Photoreceptor plasticity in the albino rat retina following unilateral optic nerve section

doi:10.1016/0014-4835(92)90111-5

Experimental Eye Research

Volume 55, Issue 3, September 1992, Pages 393-399

https://doi.org/10.1016/0014-4835(92)90111-5 Get rights and content

Abstract

Rhodopsin content of the retina increased when an albino rat was moved to a lower intensity cyclic light, and decreased when moved to a higher intensity. Unilateral optic nerve section was employed to test if intact optic nerves are necessary to maintain regulation of rhodopsin when albino rats are switched between two intensities, 3 lx and 600 lx ( $12 hr 12 hr$ , cyclic light). The ability to regulate rhodopsin content was altered but not lost in the eye which had the optic nerve transected. This alteration was in the direction of incomplete up-regulation when the intensity change was from high to low, and was in the direction of excessive down-regulation when the intensity change was from low to high. This indicates that efferent fibers from the brain to the retina may be involved in the regulation of rhodopsin content. Using histological techniques, cell number and rod outer segment (ROS) length were measured: surgery alone had no effect on ROS length or outer nuclear layer thickness and in all cases ROS lengths were inversely related to habitat illuminance.

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Another possibility is that a rebound effect of the blast wave reflecting inside the holder is causing contralateral eye injury. Additionally, retinal changes in the contralateral eye could be due to direct connections from one eye to the other, a phenomenon that has been shown to occur in retinal morphology after unilateral optic nerve transection in rats (Schremser & Williams, 1992) and in retinal physiology, which shows cross talk in intact conditions as well as well as changes in cross talk with unilateral intraocular elevation and injections of tetrodotoxin (Tang, Tzekov, & Passaglia, 2016). Here, we found that cognitive deficits, as measured by Y-maze, were observed with the open holder, in which the head could move relatively freely in response to the force of the blast, but not when using the enclosed holder.
Blast-induced traumatic brain injury is the signature injury of modern military conflicts. To more fully understand the effects of blast exposure, we placed rats in different holder configurations, exposed them to blast overpressure, and assessed the degree of eye and brain injury. Anesthetized Long-Evans rats received blast exposures directed at the head (63 kPa, 195 dB-SPL) in either an “open holder” (head and neck exposed; n = 7), or an “enclosed holder” (window for blast exposure to eye; n = 15) and were compared to non-blast exposed (control) rats (n = 22). Outcomes included optomotor response (OMR), electroretinography (ERG), and spectral domain optical coherence tomography (SD-OCT) at 2, 4, and 6 months post-blast, and cognitive function (Y-maze) at 3 months. Spatial frequency and contrast sensitivity were reduced in ipsilateral blast-exposed eyes in both holders, while contralateral eyes showed greater deficits with the enclosed holder. Thinner retinas and reduced ERG a- and b- wave amplitudes were observed for both ipsilateral and contralateral eyes with the enclosed, but not the open, holder. Rats in the open holder showed cognitive deficits compared to rats in the enclosed holder. Overall, the animal holder configuration used in blast exposure studies can significantly affect outcomes. Enclosed holders may cause secondary damage to the contralateral eye by concussive injury or blast wave reflection off the holder wall. Open holders may damage the brain via rapid head movement (contrecoup injury). These results highlight additional factors to be considered when evaluating patients with blast exposure or developing models of blast injury.
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RGCs surviving ONT could be responsible for the STR residual response, although this is unlikely because less than 18% of the RGC population survive ON axotomy in the adult rat (Berkelaar, Clarke, Wang, Bray, & Aguayo, 1994; Villegas-Pérez et al., 1993) or mice (Galindo-Romero et al., 2010). In addition to RGCs, other neuronal populations, such as the amacrine cells, which apparently are not directly affected by ONT (Carter et al., 1987; Schremser & Williams, 1992; Villegas-Pérez et al., 1993), could be responsible for the residual STR, as has been shown in other species such as cat and human (Sieving, 1991), and in transgenic mice lacking RGCs (Brzezinski et al., 2005). We cannot discard the possibility that other retinal neurons such as the bipolar could also contribute to the residual STR after ONT.
Optic nerve transection (ONT) triggers retinal ganglion cell (RGC) death. By using this paradigm, we have analyzed for the first time in adult albino and pigmented mice, the effects of ONT in the scotopic threshold response (STR) components (negative and positive) of the full-field electroretinogram. Two weeks after ONT, when in pigmented mice approximately 18% of the RGC population survive, the STR-implicit time decreased and the p and nSTR waves diminished approximately to 40% or 55%, in albino or pigmented, respectively, with respect to the values recorded from the non-operated contralateral eyes. These changes were maintained up to 12 weeks post-ONT, demonstrating that the ERG–STR is a useful parameter to monitor RGC functionality in adult mice.
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This study outlines the time course of cellular changes which occur within the renewal process of the rod cell during a switch to a new cyclic intensity environment. In the following experiments we demonstrate that by using the renewal process, Sprague-Dawley rats switched to a new cyclic intensity can adjust both the length of the outer segment and the amount of rhodopsin per retina.
Previously it was established that the rod outer segment (ROS) length is not constant when animals are exposed to an intensity different from their normal environment. In the present study, we investigated how changes in ROS length were achieved by the rod cell. We noted that soon after a change in intensity, the ROSs were always shortened. This occurred when rats were switched either to a higher or lower light intensity than their rearing level. A final ROS length was achieved within 21 days (approximately two turnover periods). This length change required decreased disk removal in animals switched to a low light to achieve a lengthened ROS. In animals moved to a higher light intensity, however, disk removal rate did not change but ROS length did shorten, suggesting a change in disk addition.
It is known that rhodopsin levels are up- and down-regulated with changes in environmental lighting. In this study, rhodopsin levels of animals switched from a low, cyclic intensity of 3 lx into a more intense cyclic light, 200 lx, dropped dramatically within 7 days to the rhodopsin value of an animal reared in the higher intensity. The rhodopsin level for animals moved to a less intense light, 3 lx, gradually began to rise on the third day in the new light and reached a plateau at the level of a low intensity reared animal on day 21. Despite some oscillation, by day 28 all animals switched into a new light had achieved and sustained rhodopsin values expected for the new light intensity.
Changes in ROS length did not fully account for the measured changes in rhodopsin levels. Also, the rate of change in ROS length (μm day⁻¹) for switched animals varied throughout the time in the new intensity. Furthermore, the rate of lengthening the ROS was different from the rate of shortening the ROS. Shedding patterns for animals born and raised in 3 lx or 200 lx were the same, however, patterns did change once an animal was switched. All these data indicate that several aspects of the renewal process are involved in the modification of the rod cell to a new intensity environment.
Rod outer segment (ROS) renewal as a mechanism for adaptation to a new intensity environment. II. Rhodopsin synthesis and packing density
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Using intraocular injection of a ³H-phe and ³H-leu mixture, we found that the net synthesis of rhodopsin is light-intensity-dependent and can adjust when an animal encounters a new lighting environment. Rhodopsin net synthesis dropped dramatically in day 1, 200-lx immigrants; however, preliminary studies show that the opsin mRNA levels in these animal were the same as that found in the 200-lx-native group. This suggests that the changes in the net synthesis of rhodopsin found when an animal is moved to a higher intensity light may be controlled at some point post-transcriptionally. Microspectrophotometric measurements on single rod cells revealed that the differences in whole-eye rhodopsin levels between the two cyclic intensity groups, 3 lx and 200 lx, were also present at the single cell level. This supports previous studies suggesting that the density of rhodopsin per disc varies according to the intensity of light to which the animal is exposed. Individual rods also had differences in packing density of rhodopsin at the base compared to the tip of the same outer segment when the animal had been switched to a new intensity for one half of a turnover period (5 days). This indicates the amount of rhodopsin per disc is regulated and suggests that renewal is the process responsible for creating a modified outer segment. Animals, when switched to a new intensity, can adjust the synthesis of rhodopsin and the number of molecules added per disk to ensure the appropriate packing density of rhodopsin in the rod outer segment (ROS) disk membranes for that level of light intensity.
Alterations in light-evoked dopamine metabolism in dystrophic retinas of mutant rds mice
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In dystrophic retinas ofrds mice, which are devoid of photoreceptor outer segments, high steady state levels of dopamine were found in dark and light periods. These levels were similar to those observed in normal, BALB/c mouse retinas. Major differences were determined, however, between dopamine turnover in normal and dystrophic retinas. While substantial light-evoked elevation of dopamine synthesis and utilization was observed in normal retinas, dopamine synthesis and metabolism inrds retinas was very low and response to light was depressed. Retinal dopamine metabolism was already depressed in 2 week oldrds mice, prior to the onset of photoreceptor cell death, relative to that in age-matched BALB/c mice. At 1 month of age, robust light/dark differences in retinal dopamine metabolism were observed in BALB/c mice, while no significant effect of light was seen inrds mice. The limited ability of the dopaminergic system inrds retinas to respond to light may be due to the absence of normal outer segments. Interestingly, in oldrds retinas, although most photoreceptor cells had degenerated, a small but significant light-evoked increase in dopamine metabolism was measured. The presence of relatively high steady state levels of dopamine inrds retinas, despite the reduced dopamine synthetic activity, is maintained by a compensatory reduction in dopamine utilization. Thus, although a considerable amount of dopamine is present in therds retina, it might not be available to exert its biological functions.

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Photoreceptor plasticity in the albino rat retina following unilateral optic nerve section

Abstract

Neurosci. Res.

Exp. Eye Res.

Biochem. Biophys. Res. Commun.

Exp. Eye Res.

Comp. Biochem. Physiol.

Neurosci. Lett.

Brain Res.

Eur. J. Pharmacol.

Brain Res.

Brain Res. Bull.

Exp. Eye Res.

Exp. Eye Res.

Brain Res.

The β-adrenergic receptor and the regulation of circadian rhythms in the pineal gland

Circadian rhythms in the Limulus visual system

J. Neurosci.

Limulus brain modulates the structure and function of the lateral eyes

Science

Centrifugal fibers to the retina in the monkey and cat

Nature

Rhodopsin decreases in rat retina following optic nerve section

Invest. Ophthalmol. Vis. Sci.

Light and efferent activity control rhabdom turnover in Limulus photoreceptors

Science

Dopaminergic regulation of cone retinomotor movement. I. Induction of cone contraction is mediated by D2 receptors

J. Neurochem.

Antibodies against filamentous components in discrete cell types of the mouse retina

J. Neurosci.