THE RETINAL MIRROR REFLEXES

By Ejle i - Holm.')

The mirror reflexes have, of course, been noticed and described soon after the discovery of ophthalmoscopy. They were submitted to closer study by Dimmer (1891). Since that time the examinations have become easier and more exact by the electric ophthalmoscope, and Vogt (Klin. Monatsbl., vol. 66, 838, 1921) with the help of red-free light was able to make finer observations. It may therefore be useful to submit such a question to renewed examination, whence I have focussed more attention than before on these reflexes. I have essentially performed examinations in the erect image, which permits of more exact observations and of varying the experimental condi- tions. Whereas, in the inverted image, the circumfoveal reflex for example on the whole is more distinct, it is easier in an erect image, by moving the ophthalmoscope in front of the pupil, to get the reflexes to move and to elicit them in dif- ferent places so as to afford an impression of the level of the retinal surface. A large pupil therefore is also more appro- priate for the study.

A s is known, the mirror reflexes chiefly arise from the surface of the retina and from the vessels. Whereas these latter reflexes are very constant, being observed at any age, the sur- face reflexes are best and strongest in children and adolescents; it is unknown to what that is attributable. They are essentially observed round the posterior pole, the condition for their be- coming visible being that the light is reflected through the pupil. The plane of the retina must thus be at a fairly right angle to the axis of the eye in order to be visible. A real image - -

* ) Read in the Ophthalm. Soc. in Copenhagen Decbr. 1948.

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of the source of light is not seen, that is only possible on the bottom of the fovea, which acts as a concave mirror.

Apart from the macular region the surface reflexes a r k from approximately plane surfaces, with small deviations which are essentially caused by the larger vessels. On these nearly plane surfaces the reflexes move, when the mirror is moved before the pupil. Thus they acquire a somewhat fleeting character, appearing and vanishing according as the ophthal- moscope is moved.

Where there are deepenings or prominences, they beconie more persistent, however, although they move a little with the angle of incidence of the light. The size of the pupil therefore is of great importance for the look of the reflexes: in case of dilated pupil they are more diffuse, and they can be elicited on larger surfaces, whereas, in case of narrow pupil, they are more confined and sharp, only being visible where there are greater changes of level, whence the circumfoveal reflex is more exactly circular and more sharply limited.

The surface reflexes are white and, particularly in children, they have a delicately chagreened, moirk-like appearance, which may possibly be explained by delicate unevennesses cor- responding to the sustentacular fibers of the retina on the internal limiting membrane. Now they follow the movements of the mirror, now they move in the opposite direction accord- ing as they come from convex or concave surfaces. They often stop at the border of a vessel or, sooner, a little outside it, because here the surface rises, but they may even send elonga- tions across the vessel or follow it so as to cover it partially.

Besides these movable and very varying reflexes there are, as was mentioned, the two more constantly occurring and located reflexes, namely: the foveolar reflex from the bottom of the fovea and the circumfoveal reflex. Of both of them thc names macular reflex and foveal reflex are used, whence it is unpractical to use these names. The foveolar reflex as a rule is small and sharp, being observed longest at advancing age : the circumfoveal reflex forms a circle which indicates the- thickest place of the retina, i. e. the highest place of its central area, and it is sharply confined towards the fovea, whercas, outward, it may continue in the surrounding flat reflexes,

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The foveolar reflex moves in the direction opposed to the movements of the mirror, sometimes reflecting the source of light so distinctly that, if the ophthalmoscope mirror is per- forated, the hole is seen as a dark spot in the center of the reflex. Perhaps that is the reason why, in older books, the reflex is described as being sometimes circular. It may even be found to be reported that, on stereoscopic photographs, the reflex is seen lying in the vitreous body before the foveola (Bedell, Am. J. of Ophth., vol. 29, 1946). That is likewise ob- served in a binocular ophthalmoscope. However, there is no doubt that that is due to an optical delusion elicited by the reflex in the two pictures acquiring a different location on the retinal surface. In the same way will it be possible to see reflexes from a convex surface as issuing from a place behind this surface. In some cases the bottom of the fovea is less regular, and produces a deformed or double reflex without that acquiring any pathological importance.

On the oblique plane between foveolar reflex and the cir- cumfoveal reflex generally no reflection is seen, exceptionally only a sector-shaped reflex, which peripherally fuses with the circumfoveal reflex. This reflex according to Kreiker (v. Grae- fes Archiv f . Ophth., vol. 123, p. 446, 1930) almost always lies nasally; a single once I have seen it lying temporally. It shows that the fovea in these cases has an oblique position, and if the reflex is regularly sector-shaped, that means that the fovea is infundibuliform.

The circumfoveal reflex is not so constantly seen as the foveolar reflex, and its appearance and intensity vary accord- ing to the conditions. It may happen that, in case of narrow pupil, it is observed as a thin, regular, and sharply delineated, shining white ring which, when the pupil is dilated, becomes faint and diffuse or is merely seen partially. I t must therefore be borne in mind that nothing can be inferred from the dif- ference of the reflexes in the two eyes, unless the pupils are of equal size. In young individuals with many reflexes it may also fuse with the surrounding flat reflexes so that they a re only seen stopping suddenly and sharply at the border of the fovea.

At the papilla narrow reflexes may often be seen, which

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indicate a slight prominence as a rule closely outside its border. Best known and the most pronounced is the so-called Weiss’ reflex at the nasal side of the disk in myopes, indicating a special prominence, the so-called myopic nasal neuritis, whereas the temporal border is flattened. In myopes very few reflexes are seen between papilla and fovea, whereas, normally, some fine, though sharp small reflexes may often be seen at the temporal side of the disk in an area extending half-way to fovea. They consist of numerous small, short, vertical, paral- lel lines. They have been described by Vogt (1921) who saw them best in young individuals with undilated pupils and in red-free light. Sometimes they are also seen closer to the fovea, and very luminous in the circumfoveal reflex. Vogt explains them by the existence of some preretinal or super- ficial delicate retinal folds, which in the red-free light are seen to form a fine lattice-work with the streaks of nerve fibrils.

Also with an ordinary electric ophthalmoscope these re- flexes are seen to be very sharp and strong, I have seen them particularly sharp in a case of retrobulbar neuritis, but as was mentioned, they belong to the reflexes occurring in normal individuals.

Finally, outside the circumfoveal reflex there may some- times be seen the so-called Frost’s or >>metallic<< dots, which according to Kreiker are mostly found above the circumfoveal reflex. At some movement or other of the mirror they suddenly appear as a group of luminous dots which, at the slightest movement, disappear again simultaneously.

The diagnostic importance of the retinal reflexes in eye diseases is somewhat limited because, as a rule, nothing can be inferred from the absence of reflexes in somewhat older individuals, but in some cases they may be useful for the estimation of the retinal surface, whether there is a promi nence or a depression. They are of special diagnostic signi- ficance in cases of edema in the macular region. Such an ,edema manifests itself partially by the retina becoming slightly .opaque, partially by the appearance - also in older persons

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- of many irregular reflexes showing that the surface has hecome uneven, as it were, wrinkled. In light cases, at the occurrence or at the disappearance of the edema, the circum- foveal reflex is seen to dissolve into a ring of radial reflexes. In severer cases it disappears entirely, and the mentioned wrinkled reflexes are observed in the entire area with the ex- ception of the bottom of the fovea, where the red spot con- tinues to be visible, eventually with preserved foveolar reflex. In uncomplicated cases the visual acuity persists normal, and in a case of sympathetic ophthalmia I have seen these reflexes persisting for a whole year, and subsequently disappearing gradually, whilst the visual acuity kept normal all the time. In the beginning this case also presented papilledema. The eye was almost always injected, and there were but few pre- cipitates ; periodical exacerbations rapidly yielded to intra- muscular injections of milk.

In case of degenerative affections of the macula there usual- ly is no macular edema, whereas, in more limited affections, such as choroiditis in the proximity or scotoma helieclipticum, it is frequently observed. In choroiditis the conditions acquire a somewhat irregular appearance according to the location of the choroiditis, and with reflexes which are now characterized by edema now by traction.

Recently we came across a case suggestive of the import- ance of paying regard to the reflexes. The patient was a young man who was treated for choroiditis near the fovea of his left .eye, and I discovered that there were wrinkled reflexes in the inacula region of the right eye. I did not find any other changes there, but keeping the eye under observation I a fortnight later found a choroiditis covered with a whitish retinal opacity at the inferior temporal vessels a couple of P.D. from the papilla. The visual acuity of the eye continued to be good. Oftenest this macular edema is seen as a collateral edema in affections of the anterior section of the eye, particularly in iridocyclitis. As is known, central choroiditis may likewise occur here or, though less frequently, only a central scotoma. In keratitis it may also occur, probably particularly in disci- form keratitis; I have recently seen it in a keratitis situated .close to the limbus, with folds in Descemet’s membrane, pre-

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cipitates and path of light in the chamber. Also in extrabulbar affections it may be found, we have for example seen it after an operation for squint with advancing of the external rectus, where a considerable edema of the surroundings of the eye occurred. Vogt reports having seen it as sole ophthalmoscopic sign in an accessory sinus affection, and Baillart (Ann. d’ocul- 175, 1938), after a tooth extraction.

In retrobulbar neuritis with pronounced papillitis I have seen such an edema of the nasal part of fovea, but I do not think that it is found in retrobulbar neuritis without papill- edema. Sven Llarsson has recently treated the macular and foveal reflexes in relation to affections in the optic nerve (Acta psychiatr. et neurol. Suppl. XLVI; NOLR Nr. 1010). He re- minded of Haab (1916) having seen the foveal reflexes disap- pearing in optic nerve atrophies, and of Vogt (1921) in persis- tent scotoma after retrobulbar neuritis having seen the macul- a r reflex becoming irregular and being replaced by several concentric rings. Larsson particularly mentions a case of uni- lateral retrobulbar neuritis with impairment of vision, in which normal disks and normal circumfoveal and foveolar reflexes were found by the first examination. However, after the lapse of a few months temporal discoloration was found, and both the foveolar reflexes disappeared, and the outer reflex was interrupted. This disappearance and interruption of the reflexes was interpreted as being the result of atrophy. Lars- son had not found this as a constant symptom however.

In embolism of the central retinal artery no superficial reflexes are seen, which may be explained by the rapidly oc- curring opacity of the retina not being occasioned by a pure edema. It must here be assumed that cells and tissues rapidly change and become opaque, which accords with the fact that irreparable changes in the retina appear already after about 15 minutes’ interruption. Of authors who in case of arterial embolism have carried out anatomical examinations Nettleship and others later found both edema and degeneration in the ganglionic layer, whereas others, for instance Elschnig and Coats, did not find any edema, but did find ischemic necrosis with albuminous coagulation. Whether other conditions due to atrophy are observed later, I ignore.

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Presumably it may also be ascribed to the degenerative changes that surface reflexes in the macular region are not either seen in albuminuric retinitis, perhaps, because these affections as a rule are not observed a t a sufficiently early stage. On the other hand, I have, contrary to expectation, seen them a t a n early stage of diabetic retinitis in two young indi- viduals who otherwise only presented fine hemorrhages (aneur- ysms) scattered all over the retina, and whose vision cons- tantly was good.

Finally Vogt mentions reflex changes in the macula in retinitis pigmentosa, which supports the assumption that they may be met with in atrophic conditions. In my opinion, how- ever, there is not in such cases a question of what I call wrinkled reflexes, but of irregularities and interruptions in the circumpapillary reflex. In a 55 year-old man with retinitis pigmentosa I have myself noticed that the foveolar reflex was missing, whereas the circummacular reflex was dissolved in radical sections, here sooner a consequence of atrophy than of edema.

What remains to be discussed is the mirror reflexes form- ing on the vessels. They are the most persistent reflexes, be- cause they form on walls with a strong flexure. In contra- distinction to the surface reflexes they are moreover observed throughout life, anyhow if there are no very coarse pahological changes as in embolism of the central artery and in amotio retinae. The arterial reflexes are yellowish, whereas the re- flexes on the veins are whitish just as the surface reflexes. Naturally they lie on the middle of the vessels, being absent only where the vessels wind forward as a t the issue from the vascular funnel on the papilla. On the arteries they cover about one third of the breadth, but it must be borne in mind that their width in some degree is influenced by the size of the source of light and of the pupil. On the veins they are Yery narrow, with irregular contours, presenting fine inter- ruptions on closer inspection.

Great disagreement prevails with regard to the place of formation of these reflexes. Helmholfz briefly declares that

they form in the vascular wall, whereas Dimmer opines that. in the veins, they form on the anterior surface of the blood column and, in the arteries, partially here and partially in the interior of the blood column as an expression of the axial current in the vessel. He substantiates this by the vascular. walls having about the same index as the retina, and by his having observed the blood corpuscles in the vessels of frogs as shining dots or spots. Kreiker (Klin. Monatsbl. f . Aug., vol. 72, p. 621, 1921) on the ground of studies in red-free light came to the result that they form in the retina above the res- sels. He, too, had noticed that the surface reflexes may extend to and fuse with the vascular reflexes. Both these conceptions are constantly met with in the literature, it often being men- tioned as generally acknowledged that they originate from the blood column, e . g . Gifford’s Textbook of Ophthalm. 1947. Bail- Zart (XV. Concil ophtalm. internat., Egypt 1939; Trait6 d’oph- talm. 1939) deems it probable, however, that they form on the surface of the retina, whereas Duke-Elder thinks that they are partially due to some light which is reflected from the blood column, partially originating from the vascular wall, where the most important reflecting medium is the tunica media. There is much that speaks for this latter explanation. On the other hand it is difficult to explain how a reflection from the blood column should become wider and stronger on arteries than on the larger veins. Nor are reflex spots from the blood corpuscles seen in human beings for example in slit-lamp examinations of the vessels of the conjunctiva. A reflection from the surface of the retina might sooner be thought of with regard to the veins, where the reflex is white just as the sur- face reflexes. In children these latter are, however, far stronger than the venous reflexes, and i f they, in case of dilated pupil, are allowed to pass across the retina, it is seen that they are quite independent of the vascular reflexes both in places, where their lustre shows that the surface of the vessels does not arch, and in places, where they pass on to the vessels or send offshoots along them. They may be seen to cover the venous reflex in a small zone, and then, by a slight movement of the mirror, moving away from the stationary venous reflex.

Then there are the conditions of the arteries in arterial

hypertension. Whereas the arteries become narrower, the re-- flex becomes wider - anyhow relatively wider, covering for example half instead of one third of the artery: at the same time it is intensified. It is also seen that the arteries in case of caliber change have relatively wider reflexes in the narrow places. These phenomena cannot be explained by a reflection from the blood column, and probably only by an increased reflection from the vascular wall. According to A . V . Hallum (Arch. of Ophth., vol. 37, p. 472, April 1947) it is thus possible to distinguish an arterial spasm from an organic change by the fact that the reflex on the spastic arterial branch does not increase and, perhaps, even decreases.

The increased reflection from the vascular wall in hyper- tonic retinopathy is generally explained by a hyaline degenera- tion (e. g. M . Gunn, Transact. of the Ophth. Soc. of the United Kingd. 18, 356, 1898). It is known that such a hyaline de- generation frequently is met with just in the tunica media of the small arteries, particularly in the brain and in the glomeruli of the kidney. In case of hypertension it has also been demonstrated in the retina by J . H . Friedenwald (Acad. Med. New York, Jany. 1935). In this condition small reflecting spots form in the tunica media, which make the reflex more luminous and visible in greater parts of the width of the artery at the same time as it loses its sharp delimination. In pro- nounced cases the cylindric shape of the artery thus becomes visible - by the so-called copper-wire arteries. If the de- generative changes increase with >>fibrous arteriosclerosis<(, the artery loses its mirror reflex, and the whitish, so-called silver- wire reflex appears. Here the changes are aggravated by de- generation and thickening of intima so that the blood column becomes thinner or invisible. In case of complete occlusion of an artery, which may also be due to other causes, the term silver-wire artery is often applied to the white line which persists, though, according to some authors, unjustly, at any rate when there is a question of other causes.

Finally it may be mentioned that in case of retinal degener- ations may be seen deposits of cholesterol and similar substan- ces in the retina or in Bruch’s membrane; they emit shining yellow reflexes which sometimes, when the ophthalmoscope

is moved, move so that the shape of their surface can be judged.

S urn mu r y . Survey of the conditions of the mirror reflexes on the sur-

face of the retina. The foveolar reflex sometimes reflects the shape of the source of light, and if it binocularly is seen to lie before fovea, that is due to the different position of the re- flexes on the two images. Edema of the macular region is charaxterized by irregular, >wrinkled<< reflexes in the entire region with the exception of foveola, and is often met with in case of affections in the surroundings, but also in iridocyclitis, sympathetic ophthalmia, severe keratitis, and even in extra- bulbar affections. The mirror reflexes from the vessels are explained as arising from the vascular wall, and their increase in case of hypertension, by hyaline degeneration in the tunica in ed ia.