Chapter 07: Effects of Extraocular Movements upon the Pupil

CHAPTER 7 Effects of Extraocular Movements upon the Pupil CONTE T A. Summary .......... ... . . . . . . . . . . . . . B. Pupillary Diamet r during ertical and Horizontal Eye Movement . . . . . . . . . . . . . . C. Ani ocorla during Lateral Gaz ("Tournay' Phenomenon") .•.................... 1. Historical Background . . . . . . . . . . . . . . . 2. ppearance . . . . . . . . . . . . . . . . . . . . . . 395 395 396 396 397 3. Course . . . . . . . . . . . . • . • • • • • • • • · • · · 4. Mechanism and Significance . . . . . . . . . • (a) Possible Optical Distortion . . . . . . . . . (b) Probable Neurologic Events . . . . . . . . (c) Incidence . . . . . . . . . . . . . . . . . . . . . (d) Physiologic Significance . . . . . . . . . . . D. The Lid-close Response . . . . . . . . . . . . . . . . 397 397 397 397 401 401 402 A. Summary The pupil often have be n aid to be affected by extraocular movement . Thi wa uppo ed to be true not only under path logic condition but in normal individual a well. In addition to the well-known mio i that accompanie convergenc during the near-vision reaction, the pupil were aid to enlarge or to con trict during vertical or horil ntal conjugate gaze. The e tatement were not accompanied by convincing evidence, and our own experiments failed to upport them. The pupil al ·o wer . aid to become unequal during horizontal gaze: the pupil in the abducted eye wa said to enlarge while that in the adducted eye contracted. Many authors until the pre. ent have con idered thi a con tant phenomenon of ·ufficient amplitude to cau e "phy iologic ani. ocoria" ("Toumay' phenomenon"). When te ted with photographic record under controlled condition thi phenomenon wa found to be a relatively rare anomaly, u ually of mall extent. It probably occurs in about 10% of the population to a degree reliably discernible under clinical conditions (more than 0.35 millimeter anisocoria). In a few individuals it is larger, with maximal changes in pupillary symmetry of up to 1 millimeter between the straightahead and deviated gaze. Since the phenomenon can be found in individuals apparently in perfect health, no pathologic significance should be construed. On the other hand, these findings should not be exaggerated by saying lateral gaze is a common (or universal) cause of "physiologic anisocoria." It is important that in the majority of healthy people lateral gaze does not cause pupillary inequality. Spontaneous blinks, lid closure evoked by sensory timuli, or attempted closure of the lids agai nst resistance each have been said to elicit pupillary movements. When experimental errors are excluded, this does not take place. B. Pupillary Diameter during Vertical and Horizontal Eye Movements Occa ionally. some rather dd notion were pubIi hed about pupillary behavi r during extra cular movement . Thu., B chterew ( I 83) aid that fa t eye movement would . hake the ptic nerve , which would transmit thi. movement mechanically to the brain tern. This, in turn. would constrict the pupil by up etting the equilibrium of pres ure within the ventricle , thereby timulating the pupillary nuclcu . lgi (1925) thought the pupil dilated during up-gaze becau e thi movement pulled on the long ciliary nerve . • while in down-gaze the short ciliary nerve. were . tretched, con tricting the pupil . Gianelli (1907) and later author believed irnilar events took place during lateral e e mo ement . Only few authors commented on pupillary reaction during vertical gaze. They aid that up-gaze brought on mydria i and down-gaze brought on mio i (Morin, 1938; Adrogue. 1939; Ri . · a. ain, 1942). In our tudie on 167 normal people wh . e ey were photographed in darkne s with infrared fla. h expo ure , we found no con i tent relation between eye movement and pupil- lary ize (Table 7-1 and Figure 7-1). The examinations consisted of series of rightand~left, up-and-down gaze, interspersed by tra1ght-ahead gaze, as follows: 10 seconds straight - 10 seconds right - 10 seconds straight - 10 seconds left - 10 seconds straight - 10 seconds up - 10 seconds straight. In 15 of these subjects down-gaze also was recorded, but the conditions were not the same as in the other directions of gaze because of the need to lift the lid artificially during down-gaze. In subjects of the series the first straighta~ead picture had t_he largest pupils. This agrees with general expenence: the subject is not yet fa_miliar with the procedure and thus tends to be wide awake and expectant during the earliest trial. Later, fami liarity and boredom reduce the degree of arousal ~nd. <:°nsequently the pupil size. In twenty-one md1v1duals the pupils were largest after 10 seconds_ of ~ight-gaze, in fourteen subjects after left-gaze, m stxteen during up-gaze, and in 107 395 396 / I. Anatomy and Physiology four ( of the fifteen when it was tried) in downgaze. All these differences were small. During lateral eye movements the eyes of twenty-four people converged slightly, and both pupils became a full millimeter or more smaller than during straight-ahead gaze. This happened four times while looking to the right, three times while looking to the left, and seventeen times d~ring both right- and left-gaze. Otherwise, the differences between readings in different direc- tions of gaze were not significantly larger than v_ariations of pupil size in the straight-ahead position. We conclude from these :findings that extraocular movements have no effect upon the average pupillary diameter, except for occasional arousal reactions when the subject works hard to look up, down, or sideways; or when an inadvertent near response accompanies the eye movements. C. Anisocoria during Lateral Gaze ("Tournay's Phenomenon") 1. Historical Background looked for so long. In 1921 Tournay said that he had never missed it in a normal subject. In 1927 he wrote a special paper to disclaim priority for its discovery and offered the French translation of an I tali an paper written by Gianelli in 1907 as the first report about the subject. This publication had escaped him in 1917, since he had been unable to conduct a literature search while in the army. Despite this honorable disclaimer, the phenomenon became established as "Tournay's phenomenon." A large and fairly diffuse clinical literature soon accumulated (Table 7-2). Opinions varied as to the precise appearance of the phenomenon, its mechanism, and its pathologic significance. Gianelli had described both pupillary dilation in the abducted eye and constriction in the adducted eye. Tournay and others found the dilation in the abducted eye much more marked than the constriction in the adducted eye; the latter was only slight and could be missing. Others insisted on the On May 22, 1917, a young neurologist, Captain Auguste Tournay of the French Army, 13th Region, presented a note "on the laws of normal isocoria and anisocoria" to the Academie de Medecine in Paris. He reported that the classical rule that the right and left pupils normally remain equal at all times and that anisocoria indicated a pathologic condition was erroneous. He had noticed that "physiologic anisocoria" can be produced by lateral eye movements: when normal subjects whose pupils were equal looked to the right as far as possible and maintained this position, the right pupil became larger than the left; and the reverse took place when they looked to the left. This also happened when the laterally placed fixation point was near, so that accommodation-convergence was elicited. This "physiologic anisocoria" in lateral gaze soon was commented upon by many others, who wondered how such an obvious phenomenon could have been over- . T T T a.of T T T T T T T 7.0{T T i6.J E E .5 Pi #2 (..38) EJr. l}. _. 0 0 #8 <t 15) ·~- i---4---4-+•"" # s • 22R L(f•29) ,0, 0-0 EII::.. . ____,,,.._..___ :0, / 'G ·1 ;• .\/ I. --·---· ·-~-#6 c,a2> r EJ- ~ . : . SRLA.TSR 'Gf . 0 .. • G> ,._. , l--t---4----t--' . 0 SR L .&. T #18 (f32) A'Y 1----t --f---1-4 SR LAT T #12 T T T T Ell-~-.., / t,-0 0-G) 01·~:0' ~ sRL1.• T #14 (f52} ·-----40 I ---t----t---t----1 S R L . .&. T s R #20 LAT I: El • El (.'40) 0 f T 0-0 '0 . l--<---4-S ff LA 'Y I I./:.· 0 (#28) SRLAT ! 5.0t 0: ::::, a. #9 1----t--f---fi--f S R LAT #7 (f35) fo>-0-0 :0 0 0\ 0 ·--i---4-1 l--t--1--t ---t SR LAT #5 I: (f 56) SRLA'Y #3 (lllf35} (#24) T _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ _ __ 4.0..,_ Figure 7-1. Pupillary diameter during different directions of gaze. Each group of measurements represents a different normal subject: # indicates case number (age and sex in brackets); a square marks the first straight-ahead gaze picture for each subject, and dot groupings above S mark the following pictures with straight-ahead gaze; circles show other directions of gaze (R for right or~ for left, as indicated on the abscissa for each subject) . An up-triangle means up-gaze, and a down-triangle down-gaze. The vertical brackets for each subject show the range of all straight-ahead pictures. Each measurement represents the ave rage of the two eyes, (R + L)/2. 7. Effects of Extraocular Movements upon the Pupil Table 7-1. 397 Pupillary diameter during different directions of gaze GAZE NUMBERS OF PICTURES TAKEN AVERAGE DIAMETER LARGEST OF SERIES First straight - ahead 167 6.54 mm 107 times Second to fifth straight 167 6.52 mm 5 times Right 161 6 . 04 mm 21 times Left 156 5 . 97 mm 14 times Up 164 6.13 mm 16 times Down / 15 opposite, namely, that pupillary contraction in the adducted eye was constant, and dilation in the abducted eye was exceptional; or that both pupils dilated, the one in the abducted more than the other. 1 These phenomena were said to occur in a long list of pathologic conditions as well as in normal subjects. Many explanations were offered, and the idea that lateral gaze will cause "physiologic anisocoria" became widespread: textbooks cautioned that it is important to have the patient look straight ahead to avoid such asymmetries; and existing anisocoria in individual cases was sometimes dismissed as possibly due to slight deviation of the eyes and therefore physiologic. We had, over the years, tried a few times to demonstrate Tournay's phenomenon with photographic, cinematographic, and electronic recording techniques, but had been unsuccessful (Figure 7-2). Sharpe and Glaser (1977) had the same experience. In a later investigation on a larger number of subjects, however, we found that it did occur in some (Loewenfeld, Friedlaender, and McKinnon, 1974). 2. Appearance Among 150 healthy persons, 89 did not have the slightest trace of this asymmetry, but in 57 cases the relation between the two pupils changed in lateral gaze (Figures 7-3, 7-4, and 7-5 and Table 7-3). As seen in Figure 7-5, the extent of these asymmetries in many of these cases was barely perceptible, and only 22 had anisocoria in excess of 0.35 millimeter, the limit of reliable detection under clinical conditions. Often these changes were asymmetric or unilateral: when the subject 1. Some of these descriptions were quite fanciful. For example, Azadeh (1957), evidently mjstaking optical distortions of the pupils in deviated gaze for actual pupil changes, claimed that the pupils varied their shape and position when the eyes were moved from the primary position, in lateral as well as in up- or down-gaze. This was thought to be due to central inhibition of different iris sectors, "synergic" with innervation of the extraocular muscles. 6 . 38 4 times looked to one side the p u pils remained equal, but on looking to the other s ide, the abducted pupil became larger than the adducted one; or the asymmetry was much more marked upon gaze to one side than to the other side. In 4 cases, there was anisocoria on looking to the right and to the left, b u t the same pupil always became larger than the other, both in abd uction and in adduction, and even on up- or down-gaze. 3 . Course In 15 individuals whom we examined repeatedly over periods of from 5 to 10 years, the results remained entirely consistent. Some of these were tested on more than 50 separate occasions. Tou rnay's phenomenon therefore is a consistent trait: when it is absent in an individual at one time, it will not appear at another time· and when it is found on one occasion, it will be seen in exactly the same way every time. 4. Mechanism and Significan ce (a) Possible Optical Distortion As the subject's eyes are turned sideways, the pupils no longer look round to the observer b u t appear as slanted ovals. However, this optical distortion is not responsible for the pupillary inequality in lateral gaze. The most telling evidence for this is that in persons whose pupils become unequal during lateral gaze, the anisocoria persists for a short time after the eyes arc moved quickly back to the primary position. When they are photographed before and after the lateral gaze effort, it can be seen that in these people Toumay's anisocoria is real (Figure 7-6); and since the eyes again look straight forward after the reaction, optical distortion can play no role. (b) Probable Neurologic Events Since the pupil in the adducted eye constricts and that in the abducted eye dilates, the simplest explanation would be that during adduction parasympathetic impu lses reach the iris sphincter, while during abduction such impulses are inhibited. This assumption appears borne out by the fact 398 / I. Anatomy and Physiology Table 7-2. "Tournay's phenomenon" YEAR AUTHOR YEAR 1926 1926 1927 Gianelli 1907 1917} 1918 192 1 1921 1921 1921 1921 1922 192 1 192 3 1924 1925 192 5 1925 Tournay Caillaud Coutela {d} Landolt {d} Magitot Tournay Blatt Chenet & Noyer Doyne Behr Igi Karbowski Terrien YEAR AUTHOR 1929 1931 Jaensch Bollack Monbrun Morin Velter Rfos Sasiain Duke Elder Bing & BrUckner Bonnet Cogan Azadeh Guillaumat Morone SharEe & Glaser Loewenield & al. 1936 1938 1938 1938 1938 1942 1949 1953 1950 1956 1957 1959 1959 1974 1977 De Rosa Sabbadini SchiffWertheimer Tournay Velter & Tournay Tournay Bing & Franceschetti Morin Aliquo-Mazzei Sciortino 1927 1927 AUTHOR 1932 1934 1935 1935} Tournay 1936 This Table is only a small sample of a large and diffuse literature; we have not made a special search and included only what happened to come our way. that Toumay's anisocoria is abolished by conjunctiva! instillation of anti-cholinergic drugs (Figure 7-4, line D). If the enlargement of the abducted pupil were due to ympathetic impulses to the dilator muscle, it should still be found in the pre ence of atropinic drugs. This finding agree with the repeated statements of Tournay and others that the phenomenon was seen in patients with cervical sympathetic paralysis. At which site within the parasympathetic reflex arc could this phenomenon be produced? The afferent pathways can be ruled out, for the phenomenon can be observed in darkness. The central neuron between the s 6-A ---1 l ,a.tet.~ 9a.ze = ma pretectal area and the oculomotor nucleus also does not appear to be involved, s ince Tournay's phenomenon is not related to consensual deficit, the earmark of imperfections in this neuron. As can be seen in Table 7-3, consensual deficit was observed in persons without Tournay's phenomenon, and the reverse. The explanation offered by Gianelli, Behr, and others, namely, that the phenomenon could be brought on by stimulation of long ciliary nerves or paralysis of short ciliary nerves brought on by torsion or traction of these nerves during extreme lateral gaze, must be rejected for several reasons. ¼101:z~ ¼=-==_, .. _.,.., __ .,.,.. .. 9 nght ie1-t ••ca::_ s- Il l " " " " ' I ll s , 6 5 =B I ll "' - •=-- l -=-==-• 9 11111111 I ll ""'"" 1111 " " ' " ' 3a$ec.l ga.z.e ri.ght "' " "' """"' "" a 1 t 6 E 5 E •==-==== =c II 111 1 111 Ill -•-•=•• ~~°1:i~-==down 111111 111 o., sec. ..- 11111111 =•·---- -=•-··- "" Ill "' "" " "' Figure 7-2. Unaffected pupillary diameter during horizontal eye movements. The records were obtained from a healthy, e mmetropic 23-year-old woman. All records were taken in darkness with the e lectronic pupillograph. At the beginning of each line the s ubject looked straight ahead at a small, dark red fixation spot about 6 feet distant. During the times indicated by the interruptions in the traces she looked as far as possible to the right or left "" '" ' "' '"" ""' ""' "" "' "" ==-~30$&. ~ gaze left "" " " ""'"' -=111 1111111 ----- -II"" -- a:::a "" ""' "' 1111 Ill - "" ~ 3;::f- ~ -=--- ---= ---- --up 1111111 111111111 1111 111 111 11111 (A and B) or up and down (C). No records were taken during these maneuvers beca use the optical distortion of the pupils would have made them meaningless. After each period of deviated gaze, the subject quickly re turned her eyes to the straightahead position while the records were resumed. As can be seen, he r pupils remained equal during a ll of these eye movements. 7. Effects of Extraocular Movements upon the Pupil Table 7-3. Pupillary asymmetries in subjects with Tournay's syndrome AGE NO . SEX ---2 M 36 - 8 ""'f2 F21 ~ ""I6 F26 17 M 22 21 M ...bl.. F ...,14_ M ~ M 24 30 23 28 ...ll.. ....M..1.?... _ 3_ ....lYLl.L ...1Jl.... ...M....ll... ....:!.Q._ M 22 ....il... M 25 44 F 24 46 :VI 22 50 ....M....£L 51 M 23 ...S&.. M 23 67 M 23 68 '""f."24 ....filL ....M..l1... ...lQ_ M 19 ...1JL l\I 23 ..IL ....M...bL .....§1_ F 22 ...filL M 22 ....fil... M 22 93 M23 / 399 PUPIL SIZE (mm)* 6.97 7 .1 5 6.23 6.75 6.60 5.06 7.68 [;i. 35 6 . 40 6.62 7.15 6 .18 5 . 85 6, 3[;i 6.59 6.69 6.94 6.52 6.89 7 . 50 5.93 6.40 6.27 6.30 4.74 7.03 6 . 58 5.64 5.82 central ANISOCORIA *** .30 R > L .30 R < L .40 R > L . 30 R > L .39 R < L .20 R < L . 20 R < L . [;i3 B. < I, .13 R > L .35 R > L .30 lP L . 23 R > L .45 R < L , 21 B< L . 45 R < L . 52 R > L .68 Il < L .20 R < L . 35 R < L .15 R < L .15 R > L . 40 Il< L . 35 R > L . 26 Il< L . 32 R < L . 30 R > L . 40 ll < L . 35 H > L .10 R > L ACA** TOURNAY n L gaze gaze SEX - - - - --- . 05 .10 .34 .40 . 03 . 20 .35 ____,_1Q_ . 10 .10 _ o_ _ o_ .05 -:zo- - ~ - 0+ - 0- - - 00 0 0 JQ_ .20 __k_ .10 .....l!:...... _ t_r_ .25 .10 JQ_ .30 ..:1.Q.._ _ o_ _ o_ ___,_§.Q_ ...Q_ .....i.L:...__ . 15 0 0 . 30 0 0 _o__ _ o_ _o_ _ s_l_ _ o_ 0 -:-io- 0 ~ ~ ~ M 22 95 -wr M22 tr 0- 0 ..:...§.Q__ -- 100 """f'""if5 105 M 59 107 M 51 109 F 26 111 F 24 112 .....E..J1.... 114 F 25 116 M 64 117 i\1 27 118 F 27 119 F 28 £ Gil _ill 122 124 _fil F M F F ...ill. 132 F 134 M .40 0 137 F .50 .30 139 M 0 ..:1.Q.._ ---1L.. sl_ .15 .:.lQ_ __ 140 M _ 142 M ~ ..:..§.Q_ _ o 143 M . 60 .:.lQ_ _ o_ __o_ .:.lQ_ _ o_ .10 ..JJi._ _ o_ sl_ 0 ~ __ 0 .10 tr .....1!lli. M ....ill. F ' 149 F central ANISOCORIA *** PUPIL SIZE (mm)* NO . AGE 32 43 18 36 54 37 30 47 70 27 22 18 15 24 6.01 6 . 25 5.48 5.40 5 . 75 6 . 55 5.73 5 . 65 5 .08 4.03 6 . 46 7.84 6 . 24 [;i ' 1~ 4.95 5 .18 7.51 5.90 3.90 6.64 6.51 6 . 51 4 . 83 6.63 6.96 7 ,6~ 7.33 6.34 . 25 R < L .4 2 R < L .55 R ,- L .80 R < L . 10 R < L .10 R> L . 20 R < L . 40 R < L . 20 R > L . 20 R> L . 24 R ?' L .69 R < L .28 R < L .19B<I, .10 R > L . 20 R< L . 43 R < L . 50 R < L .45 R < L . 21 R> L .12 R < L . 50 R < L . 96 R> L . 30 R> L .42 R < L ,22 IPL . 25 R> L . 32 H. < L TOURNAY L R --0 .20 ~ 7o .70 .70 .30 . 40 -:so ~ __ o_ ACA** l. 30 --:zo - 0~ .65 0 .80 .1 0 _,_1.Q_ _ _,_lQ_ _ o __o_ ....:.lQ_ ......d.L __ o_ _ o_ ~ . 40 . 40 .62 0 _,_lQ_ ......:.1Q_ _ .20 _ o - -0.35 ----::i5 --:-zo .25 .35 0 0 . 20 ~ __o_ _,_iQ_ .30 .1 5 .1 5 - -0.40 .70 .20 0 0 0 0 0 0 0 0 0 0 0 tr 0 tr 0 0 0 0 sl 0 tr tr 0 0 0 0 0 0 0 * Average pupil diameter = (R + L) : 2; ** ACA = alternating contrac tion anisocoria : on unilatet·al light stimulation the pupil of the stimulated eye contracts more exte nsively than the pupil of the non-stimulated fellow eye: in man and monkeys this is an anomaly: tr= barely perceptible trace; sl = slight : +=distinct; *** .1\-Iax im al values are given: for minimal values see Figure 8. Fron Loewenfeld, Friedlaender, and 11cKinnon, Amer . ~ - Opht hal . 78 : 449 - 469. Publishing Co . A.With Tournay's Syndrome o.s. O.D. & < 4.44 mm O .D. C f 10 .19'.I, ~ 4.69mm GAZER o.s. >® ♦ 7 . 17'.I, Reprinted with pernission of the Ophthalmic B.Without Tournay's Syndrome ~ & +11. 82'.I, < 4.80 mm O.D. V ~ 5.40mm GAZER < + •1.63% GAZE L O.D. o.s. O.D. O.S . 4!2) + o. o:;'.I, GAZE L o.s. <~ f 14 .12'.I, F igure 7-3. Percent changes in pupillary diameter during lateral gaze. Outline diagrams for two subjects are shown. They looked straight ahead (top graph), or about 43° to the right (middle graph) or to the left (bottom graph), for 10 seconds each. In subject A, with Tournay's phenomenon, the pupil in the abducted eye dilated while the pupil in the adducted eye constricted. In subject B, without Tournay's phenomenon, both pupils constricted slightly in right- and left-gaze, the right pupil slightly more than o.s. O.D. ~ p.43 '.I, < ~ p.o7'.I, the left. O.D., right eye and O.S., left eye; down-arrow, pupillary contraction, and up-arrow, pupillary dilation. Pupillary diameters (in millimeters) during straight-ahead gaze in darkness, are shown in the top diagrams. (From I.E. Loewenfeld, RP. Friedlaender and P.F.M. McK.innon,Amer. J. Ophtha/., 78 [1974]:449; published with permission from The American Journal of Opthalmology, c The Ophthalmic Publishing Company) 400 / I. Anatomy and Physiology The most reasonable explanation appears to be the following. When a person who has Tournay's reaction looks to the side, a few of the supranuclear impulses to the internal rectus nucleus stray to the EdingerWestphal nucleus. In horizontal gaze this supranuclear input is excitatory to the adducting and inhibitory to the abducting side. In unilateral cases such stray supranuclear innervation to the sphincter nucleus would be present on one side only. Since the phenomenon is inextensive, the slightest trace of such activity would suffice to cause it. The assumption of such anomalous co-contraction of the pupillary sphincter and the medial rectus does not appear farfetched because these two muscles co-contract during reactions to near vision. A similar explanation has been offered for the co- To begin with, the thought is awkward that these nerves should be too short to adjust to full rotation of the globe without harmful traction. And it appears unlikely that traction of nerve fibers, sufficiently strong to cause transient paresis, could be repeated many times without permanent injury. Further, why should traction in one direction (during adduction) stimulate the nerve fibers, but traction in the other direction (abduction) paralyze them? Besides, in some persons the same pupil always becomes smaller (and the other larger) in all directions of gaze; and when the lateral fixation spot is nearby, strong bilateral accommodation, accompanied by miosis, testifies to the functional integrity of these nerves during extreme lateral gaze. A. T SUBJECT 1 100. 4/20/ 1973 G'.) :•:1,-t+-}r-J-i-J,-f~r-+-r-ilr-J-~f ls ~lJ-}~J~-t+-}·+ 1 r-~1-t: R S L S R S L s n s L s u S L S R S L S R S L S R S L S R S L S R S L SHSLS jI ia:r-t=Jr.-~-t=:!;;j-t=:!::f-~-l=:;!;;jr-c::::!::fr-1:::!:::::j+ r- (+)l --l-(+)l r- -T~j--:- -i-(i.)1•-;- -I--:- -r-·j-r--- --I 'f• . .! --r + 'TJ_<+>1•-l- -T- -. ♦ + ♦ + + t· + • • • + + 6.51i:-rI--1--t(+)j 5. o_f 4 .. •a 1 + + (+.)j• + + f 100, 4 / 25/ 1973 S R S L S RS L S R S L S R S 4.0 t S R S t S R S L S R S L S R S L S R S L S R S L S 1=:::::::J-l:::!::::=:t-t:::::=::1-t:::::=:1-t:::::=:1'- t:::::!::1-t::::::::j-l::::::::j-t::::::::::j-l::'.::::J- t. i.. I!t ~-1 ♦ a.JC(+) . t -+- -T- (+) :::1 ~ - I 1 (T) <ii (+) @(i)(T) @ (i) (T) (T) (+) I .-r-l-1-.-1-J-r-j-1-rl-.-r-1-1-)-r-rr-f-1-r:-f11-1-l-r-"'1·~i-.-1 ♦ + + + + t f:/ 1• a .6-t:=:::=f- t:::::::1-t:::::;j-t:::::;j-t::::::::;;j-t=:::::1-~-l:::;!=:j-l:::!::::::l-t::::::=:i-t:o i D. 4 : 7. l f 100, 5/3/ 1973 S R S L ~ ~ ~ I; S R S L S R S L S R S L S R S L ~ ~ !,J1 ~ g; p., 6. 0 S R S L S R S L S R S L S 100, 5/3 / 1973 ! r~:Ji: ~i J,I~l1~1~ II Ji <r ijiJ<i' .l1l?rlrc1t 1jr J/f rlr1c;ill SRSLSRSLSRSLSRSL SRLSSRLSSRLSSRLSSRLSSHLS -l::::::::;j - ~-t:::=::::j- ~ - ~- t:::::::j- t:::::::::j-l:::::::::j-t:::::'.:::::f-t::'.::::::::f10-SECOND INTERVALS - Figure 7-4. Tournay's phenomenon. The records were obtained from a 45-year-old woman who had the most pronounced Tournay's phenomenon in our series (subject 100 in Table 7-3). She also had slight, variable "central see-saw" anisocoria, with the right pupil from 0.1 to 0.5 mm smaller than the left one in straight-ahead gaze. Series of experiments were done on different days, as indicated for each line. Infrared flash photographs were taken in successive sets with each picture exposed after IO-second periods of straight-ahead or of deviated gaze (10 seconds straight - 10 seconds right - 10 seconds straight 10 seconds left), as indicated on the abscissa. The right and left pupil diameters of each picture were measured and plotted, with the right pupil represented by crosses, the left pupil by dashes (interconnected by vertical lines for each photograph). For each pair of eyes, the measurement of the abducted eye was circled. The ordinate represents pupillary diameter (in mm). The broken line shows changes in average pupil size from picture to picture, (R + L)/2. A, B, and C: Tournay's phenomenon occurred in the same way in each experiment. On gaze to the right, the right pupil became larger and the left pupil smaller, and the opposite happened during gaze to the left. The experiment D was done about 1 hour af~ ter C. Both pupils had dilated in response to conjunctiva] instillation of two drops of I% Mydriacyl, an atropinic drug. The Tournay reaction was abolished. (From I.E. Loewenfeld, R.P. Friedlaender, and P.F.M . McKinnon, Amer. J. Ophthal., 78 (1974]: 449; publi hed with permission of The American Journal of Ophthalmology, The Ophthalmic Publishing Company) 7. Effects of Extraocular Movements upon the Pupil contraction of extraocular muscle drome. in Duane's yn- (c) Incidence As already mentioned, Tournay's phenomenon had been described in a large as ortment of pathologic conditions. But since it can be found in perfectly healthy individuals, there is no reason why it should not be observed in any pathologic group. To determine an unusually high incidence in particular pathologic populations would require large-scale experiment with refined techniques. These hardly appear justified because of the lack of clinical u efulness of the information. We have examined thirty patients with neurosyphilis and various pupillary syndrome and found the phenomenon five times, that is, about as often as in the normal group. Some authors have confused Tournay's reaction with the rare pathologic "abduction phenomenon. But in that (usually unilateral) yndrome, the pupil in the abducted eye constricts while the other pupil remains unaffected. In patients with the abduction phenomenon, there is third nerve paresis or palsy on the affected side, and the pupil is fixed to light or to light and near vision. The abduction phenomenon thus differs from Tournay's phenomenon in all respects. (d) Physiologic Significance Tournay's phenomenon is a relatively rare anomaly. The number of positive cases we have tabulated is probably larger than the true incidence becau e in many of the subjects a single series of photographs was taken, and an accidcntaJly coinciding hift in "central, see- aw" ani ocoria could have occurred. When this is con idered and ca es with only faint asymmetries are eliminated, the incidence of Tournay's phenomenon does not exceed 10% of the population. Does it matter whether a n asymmetry of a few tenths of a millimeter develops between the pupils during R A R I I \ , I I I \ I I I \ ' ', ...... ___ .,,,, ,,, ✓ ' \ - 401 extensive lateral gaze movements? In _te~s of viSual function or of the well-being of the subject it does not, but an important principle is involved. If a system is used 1.3 L2 I.I 1.0 .9 .8 ANISOCORIA In mm. .7 .6 .:I .4 R>L .3 .2 .I O .I .2 .3 .4 .:I R<L Figure 7-5. Anisocoria on lateral gaze among 57 normal subjects (same ubjects as in Table 7-3). Columns to the left of zero mean that during gaze to the left the left pupil became larger than the right pupil, or an existing L > R anisocotia was enhanced, or a R < L anisocoria was reduced or reversed. Columns to the right of zero mean the corresponding changes during right-gaze. The numbers given with these columns are subject numbers, as in Table 7-3. Thirty-five subjects had slight asymmetries of the Tournay type (above the broken horizontal line). These were unilateral in some cases, in others bilateral, symmetric or asymmetric. Twentytwo subjects had Tournay's anisocoria that would have been obviou under clinical conditions (below the horizontal broken line) . (From I.E. Loewenfeld, R.P. Friedlaender, and P.F.M. McKinnon, Amer. J. Ophthal., 78 [1974J:449; published with permission of The American Journal of Ophthalmology, e The Ophthalmic Publi hing Company) 'I \ I I I B \ ,, I I 4 ,--- ........, ' ,,., L .,,,.--- - ... , ' I I , ' ' ........ ____ ,,,,,, .,, I L ... ' ' I I Figure 7-6. Effect of lateral gaze on the pupils of subject 100 of Table 7-3. ~• right pupil a_nd L, left pupil, with the subject looking at the examiner. The outline drawings were made from projected image of the original infrared film, enlarged to x 10 natural size. T~e broken !ine sho~v the p_upils in darkness in the first picture, with the subJect looking straight ahead. After this picture was taken, he l?Oke~ ~bout 43° to the right (in A) or to the left (in B), and_held this po 1t1on for 14 econds. She then quickly resumed tra1ght-~head gaze, and about 0.1 to 0.2 second later the eyes were again photographed (so lid lines). Note that the pupil of the recently abducted eye (the right eye in A and the left eye in B) had enl_arged while the o~e of the recently adducted eye had contncted (the left _eye in A and the right eye in B). (From LE. Loewenfeld, R.P. Fnedlaen~er, and_ P.F.M. McK.innon,Amer. J. Ophthal., 7 [1974]:449; published with permission of The American Joumal of Ophthalmology, The Ophthalmic Publishing Company) 402 / I. Anatomy and Physiology as a measuring tool in physiologic experiments and clinical diagnosis, its limits of error should be known; and for the pupil these limits are narrow: with a total range of movement of about 9 millimeters, the pupils in most healthy people remain equal during all reactions within about 0.3 millimeters, that is, with an error of only up to ±3% of full scale. Further, the iris system is able to respond to light and to other stimuli near the sensory threshold of intensity. The elegance of this system as a biologic indicator would be lost if this great sensitivity were not coupled with stability. In other words, while it may not matter to the individual whether the pupils become slightly unequal during lateral gaze, it does matter theoretically that moderate eye movements normally will not upset the binocular symmetry and that the iris system in this regard also is orderly. Much controversy could have been avoided if it had been established firmly that in man " physiologic anisocoria" associated with eye movements, to a degree plainly visible on inspection, is a rare anomaly. D. The Lid-close Response By "lid-close reflex" most authors meant pupillary constriction occurring upon forceful closure of the eyelids, especially when the examiner held the subject's lids open. Though found in normal individuals also, this reaction was especially striking in eyes with the pupil fixed to light: blind eyes and eyes with Argyll Robertson or with tonic pupil syndromes. The phenomenon was first described by von Graefe in 1854 and later became known as the "Galassi-Gifford," "Piltz-Westphal," or "orbicularis" phenomenon. We have described this pupillary behavior in the clinical section of this book (Chapter 21), and have discussed there why we consider it artifactual, that is, not a separate pupillary response but due to an inadvertent and unconscious near-vision effort. When normal individuals close their lids (lightly or forcefully, with or without resistance), the pupils are not affected, provided that the subject continues to look steadily at a distant fixation point throughout the test, and that the test is done in darkness with the help of an infrared-sensitive viewing or recording device, so that the lid closure docs not affect the amount of light entering the eye. 8 7 Spontaneous lid blinks, likewise, elicit no pupillary movements in darkness (Figure 7-7,A), but when they are examined in light, they are followed by small pupillary contractions and redilations (Figure 7-7,B). These are caused by the short "dark periods" that result when the eye is closed by the lid. As described for the "darkness reflex" in Chapter 4, the retina gains sensitivity during such short interruptions of the light; and therefore the pupil contracts after the end of the dark period, when the light again enters the eye, as if this light had been increased. When eye blinks are provoked by menacing movements, by touching the eye, or by other sensory stimuli, the small light-induced contractions just mentioned may be suppressed, and the blinks will be fo!Jowed by psychosensory reflex dilation (Figure 7-7,C). The pupillary movements associated with .ill these different kinds of lid closure are bilateral and equal in the two eyes, even though the lid movements themselves may be asymmetric, that is, more pronounced on the stimulated than on the other side. ~+J-~-~_;:;_;:;_:;:;;;:;;;;;;:;_:;_;;_;;;_;_;:;:;;_~)J.-_-..,,_-:-..,,-:--=--=-=--.;;_;_.,;:-_.,;:-~,:-~!J~~--.....-.....-_-_-_----A 61------------------------- - ---1 Room dark 5 4 n-TI~------- 7 t 6 t 5 4 -C ::::C C Diffuse lllumlnatlon E 3 E 0.1 sec. ---+ Figure 7-7. Lid-close reactions. Pupillogram of a normal 23year-old woman. In A the room was in darkness, and in B and C in diffuse room light; c means the eyes were closed. In A and B these eyeblinks were intentional (i) or spontaneous (s). Note that they did not affect the pupils in darkness but were followed by small pupillary coo tractions when the test was done in light. In C the right eye was touched lightly with a cotton wisp (t). The contraction movement after the blink was inhibited, and the pupils dilated instead. This was an ordinary psychosensory response.