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Studies on the Hormonal Control of Circadian Outer Segment Disc Reports Studies on the hormonal control of circadian 40 outer segment disc shedding in the rat ret- • Intact ina. MATTHEW M. LA VAIL AND PATRICIA ANN c WARD. 30 Previous work suggested that the circadian burst of outer segment disc shedding that occurs soon after the onset of 8| light in the morning might be mediated by the pineal gland. In the present study the pineal glands of albino rats were either surgically removed or deafferented by 1= 20 bilateral superior cervical ganglionectomy. Neither sur- gical procedure affected the burst of disc shedding at 2, 3, or 11 weeks postoperatively. In addition, neither hypophysectomy nor parathyroidectomy and thyroidec- 10 tomy perturbed, the burst of disc shedding. Therefore the burst of disc shedding appears to occur independent of pineal, pituitary, and parathyroid-thyroid gland control. Previous work demonstrated that a large burst 0 2 4 6 8 of rod outer segment disc shedding occurs soon (0700) (1100) (1500) after the onset of light in albino rats maintained in Hours after lighting change (Clock hours) cyclic light.' This cyclic event has now been found M 1 to occur in rods of several species,2 and cones of Dark Light several species have been shown to shed packets Fig. 1. Counts of large phagosomes in the retinas of discs soon after the onset of darkness.3'4 In rats of intact Sprague-Dawley albino rats perfused at the burst of rod outer segment disc shedding fol- different times of the lighting cycle. For all figures lows a circadian rhythm* for at least 3 days in with phagosome counts, each point represents the continuous darkness; the burst occurs at the same mean number found in ten 180 /am lengths of time without the onset of light.' The possibility of pigment epithelium in the eye of a single animal, pineal gland involvement in the regulation of disc five consecutive 180 /am lengths were examined in shedding was raised in light of two features. First, the posterior retina on each side of and beginning the pineal gland (driven by the suprachiasmatic about 400 /nm from the optic nerve head. Units of nucleus of the hypothalamus5) mediates a number variance were omitted from the graphs for clarity, of circadian rhythms through its metabolism of since they were small; most S.E.M.s were less melatonin.6> 7 Second, it is also known that reser- than ±2.3. pine blocks some circadian rhythms by depleting noradrenaline from the afferent nerve terminals in the pineal gland, which project from the superior ing the pineal gland itself. We have also examined cervical ganglia.7 Since it was found that reserpine some other sources of potential hormonal in- blocked the burst of disc shedding the morning fluence on cyclic disc shedding. We were particu- following its injection,1 the pineal gland was larly interested in the pituitary gland because it strongly implicated in the control of rhythmic disc produces several hormones, and it is well-estab- shedding. lished that the pituitary helps to regulate the cir- In the present study, we examined the role of cadian rhythm of plasma cortisol.8 the pineal gland in cyclic disc shedding by surgi- Materials and methods. The histological pro- cally removing the superior cervical ganglia bilat- cedures and methods for quantifying shed phag- erally to deafferent the pineal gland or by remov- osomes have been presented in detail else- where.1 * Further evidence that disc shedding in the rat truly Sprague-Dawley noninbred albino rats main- follows a circadian rhythm is that (1) a burst of shedding tained at the Zivic-Miller Laboratories (Allison still occurs in the morning on the twelfth day of continu- Park, Pa.) were used for the studies. The rats were ous darkness (LaVail, unpublished observations) and (2) kept on a 12:12 light-dark cycle, with the onset of constant light abolishes the burst." light at 7:00 A.M. and an in-cage illuminance level 0146-0404/78/121189+05$00.50/0 © 1978 Assoc. for Res. in Vis. and Ophthal., Inc. 1189 Downloaded from iovs.arvojournals.org on 09/27/2021 Invest. Ophthahiwl. Visual Sci. 1190 Reports December 1978 for the hypophysectomized rats which were all females. In order to allow for metabolism of any circulat- ing or stored hormones in nonablated tissues, the rats were allowed to live 2 or 3 weeks after the surgical procedures before vascular perfusion with fixative. A few of the superior cervical ganglionec- tomized and pinealectomized rats were allowed to live 11 weeks before fixation. All the experiments were carried out completely at the Zivic-Miller Laboratories, with the animals kept in the same lighting conditions from the time of surgery to the time of fixation. Results. Intact, noninbred Sprague-Dawley rats at the Zivic-Miller Laboratories showed essen- tially the same burst of disc shedding soon after the onset of light (Fig. 1) as seen in our previous work with inbred Fischer rats (Fig. 2a in Ref. 1). We could find no differences in the burst of disc shedding between the superior cervical ganglio- nectomized and pinealectomized rats or between these animals and either their sham-operated con- trols (Fig. 2) or intact animals (Fig. 1), given the variability that we see even among intact animals (Fig. 1 and Fig. 2a in Ref. 1). That is, a burst of disc shedding occurs within 1 hr after the onset of light (Fig. 3, A), and then the number of phago- Fig. 2. Light micrographs of the retinas of somes in the pigment epithelium falls to a lower, pinealectomized rats perfused at different times of basal level by about 4 to 6 hr after the onset of light the day. A, 1.25 hr after the onset of light. Many (Fig. 3, B). large phagosomes are present in the pigment Removal of the pituitary gland did not affect the epithelial cells and their processes. B, six hours rhythmic burst of disc shedding that occurred soon after the onset of light. Only a few large phago- after the onset of light (Fig. 4, A). Similarly, rats somes are present (arroivs). (Epon-Araldite sec- that had been both parathyroid and thyroidec- tions; 1 to 1.5 ju.ni. toluidine blue; x720.) tomized showed no perturbation of the burst of disc shedding (Fig. 4, B). of about 0.5 to 5 foot-candles, somewhat lower In all groups of animals, the basal level of large than in our previous work.' Surgical procedures phagosome counts at 4 to 8 hr after the onset of were performed by the Zivic-Miller Laboratories. light was consistently slightly higher than that As a check on the surgery, we noted that each of seen in our previous work.' Although this may the superior cervical ganglionectomized rats dis- have been due to the slightly lower illuminance played bilateral ptosis, and we occasionally exam- levels in the present study, it may also have been ined the brains of the pinealectomized rats to be due to the fact that the animals were of different sure the pineal gland had been removed. Other genetic strains. surgical procedures included hypophysectomy In several of the groups of animals there were (both by conventional means with the para- second or third apparent peaks in phagosome pharyngeal approach and by the additional injec- number alter the initial peak that occurred at 1 to tion of formaldehyde to destroy any residual pi- 2 hr after the onset of light (Figs. 1, 3, and 4). tuitary tissue) and removal of the thyroid- These peaks in the curves may represent only parathyroid gland complex. Intact, nonoperated variation among animals, since twofold differences control rats and sham-operated controls were also can exist among animals killed at a given time (Fig. examined. All rats were 2 to 4 months of age at the 2a in Ref. 1). Unfortunately, the inherent variation time of surgery. Both male and female rats were among animals in the rat system precludes resolu- examined with each surgical procedure, except tion of this issue. Downloaded from iovs.arvojournals.org on 09/27/2021 Volume 17 Number 12 Reports 1191 40 Superior cervical Pinealectomy ganglionectomy Sham Sham 30 ge 0 2 4 6 8 0 2 4 6 8 (0700) (1100) (1500) (0700) (1100) (1500) Hours after lighting change (Clock hours) Dark Light Dark Light Fig. 3. Counts of large phagosonies after different surgical procedures. A, Bilateral superior cervical ganglionectomy and sham-operated controls. B, Pinealectomy and sham-operated controls. The different curves represent separate experiments. Postoperation intervals were 2 weeks in B, 3 weeks in A, and 11 weeks for the dots unconnected by lines in both A and B. 40 Hypophysectomy Thyro-parathyroidectomy Sham Sham 30 20 8.1 0 2 4 6 8 0 2 4 6 8 (0700) (1100) (1500) (0700) (1100) (1500) Hours after lighting change (Clock hours) Dark Light Dark Light Fig. 4. Counts of large phagosonies after different surgical procedures. A, Hypophysectomy and sham-operated controls. Hypophysectomy followed by formaldehyde injection was used for one rat at 1, 1.5, and 7 hr after the onset of light, and the counts of these were indistin- guishable from those of conventional hypophysectomy. B, Thyroid-parathyroidectomy and sham-operated controls. Discussion. The results of this study indicate ganglionectomy data are in close agreement with that the pineal, the pituitary, and the parathyroid- those of Tamai et al.,9 who carried out similar ex- thyroid complex are not responsible for regulating periments but, for the most part, used shorter the circadian rhythm of outer segment disc shed- postoperative intervals. ding. The pinealectomy and superior cervical Although these studies do eliminate certain Downloaded from iovs.arvojournals.org on 09/27/2021 Invest.
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