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J. Neurol. Neurosurg.'Psychiat., 1949, 12,^ 219.
THE TONIC^ PUPIL BY
G. S. GRAVESON
From the Department of Neurology, Manchester Royal Infirmary
The peculiar phenomenon of the tonic pupil was
first described in detail by Strasburger in 1902. Later in the same year both Saenger and Nonne reported further cases and Saenger proposed the
name "^ myotonic pupillary^ movement"^ for the
condition. Until this time the disorder had not
been separated from others causing mydriasis^ or
alteration in^ the^ pupillary reflexes. Yet^ the curious
slowness of pupillary^ movement, characteristic^ of the condition, must^ have been^ recognized^ earlier; indeed in 1818 James Ware described a patient who
very probably had a tonic pupil. His patient,
whose pupillary abnormality had been known to
exist for at least twenty years, was " a lady between
twenty and^ thirty^ years^ of^ age,^ the pupil^ of^ whose
right eye, when she is not engaged in reading or in
working with her needle, is always dilated very
nearly to the rim of the cornea; but whenever she
looks at a small object, nine inches from the eye,
it contracts within less than a minute to a size
nearly as small as the head ofa pin ... its contraction
never remains long after the attention is withdrawn
from a near object."
After 1902 the condition was reported on several
occasions, both in this country (Markus, 1906;
Weber, 1923; Moore, 1923, 1931; and Morgan and
Symonds 1927, 1931) and abroad, but it did not
attract much attention until the, work of Holmes
(1931) and Adie (1931, 1932). To Adie in particular
must be given the credit for attempting a synthesis
of available information into a semeiological plan.
He divided the tonic pupil into^ two^ forms,^ the'
typical and^ the^ atypical, each^ of^ which^ might^ be
associated with^ absence^ of^ one^ or^ more^ tendon
reflexes, but^ with^ no^ other^ neurological^ abnormality.
Collier (1933) first called this combination "^ Adie's
Syndrome," a name which has been generally
applied ih Europe and America. In this^ country,
following Bramwell's (1936) suggestion, the double
eponymous title^ of^ the^ "^ Holmes-Adie^ syndrome"
has been perhaps more widely used.
The "^ typical "^ tonic pupil, in Adie's view, was
a unilateral disorder in which the affected pupil
was larger than normal, did not react to^ torch
light but dilated slowly in the dark, subsequently
contracting slowly in daylight, and showed a
characteristically slow contraction and relaxation
with ocular convergence. The "^ atypical "^ forms were less clearly defined but included some forms
of internal ophthalmoplegia and complete^ light
rigidity with a^ tonic convergence reaction.^ Since
Adie's description, this^ conception of^ the^ atypical
tonic pupil^ has been^ so^ far enlarged^ upon^ that,
for example, Lowenstein and^ Friedman^ (1942)
write, "^ In^ atypical^ cases^ all^ the^ modifications
obserVable in pupillary disease both of syphilitic
and other causation may be exhibited." Similarly
Alajouanine and Morax (1938) claim that between
the typical tonic pupil and the Argyll Robertson
pupil all intermediary forms are possible. If these
statements are even partly true the practical
difficulties of diagnosis which not infrequently
arise are understandable enough.
Apart from what distinctive pupillary abnormali-
ties must necessarily be found before a diagnosis
can be made, two other problems remain to be
solved: (1) the site of the anatomical lesion and
(2) the nature and specificity, or otherwise, of the
underlying pathological process. This paper is
an attempt to throw light on some of these problems.
Clinical Observations
Fifteen patients, twelve females and three^ males,
varying in age from 12 to^55 years, have^ been
studied, in each of whom^ was^ found^ evidence^ of
"tonicity "^ of^ one^ or^ more^ of the^ three^ principal
actions of the^ intrinsic^ ocular^ muscles, viz :^ pupil-
lary contraction on^ exposure to^ light and with
ocular convergence, and the ciliary muscle response
to accommodation. The detailed clinical^ findings in
these patients are set out in^ Tables^ I^ and^ II.
Symptoms.-Of the^ fifteen^ patients, eleven^ were
originally seen^ because^ of^ pupillary inequality
noticed either by themselves, their^ friends, or^ their
doctors; and four attended because^ of^ blurring
of vision with or without headaches.
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Within these limitations the range of values has been: for contraction normal (2) to 90 seconds; for relaxation 4 to 135 seconds (all measurements (^) by stop watch). Only excep- tionally did contraction take longer than 20 seconds or relaxation more than 40. Adie claimed that delay in addition to slowness of movement was the essential feature of the tonic reaction. Again, accurate assessment is difficult and probably necessitates the use of a slit lamp, which was not used in this series; but the irnpression gained has been that such delay is rather unusual and that when it occurs it is more frequently seen at the beginning of contraction than at the com- mencement of relaxation. It is certainly not always seen. One other feature of the convergence reaction has often been stressed, namely, the excessive contraction which may, so it is said, continue even after convergence has been relaxed. Miosis, by which is meant a pupil of 2-5 mm. diameter or less, was produced with convergence in eight affected ### pupils (Cases 3, 9, 10, 13, 14, and 15). However, ### the resting diameters of the pupils in these cases were never greater than 4 mm. and, since in normal eyes convergence may result in a contraction of one ### third of the resting diameter' (Kestenbaum, 1947), this miosis (^) may fairly be regarded as not very excessive. In only one of the (^) eight unilateral cases ### (Case 3) was the affected pupil smaller than the normal one at the end of convergence. Continua- tion of contraction after cessation of convergence was never seen, and it seems doubtful whether this ever occurs. ### If we exclude phases of the disorder in which the ### pupil is dilated and fixed it would seem from this ### series that the essential feature of the tonic pupil is its failure to dilate promptly when the eye relaxes from a convergence movement. This may be the ### only evidence of "^ tonicity "^ of the pupil and it ### clearly is the main justification for the term, because ### sluggishness of contraction may be, in fact, purely' ### a paretic dysfunction. Just as it is probably the ### earliest tonic feature, so it is usually the most pronounced one in a (^) temporal sense, being almost ### always of longer duration than contraction. The two movements may sometimes be equally slow, but relaxation is never faster than contraction. ### Accommodation.-Defective accommodation and ipsilateral frontal headaches^ are^ the^ only ocular ### symptoms produced by the condition. They occur ### in a few patients. In these cases the onset is fairly ### abrupt, the patient noticing that he cannot see objects clearly for a brief period immediately he looks at them. More frequently near objects only are affected in this way; less commonly distant objects are transiently blurred. Power of accom- ### modation may also be weakened as well as delayed and the near point of the eye may recede. These symptoms are associated with an enlarge- ### ment of the affected pupil and they may disappear after a^ period of weeks^ or months although the latter remains. On the other (^) hand, defects of accommodation which have^ never been^ appreciated ### by the^ patient may be^ found^ on^ routine^ testing. ### Accommodation was tested by first measuring the near (^) point of the (^) eye. Then a (^) Jaeger test (^) type ### which could be read comfortably at a distance greater than this (usually J4 to J8 at 30 cm.) was ### held between the patient's eye and a distant object ### (a chimney pot about seventy-five yards away) seen through the window of the room. He was asked to look from one to the other as the test type was removed or replaced and to say immediately when the near or distant object became sharply focused. Any delay was timed by a stop watch. Normally there is no measurable delay. In all except six ### eyes some delay was found by this method. In the sixteen eyes in which such tonic accommodation was present the delay was found on looking only ### from the far to the near object in thirteen cases; ### only from the near to the far object once; and in both directions twice. These results are unusual in two respects ; first, in the matter of their fre- ### quency, for disturbances of accommodation are generally assumed to be relatively uncommon in ### this condition; and, secondly in^ the fact that ### delay in^ focusing was most commonly seen only ### when a near object was being looked at, that is, ### during active contraction of the ciliary muscle. ### Slow relaxation of this^ muscle was rare, a finding ### at variance with^ what is^ commonly described. Delay in accommodation was, (^) therefore, usually ### the result of a feebleness of action of the ciliary ### muscle. In spite of this, however, paresis of ### accommodation, as judged by a near point greater than 20 cm., was seen in only five eyes, Cases 8 and ### 10 being most definite. This slowness of accom- modation was never as great as the corresponding slowness of^ the^ sphincter muscle during conver- gence. It^ varied from^1 to^6 seconds. ### In contrast, therefore, to the convergence reaction, true tonicity, that is, delayed relaxation, of accom- ### modation is less frequently seen than simple sluggish- ### ness of ciliary contraction. The latter is analogous to the^ few instances in which contraction of the ### pupil to light was more delayed than subsequent relaxation. Adie stated that isolated tonic ace was unknown. This is confirmed iI series and no such cases have been literature. In^ all^ the^ sixteen^ eyes^ mer there was a tonic reaction on conver absent or^ tonic light reflex,^ with^ the Case 6 in^ which^ the pupil^ was^ fixed and on convergence. In this patient tion for near^ vision-^ was^ delayed^5 there was a paresis of accommodatio 29 cm.). In brief, therefore, disturbances of tion are common, though they are ofi by the patient, and a slowness of conti ciliary muscle is found more freqai slowness of relaxation. These (^) chang seen in isolation, and their only prac in the diagnosis of the type of tonic presents as a dilated and fixed pupil. Other Pupillary Reactions.-When tightly closed the pupils may contrai persons. Usually, however, they dila the removal of the light stimulus. former reaction occurs probably whether the eyes converge behind th( Similarly tonic pupils may contract^ M are closed. This, as in^ the^ normal^ cast uncommon, having been^ seen^ only^ on^ th in the series. In^ bilateral^ cases^ it^ n marked in^ one eye than another.^ On the pupil shows the^ same^ delay in after voluntary convergence.^ In^ mos ever, the^ tonic^ pupil remains^ uncha during firm^ lid^ closure. Both Holmes and^ Adie^ mention^ tI may contract^ during^ crying.^ This^ i one occasion in Case 12, a child a became alarmed and tearful when to] were to be put in her eyes. Both being widely dilated (9 mm.), sooi down to 7 mm. and slowly dilated afte had ceased. Unfortunately this war Presumably this pupillary reaction^ i more widespread parasympathetic dis occurs in^ crying. Reaction of the Pupil to Drugs.-Th reacts normally to the conjunctival i homatropine and eserine. Alajouanin (1938) go further^ and^ state^ that^ in^ eve is a "^ precocious "^ reaction, dilatation c occurring more rapidly in the affecte( the normal eye. Lowenstein and Frie moreover, found that at a certain contraction of the^ pupil to^ eserine^ th returned. Neither of these observati( ### G. S. GRAVESON commodation confirmed. In two bilateral tonic pupils (Cases n the present 11 and 15) homatropine-^ did^ not^ produce^ full ### found in the dilatation in^ one^ eye.^ In^ all other cases^ tested, ntioned above normal results^ were^ obtained. ### gence and an^ Scheie^ (1940)^ reported^ a^ series of six^ patients^ in exception of all of whom contraction of tonic pupils occurred ### both to light with a 2i per cent. solution of acetyl B methyl ### accommoda- choline (" Mecholyl "), a concentration too weak ### seconds and t6 affect a normal pupil. His results are confirmed In (near point by Walsh (1947), who considers the test of great ### diagnostic value. A 2 per cent. solution of ### accommoda- " Amechol" (Savory and Moore) was used on all ### ten unnoticed patients-2 drops from an unstandardized dropper ### raction of the being placed in each eye. A contraction of 1 mm. ently than a after 30 minutes was seen in four eyes; of 1-5^ mm. ges are never in 2; of 2 mm. in 1 eye; of 2 5^ mm. in^ 1, and^ of ### :tical value is 5-7 mm. in 2. No response was^ found in twelve^ eyes. ### pupil which The response is therefore variable, but the^ test^ is worth applying for a positive result is of great help the eyes are when the diagnosis is in some doubt. ### Lct in normal When contraction occurred with this drug there ## ite, owing to was^ no^ change^ either^ ## in the light reflex or in the W'hether the pupillary^ response^ to^ convergence,^ but^ in^ one Whethens te patient (Case 12)^ the^ delay^ of accommodation^ was ### depends on^ ### abolished and^ the^ near^ point^ of^ the^ eyes^ reduced, ### v closed^ lids,^ and in^ another (Case^ 6)^ the^ delay^ in^ accommodation ### vhen the^ eyes was reduced. e, is relatively iree occasions Associated Loss of Tendon Reflexes.-Of the nay be more fifteen patients studied, twelve had absence of one ### ce contracted or more reflexes, one had a sluggish right ankle ## relaxation as jek, and in only two (Cases 2 and 8) were the t cases, how- reflexes normally brisk. Lnged in^ size^ Associated (^) Symptoms.-Apart from (^) blurring of hat the pupil vision and^ ipsilateral^ headaches,^ the^ Holmes-Adie was seen on syndrome^ is generally considered^ to^ be^ asymptom- lged 12 who atic.^ Holmes^ (1931),^ it^ is^ true,^ mentioned^ the ### Id thatLd that dropsdrops occurrence of^ mild^ pains^ and^ pareesthesix^ in^ the limbs at the time of onset of the pupillary disturb- icontracted ances, but Adie did not refer to them. (^) French n hrcsobntrad writers, however, have frequently^ stressed^ the srnot timed existence^ of^ obscure^ pains^ in^ many^ patients^ with is part of a^ this^ syndrome,^ pains^ which^ can^ be^ related^ neither ## charge which to^ the^ pupillary^ or^ the reflex^ changes.^ Aching ## .pains, muscle^ stiffness, cramps, and^ even^ sharp ### stabbing pains of a lightning type have been ### ne tonic pupil described in the limbs. Severe^ localized^ or^ general- ### instillation of ized headache^ of-both^ migrainous^ and^ non-specific ### ie and Morax type and unrelated to the pupillary abnormality, vry case there anginal chest pains, and pains in the throat and ### r contraction neck have also been reported (Barre and Klein, d eye than in 1934; Lhermitte, 1937; Alajouanine and Morax, ### dman (1942), 1938; Sigwald, 1941). ### stage of the^ Careful^ inquiry^ in^ this^ group^ of^ patients^ revealed ### ne light, reflex that such symptoms are, in fact, not uncommonly ### ons has been experienced (Cases 6, 7, 9, 14, and 15). Their ## 228 G. S. GR logical disease. With the one exception mentioned, no cause was found for the disorder in any of the present cases. The Anatomical Site of the Lesion Several suggestions have been made about the ### possible- site of 'the lesion causing a tonic pupil. ### The absence of any post mortem confirmation ### renders discussion purely speculative, but in spite ### of this the clinical features of the conditioA, when ### critically considered, limit the possibilities to a greater extent than theories have hitherto suggested. ### Five sites have been postulated: (1) the^ supra- ### nuclear oculomotor pathways (Lowenstein and ## Frie4,Man, 1942), (2)^ the^ hypothalamus (Kennedy ### and others, 1938), (3) the third nerve nucleus (Adie, ### 1932; Behr, 1921), (4) the ciliary ganglion and/or the ciliary nerves (Magitot, 1911), and (5) the, ### sphincter muscle (Saenger, 1902). ### Of these hypotheses, (1) and (2) may be^ dismissed at once for the absence of a light response in a unilateral tonic pupil with the retention of a con- sensual reaction^ in^ the normal^ pupil places^ the lesio'n on the efferent limb of the light reflex arc. ### Saenger's suggestion that the condition is^ a^ disorder ### of the sphincter muscle^ analogous to^ the^ myotonia of ThomsoiVs disease- may likewise be eliminated. ### The not^ infrequent absolute^ rigidity of the^ pupil ### to light, and less^ often^ to^ convergence, together with ### its normal contraction when stimulated directly by ### pilocarpine, clearly indicate that the lesion is in the ### nervous pathways controlling pupil movement. ### It seems most likely, therefore, that the lesion ### affects either the vegetative portion of the oculo- ### motor nucleus or some part of the peripheral path ### of its emerging fibres. At this point argument is ### harnpered by a lack of precise anatomical knowledge ### concerning the origin and course of fibres which ### control the pupillary reflexes. It is generally agreed ### that the Edinger-Westphal nucleus is the origin of ### fibres which subserve the light reflex. These^ run ### to the sphincter muscle via the ciliary ganglion and ### the short ciliary nerves. They are usually described ### as being unilateral in distribution. Langworthy and Ortega (1943), however, state that each nucleus supplies fibres to both oculomotor -nerves. If this ### is so, then unilateral disorders of the light reflex ### can only arise from peripherally situated lesions. ## If n6t, however, it^ is^ conceivable that^ the^ changes ### seen in^ the^ tonic^ pupil may have a^ central^ cause. ### Greater obscurity surrounds the pathway of ### fibres which govern reflex pupillary contraction on ### convergence of the eyes. Its origin is depicted ### sometimes as the caudal end of^ the^ Edinger- ### Westphal nucleus, sometimes^ as^ the^ median nucleus ### of Perlia Whence fibres run to both oculomotor nerves. Their peripheral pathway is unknown, but they probably do not pass through the ciliary ganglion. Foerster and others (1936) have shown that removal of this structure in apes abolishes the light reflex but not 'pupillary contraction on con- vergence. In man, Nathan and- Turner (1942) have similarly reported isolated light rigidity of^ the ### pupil following head injuries in^ .which it^ seemed reasonably certain that the traumatic lesions were ### peripherally situated. They suggest that conver- gence fibres may relay in the episcleral ganglia of ### Axenfeld which lie in the scleral canals in close proximity to the short ciliary nerves. In the midst of this anatomical uncertainty, any attempt to localize further the site of disturbance of the tonic pupil must remain hypothetical. There seem to be valid reasons, nevertheless, for rejecting ### Adie's theory of a central nuclear disturbance. ### The term tonic pupil conjures up an idea of pupillary ### rigidity dependent on excessive tone preventing ### sphincter, movement. Adie (1932) for instance, ### speaks of a pupil " so stiff that at the time of ### examination no reaction to light or on convergence ### is obtained "^ and, again,, visualized stimuli " stored in excess and slowly liberated" from the cells of the oculomotor nucleus so producing slowness of contraction and relaxation. These two ideas are ### mutually exclusive since the first would depend 'on ### an excessive' ahd continuous sympathetic toine, ### whilst the second implies a continuous parasympa- ### thetic discharge. ### Moreover, since-, as we have seen, a tonic pupil may be persistently larger or smaller than normal ### and is always irregular, it is difficult to conceive how these various changes may result from a nuclear lesion. ### We are therefore left with the hypothesis that the lesion lies in the (^) peripheral oculomotor pathway ## viz. in^ the^ ciliary^ ganglion or the short ciliary nerves-a suggestion first made by Magitot (1911) ### and lately revived by Scheie (1940) and Leathart ### (1942). There is much to recommend this idea, though in its simplest form it fails to explain all the changes seen. Scheie suggests that there is an ### incomplete interruption of transmission in the ### ganglion or nerves which accounts for the sluggish- ### ness or absence of pupillary contraction. 'He further suggests that this partial interruption of ### conduction results in a slow liberation of acetyl- choline at the myoneural junction which diffuses ### through the sphincter muscle and so hinders its ### relaxation. If this were so it- might be expected ## that 'pupillary contraction would start in isolated segments of the iris and spread slowly to neighbour- ### ing ones.^ In^ fact^ no-such movement occurs.^ When contraction occurs the iris widens more or less ### THE TONIC PUPIL 229 ## uniformly so that the irregularity of its margin choline at the myoneural junction prevents normal ### remains unchanged. Nevertheless the implication relaxation and results in slowness of dilatation after ### of Scheie's suggestion, namely that there are the pupil contracts. This is best' seen with the' ### probably two fundamentally distinct changes, one convergence movement which is a stronger stimulus ### in the peripheral nerve the other at the myoneural to pupillary movement. Such a biochemical ### junction, seems a new and fruitful approach to the change may fluctuate' and be responsible for the ### problem. occasional variable size of the tonic pupil from day ### We have seen that sometimes light rigidity of the to day. ### tonic pupil is complete and that there may be no The site of the lesion producing a tonic pupil is ### movement of the pupil with ocular convergence, therefore, on this view, at the efferent end of the ### no matter how intense the stimulus may be. There pupillary reflex pathway. Circumstantial evidence ### is, in fact, in such cases a paralysis of the sphincter supporting this is found in the occasional occur- ### muscle and the pupil is dilated. This can only be rence of a tonic pupil after orbital injuries. Such ### the result-of an interruption of fibre conduction, cases have been recorded by Axenfeld (1906) and ### In less severe cases the pupiL contracts only under Ohm (1907). ### intense illumination and does so slowly. This If this hypothesis is correct it follows that the ### suggests a partial interruption of conduction in the tonic pupil should always be larger tha-n normal. ### efferent fibres, and we may suppose that usually In most cases this is so, but occasionally it may be, ### this affects the short ciliary nerves to a greater smaller and sometimes even miotic. In such cases ### extent than the still hypothetical convergence fibres, there may be, in addition, a paresis of the dilator ### for in most cases convergence results in pupillary mechanism, and it may be that the same process ### movement when the light'reflex is completely or that attacks the parasympathetic fibre spreads to ### almost completely absent. The irregularity of the adjacent sympathetic nerve endings. The very ### pupil may be explained by supposing that these occasional occurrence of a partial ptosis in associa- ## changes do not affect the^ ciliary nerves^ uniformly. tion with a tonic pupil (Alajouanine and Morax, ### Sluggishness of^ contraction is, therefore,^ merely 1938; Moore, 1931) supports sucli a view. ### an indication of a partial interruption of conduction The very frequent association of the tonic pupil ### in the efferent fibre. But delayed conduction will with absent tendon reflexes raises the suspicion ### not explaiii slowness of relaxation. Here we must that the two phenomena have a common' patho- ### assume a functional disturbance^ at^ the^ myoneural logical cause and a similar underlying anatomical ### junction; that, just as^ there^ is^ a^ slow^ liberation of^ or biochemical defect. Tendon areflexia in such ### acetylcholine, so^ its^ destruction^ by cholinesterase^ cases is unaccompanied by any of the objective ### is delayed. The contraction of a tonic pupil motor or sensory changes, which in other diseases ## produced by concentrations of acetyl B methyl help to determine the site of the lesion causing loss ## choline which are too weak to affect normal pupils of reflexes. This isolation of the absent reflex, ### lends support to this suggestion, for in normal eyes however, may possibly be a point in favour of ### this substance is presumably destroyed by -the regarding it as being due to a peripheral defect. ### cholinesterase present. Whether this lies on the sensory side of the reflex ## It is, therefore, possible to construct a plausible arc, whether, for example, there is some change in ## working hypothesis concerning the underlying the str6tch receptors, or on the motor* side, as for ### physiopathological disorder which results in a instance in the motor fibre or at the myoneural' ### tonic pupil. There is, first, a disturbance of junction is, however, quite unknown. Arguing by ## conduction in pupillomotor fibres, and secondly analogy from the probable site of the lesion causing ### an alteration in the chemical changes resulting from the tonic pupil, it seems perhaps more likely that ## such stimuli at the myoneural junction. Possibly the lesion is in tlhe motor pathway, but this con- ### the latter is a sequel of the former. The conduction clusion is purely a speculative one for as yet we ### defect occurs in^ the short ciliary nerves conveying possess no knowledge, either clinical or patho- ### the light 'reflex fibres and, to a greater or lesser logical, to help in the elucidation of this problem. extent, in^ the still unknown^ convergence reflex ### fibres. As a result of this the pupil may become Summary completely immobile. More often its response to 1. Fifteen patients with tonic pupils have been ### light is impaired and sluggish so that it may only studied The variability from case to case of the ### contract slowly on exposure to a strong source Of abnormal pupillary reflexes is stressed; no single ## illumination, whilst^ its^ contraction^ on^ convergence, combination^ can be regarded as typical. ## although slow, is^ more^ readily demonstrable.^ At 2. Two types of tonic pupil may be distinguished ### the' same time a delay in the destruction of acetyl- (a) the fixed type, and (b) the ordinary type of tonic
