response to 4-sec flashes of diffuse light are of the retina in the light. During dark-adapted condi- shown in Figure 2. Figure 2A shows responses in the tions, however, there was a flux of oxygen from the parafovea at two retinal depths, while Figure 2B shows retinal circulation to the outer retina in 11 of the 12 responses from the fovea at similar depths. At shallow profiles. The diffusion model allowed us to calculate3 depths, the parafoveal response shows a negative-go- that 8.9 ± 6.8% (n = 12) of the oxygen consumed by ing b-wave followed by the positive-going c-wave, while the photo receptors came from the retinal circulation. the foveal response has a positive-going sustained re- The minimum Po2 observed in the outer retina during ceptor potential in addition to the c-wave, and there is dark adaptation was higher than that in the cat retina, no distinct b-wave. Deeper in the retina, the receptor in which it is typically almost zero, even during nor- potential plateau is of larger amplitude in the 2 moxia.
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