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Aging and Degeneration of the Human Macula. 1. Outer Nuclear Layer and Photoreceptors

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Br J Ophthalmol: first published as 10.1136/bjo.65.1.23 on 1 January 1981. Downloaded from British Journal of Ophthalmology, 1981, 65, 23-28 Aging and degeneration of the human macula. 1. Outer nuclear layer and photoreceptors SAMUEL GARTNER AND PAUL HENKIND From the Montefiore Hospital and Medical Center, Albert Einstein College of Medicine, New York, USA SUMMARY In a light microscopic study of the macula of 104 human eyes obtained at necropsy of patients aged 3 to 96 we found: (1) Displacement of nuclei from the outer nuclear layer into the outer plexiform layer occurred in small numbers early in life and markedly increased after age 30. (2) Displacement of nuclei from the outer nuclear layer to the layer of rods and cones was rare in early life but increased considerably after age 40. (3) Displacement of nuclei is probably secondary to shrinkage of their attached fibres and is associated with aging. (4) Displaced nuclei apparently undergo changes in size, shape, and chromatin content and may go on to necrosis. (5) Twenty-four of the 104 eyes studied had an obvious reduction in the numbers of nuclei in the outer nuclear layer and their photoreceptors in the macular zone. All were in eyes from patients over age 40. No concomitant defect was found in the subjacent pigment epithelium, Bruch's membrane, or the choriocapillaris. The loss of nuclei of the outer nuclear layer appears to be a primary retinal disorder associated with aging. We found in the macula a loss of nuclei from the fovea and parafoveal zone. Its outer boundary was outer nuclear layer (ONL) which increased with age. the point where the ganglion cell layer was less than This loss apparently starts with displacement or 2 cells thick. Sections were examined by light micro- http://bjo.bmj.com/ migration of nuclei from the ONL into the outer scopy and the total numbers of displaced nuclei in plexiform layer (OPL) and into the layer of rods and the macula counted for each section. At least 3 cones. This observation has received little or no slides of each eye were examined and the results attention and we could not find any previous averaged. The data were graphed (Figs. 1 and 2). systematic study in the literature. Results Material and methods on September 30, 2021 by guest. Protected copyright. The normal nuclei in the ONL appear uniform with One-hundred-and-four eyes obtained at necropsy a circular or slightly ovoid shape and contain many from patients aged 3 to 96 were selected for study fine chromatin granules. Several layers of cone because sections included the macular region. Fifty- nuclei are concentrated at the fovea. Elsewhere in two of these eyes had sections through the fovea. the macula cone nuclei are near the external limiting Only eyes without significant inflammatory or degen- membrane and appear slightly larger and paler than erative disease or trauma were studied. Eyes with the rod nuclei. disciform degeneration or with pigment migration The number of nuclei in the ONL does not remain into the retina were excluded. The eyes were opened constant during a long lifetime. Significant changes in the horizontal meridian so that sections included are found with aging. Some nuclei from the ONL the disc and macula. They were prepared with celloi- become displaced into the OPL (Fig. 1) and others din embedding cut 14 rum thick and stained with into the layer of rods and cones (Fig. 2). haematoxylin and eosin. The macula includes the Displacement of nuclei into the OPL at the macula is evident even early in life but increases Correspondence to Professor Paul Henkind, Montefiore after age 30, and is most pronounced after age 50 Hospital and Medical Center, Albert Einstein College of (Fig. 1). The nuclei displaced into the OPL appear Medicine, 111 East 210 Street, Bronx, New York 10467, USA. to be mainly rod nuclei from the ONL and perhaps 23 Br J Ophthalmol: first published as 10.1136/bjo.65.1.23 on 1 January 1981. Downloaded from 24 Samuel Gartner and Paul Henkind NUCLEI DISPLACED TO OUTER PLEXIFORM LAYER 4-151 6-67 6-65 16-65 TO-s 104 Eyes l l 1l 87 Patients l 50- 7-42 6-47 r1 T T (411 5-37 z (39.31 Averoge Number of hi Fig. 1 Nuclei displaced into Nuclei ( ) 2-31 28.7) (28.0 outer plexiform layer. z a 30- N . 0-24 (24.4) F1) .I (23) 10I F- I IlI 10 20 30 40 50 60 70 60 90 100 Age 6 5 11 10 21 20 17 9 4 Eyes 3 16.3 25.4 33 43.1 54.5 65 7Z. 5 4.3 91 Average Age NUCLEI DISPLACED TO ROD AND CONE LAYER 1-131 0-171 0-57 I 60- T 1-44 http://bjo.bmj.com/ Q 104 Eyes 40 Average Number of 67 Potients ( 36.1 ) 6. Nuclei ( ) Fig. 2 Nuclei displaced into IL r r 0-26 0 rod and cone layer. T (19.6) =11a 20- (11.5) (4.1) z -_F 0-7 on September 30, 2021 by guest. Protected copyright. 0-2 016 [. 10 20 30 40 50 60 70 60 9 100 Age 6 5 11 10 21 20 17 9 4 Eyes 3 16.3 25.4 33 43.1 54.5 65 72.5 84.3 91 Average Age some nuclei from the inner nuclear layer (INL) fovea and was noted mainly in the rest of the (Fig. 3). macula (Figs. 4a and 4b). Displacement of nuclei from the ONL through the Nuclei displaced into the layer of rods and cones external limiting membrane to the rod and cone lose their normal configuration and often appeared layer has been described as a normal variant enlarged and oval with their long axis parallel to the observed most often in the macula.1 However, such rods and cones. The nuclei displaced in the OPL displacement is rare in youth (Fig. 2). Only after age varied in shape. A few retained their spherical form, 40 is it frequent, being most common after age 50. while many became elongated with their long axis A decrease in such nuclei was noted after age 70. parallel to the oblique nerve fibres of Henle's layer. Nuclear displacement is rare in the centre of the A number were enlarged and pale, some appeared Br J Ophthalmol: first published as 10.1136/bjo.65.1.23 on 1 January 1981. Downloaded from Aging and degeneration of the human macula 25 very irregular, and a few seemed necrotic. In several Ng instances we observed similar degeneration of nuclei , within the ONL. Twenty-four of the 104 eyes studied had discrete M areas in the macula with an appreciable loss of nuclei in the ONL. The loss was extensive in 9 and moderate in 15 eyes (Table 1 and Figs. 5 and 6). The loss was usually in small focal areas, but some eyes had a broad zone with a diminished number of , nuclei. The loss of nuclei was usually found opposite normal or only slightly defective retinal pigment Fig. 3 Male age 63. Parafoveal zone. There is a large number of displaced nuclei in the OPL. Most of these nuclei are pale, deformed and elongated and lie parallel to the obliquity of the fibres in Henle's layer. Some nuclei in the ONL are elongated and deformed. Some of the photoreceptors have lost part or all of their outer segments. (H and E, x 15). .~"':.m~~ ~ ~ ~ ~ ~~~~0 V ~ ~4:~ *.::: http://bjo.bmj.com/ ,~, ~ Figs. 4 upper and lower. Female age 54. Parafoveal zone. """''~~~ Many nuclei from the ONL are displaced into the inner layer- of rods and cones. Somne of the displaced nuclei have lost their on September 30, 2021 by guest. Protected copyright. regularity and are elongated ~~~~* and paler than in the ONL. The ...... ......... .................-w.w... .,.......;............ g......... rpigm'entp epithelium and Bruch's ~ a444. * '* * ,~ ~ membrane appear normal. The *~~//Z.../''~#~I&"/~..~ ~ ~ .,.~ choriocapillaris has marked ..- .. ..,.. thickening of its anterior and lateral,walls. (Upper. H and E xiS5; ower: HandE, x 38). Br J Ophthalmol: first published as 10.1136/bjo.65.1.23 on 1 January 1981. Downloaded from 26 Samuel Gartner and Paul Henkind ........... Fig. 5 upper, right eye; lower, left eye. Female aged 41. Parafoveal zone. The ONL is markedly thinned and centrally is only 1 cell thick. The OPL is also narrowed. Many photoreceptors are deformed and shortened with a loss of outer segments. There is a mild degree of irregularity of the retinal pigment epithelium with slight depigmentation. Bruch's membrane and the choriocapillaris appear normal. In Fig. Sb there are numerous displaced nuclei in the rod and cone layer. (H and E, x lS). http://bjo.bmj.com/ on September 30, 2021 by guest. Protected copyright. epithelium, Bruch's membrane, and choriocapillaris. Table 1 Loss ofnuclei in outer layer in 104 eyes Accompanying the loss of nuclei in the ONL we nLoted shrunken and deformed rods and cones a Marked Moderate and Numbers loss of loss of °/ diminution in the numbers of photoreceptors (Figs. Age ofeyes nuclei nuclei Affected 5 and 6). The reduced population of cells in the ONL Before age 40 23 0 0 0 resulted in a loss of the axons traversing the outer plexiform layer, and that layer appeared thinner than 40-49 10 3 2 50 normal (Fig. 4). 50-59 21 0 7 33k Three of the 24 eyes with marked loss of cells from 60-69 20 2 2 20 the ONL had interesting fellow eyes.
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