The elasmobranch pupillary response

Vision

Res.

Vol.

II.

pp.

1395-1406.

Pergamon

Press

1971.

THE ELASMOBRANCH

Printed

in Great

Britain.

PUPILLARY

RESPONSE

K.4RL I?. KUCH?JOW of Biology, College Station, Texas 77843,U.S.A.

Texas A & M University, Department

(Received2 July 1971)

INTRODUCTION

AND

HISTORICAL

THE PROBLEM of iris mobility in fishes is by no means well defined. The pupil of cyclostomes is presumably static. Despite earlier work by STEINACH(1890) and GRYNFELLT(1909), which illustrated both the presence of iridial musculature and pupillary mobility, however limited, in a wide range of teleosts, these fishes are still considered to have immobile pupils in modern texts (VVALLS,1942; LAGLER,BARDACHand MILLER, 1962), with the exception of a few forms such as Anguilfa, Rhombus, Protopterus, and the pleuronectids. The views on the mode of control of the pupillary mechanism in teleosts are diverse. There are at least 3 recognizable theories for Anguilfu: Direct excitability of the sphincter muscle, possibly mediated by the pigment contained in the muscle cell (MULLER. 1859 ; STEINACH,1892; GUTH, 1901; VON STUDNITZ,1932); an intrairidial reflex, possibly mediated by a rhodopsinlike pigment in the iris tissue (BROWN-S~QU.~, 1847; MAGNUS, 1899; SELIGER,1962); an intraocular reflex mediated by the retina or lens (BUDGE, 1852). No attempts have been made to study the dilatory mechanism of Anguilla. YOUNG (1931) showed that the dilation of the pupil of Uranoscopus scaber was controlled by the oculomotor nerve, while constriction was effected by the anterior spinal roots of the sympathetic system. The diversity of response in elasmobranchs led FRANZ (1905) to categorize them as follows: Diurnal-in which the pupil is mobile and in daylight has a round dilated condition; nocturnal-the pupil is mobile and in daylight is constricted and irregular in shape (also includes elasmobranchs with an operculum pupillare); deep-sea-the iris muscle is much reduced and immobile and the pupils are always wide. CARR&RE (1922a, b) and FRANZ (1931) leave little doubt as to the presence of both a sphincter and dilator in the elasmobranch iris. The muscle elements are epidermal in origin (C&RE, 1923) being formed from the anterior sheet of the pars iridis retinae of the optic cup. The operculum pupillare of batoids presents still other problems. CARARE (1923) found no muscle tissue in the Dasyatis operculum and considered its extension and contraction to be the result of action of the sphincter controlling the pupil. GRYNFELLT and DE~LLE (1908) found no evidence of muscular elements in the operculae of Torpedo, Dasyatis, Myliobatis, or Raja. In Raja they described a layer of columnar epithelial cells which contained a fibrillar structure to which they attributed a tonic function. FRANZ(1931) stated that there were muscle cells at the periphery of the operculum of Raju. He also found fibril-like structures in the columnar epithelium, but interpreted them as nerve endings and showed histologic evidence of the contractile nature of this epithelium. The factors controlling the pupillary mobility in elasmobranchs are not well defined. 1395

1396

KARL P.

KUCHSOW

BROWN-S~QUARD (1859) stated that the excised eyes still showed pupillary movements, implying a non-nervous mechanism. BATESON(1890) and FRANZ(193 1) found a consensual reflex in Raja, implying a nervous mechanism, which was absent in sharks. BEER(1894) found that atropin had no effect on the constriction or dilation of the Scyliorhinus pupil. FRANZ(1906, 193 1) was unable to show any efTect of atropin or electrical stimulation on the constriction or dilation of the Squalus acanthias pupil. However, he was able to obtain constriction in the enucleated eye of Squalus, Mustelus, and Raja, as well as subsequent dilation in Squahw. He proposed that the elasmobranch sphincter was non-innervated and directly excitable by light, as mediated by the brown pigment present in the muscle cells. YOIZJG (1933), working with Scyliorhinus, Mustelus, and Dasyafis, also concluded, on the basis of extirpation, denervation, and pharmacological tests, that the sphincter was noninnervated and directly excitable by light, but that the dilator was innervated by the third cranial nerve. VON STUDNITZ (1933), using similar techniques, concluded that neither sphincter nor dilator received any innervation. Thus, whereas all workers agree on the status of the sphincter, that of the dilator is unclear. There is a scarcity of data on the rate and extent of pupillary mobility in elasmobranchs. The general consensus is one of great extent but slow rate. FRANZ(1931) got inaximal constriction of a dark-adapted Scyliorhinus pupil in 2-3 min. YOUNG(1933) gave similar data for rates in Scyliorhinus and Musfelus, and also found that the Musfelus pupil partially redilated in light, following initial constriction. Von Stud&z denied this latter phenomenon. In all cases little or no indication was given of actual pupillary area or the light intensities involved. KUCHNOW and GILBERT (1967) showed the pupillary response of Negaprion breairosfris to sunlight and complete darkness. A slight redilation of the Negaprion pupil was also noted, following the initial constriction. GRUBER(1967) found that the pupil of Negaprion took about 1 hr to achieve maximum dilation in darkness, following several days exposure to total daylight conditions. The following work presents new data on the rate and extent of pupillary mobility, under controlled conditions, of a variety of elasmobranchs and attempts to reconcile the earlier opinions regarding the factors controlling the response.

MATERIALS AND METHODS All tests, unless otherwise stated, were conducted on live animals with the eyes intact. Animals were secured in a speciallydesignedholder to prevent movements,and perfused with sea water. Data were taken photographically, using experimental lighting during light adaptation and electronic flash during dark adaptation. Previous testing had shown that the flash had only a transitory effect on the TCSPXW,animals exposed to flash and control animalsachievingthe same amount of dilation in the same amount of time. A millimeterscale was positionedclose to the eye so that pupillary dimensionscould be measured and the area calculated. In all cases area was approximated to an ellipse, so that only two dimensions were measured, the diameters of the major and minor axes. Data are presented as a ratio of Area/Area,.,, to facilitate comparison among anhnals with different sized pup&. Animals were held in large tanks under a 16&r light, 8-hr darkness regime. The animals were lightadapted (2-6 hr) to room liiting or dark-adapted (1-2 hr) in complete darkness prior to testing. Dark response tests were carried out in complete darkness, light response tesestsat 5 x 104 ergs/cm2-sec. Light, provided by a Zeiss 100 W projection lamp, was condensed, focused, and reflected la-y as a 5-cm dia. disc onto the plane of the pupil. Light energy was measured with YSI Radiometer, Model 65. Data were obtained for Scyikwhinus canicula, Must&s mustelus, Dasyatis pastinaca, Mybbatis aquiia, Oxynotus centrina, and &&us blainville. A number of tests were also carried out with diffuse overhead incandescent illumination of 105-lo6 ergs/cm2-see (sufficient to get a maximum response) on Mustelas californicus. Hetero&ntas francisci, Platyrhinoidis triseriata, Rhinobatos productus, and Urolophus halleri; two species, Carcharhinusgalapagensis and Apristurus brunneus, were tested in the field aboard research vessels under natural illumination.

i-t I-

i+

diurnal deep-sea deep-sea deep-sea nocturnal

nocturnal nocturnal nocturnal nocturnal

Myliobatis aquila Platyrhitroirlis triseritrtft Rhinobatvs prohctrrs Uralophrrshulleri

* Not tested. t Data represents range of diameter in millinietcrs; -I- Present. - Absent.

-Ii-

; +

Mttsteltts colifornicus Sqttaltts blainville Oxynottts cetftritla Apristrrrtts brtrtrtwus Dasyaris pastittacrr

i-

nocturnal nocturnal diurnal diurnal

Habits

Scyliorltittits catticttla Ileferoilonttts frattcisci Carcharhitttts galapagettsis Mitsteltts ntusteltts

Species

Pupil mobile

I-II-

+ * 1 *

-

I-

-

-

_..___~...

Conscnsual rellex

-

Operculum

area was not calculated.

-

-

-t -

_ * -t

Reopening in light 30.0-0.6 25.9-4.2 76.5-7.6 64.3-74 20.2-l .3 33.5-7.0 37.6-28.8 78-5 41.2 40.6-20.7 22.0--l 2. I 28.9-8.3 5.34.0t 4.1-3.57 2.8-1.2?

~_..__~..~_~

(llld)

Range of am

50 40 118 93 50 50 44 50 42 45 31 35 37 7s 28

(cm)

Animal length

15 15 I5 10

15

60

30 * * *

I5

30 *

1 I

1 10

5 I5 2

30 60

Time for max. Time for max. dilation constriclion (min) (ruin) ._ __~. ~.~.~ ~.~.._ ~. ~__

1398

KARL P. KUCHXOW

Scyliorhinus cat&da, Mustelus mustelus, Dasyatis pastinaca, and Myliobatis aquila were used to determine the mode of control of the pupillary responses using pharmacological (d-tubocurarine chloride and

prostigmine, 1 mg/kg body weight, intravenously light stimulation techniques.

via the caudal vein), denervation,

and electrical, point-

RESULTS

A. Comparative data The main parameters of the pupillary responses are summarized in Table 1. The nocturnal selachians, Scyliorhinus canicula and Heterodontus francisci differed in both their light and dark response rates. The diurnal selachians, Carcharhinus galapagensis (Fig. 2), Must&s mustelus (Fig. 3), and M. californicus (Fig. 4) had virtually identical response rates to light but differed in their response rates to darkness. Two deep-sea selachians, Apristurus Scyliorhinus

canicula

”

5

10

15 20 25 TIME -min

30

45

60

FIG. 1. Pupillary response of Scyliorhinus car&da. L-light response, normal animal; N-dark response, normal animal; D-dark response, denervated third cranial nerve; C-dark response, curarized animal (all curves calculated means for 10 animals).

brunneus and Oxynotus centrina had immobile pupils. Squalus blainville, also deep-sea, had a very slow and limited light response. Both species of Mustelus showed a variable amount of redilation, following initial constriction. Carcharhinus showed no redilation in

the 5-min test period. The batoid pupillary area was calculated as the estimated elliptical area of the pupil, less the area of the operculum, considered as a half ellipse. Opercular and iridial excursions varied greatly from species to species. In Dasyatis pastinaca (Fig. 5), the operculum overlapped the ventral pupillary border in the extreme light-adapted condition, forming a double pupil. Opercular area varied from 11 to 80 per cent of the estimated pupiliary area in the dark- and light-adapted states, respectively. In Myfiobatis aquila (Fig. 6) the operculum fell well short of the ventral pupillary border, and occluded only 3-30 per cent of the estimated pupillary area in the dark- and light-adapted states. The Platyrhinoidis operculum was 3-lobed and in light extended past the ventral pupillary border to form a multiple pupil. In Rhinobatos and Uralophus the operculum was a single lobe which never extended past the ventral border under test conditions.

1399

The Elasmobranch PupiIlary Response

Carcharhinus

0'

2

1

galapagensis

3

4

5

TIME -min

FIG. 2. Pupillary response of Curcharhinusgulupagensis to light and darkness (mean curves fcr

3 tests on a single specimen). Mustelus

0’

mustelus

’

5

10 15 20 25 30

45

50

TIME - min

FIG. 3. Pupillary response of Mustelus mustelus (L,N,D,C, as in S. canicula). B. Mode of control of the pupillary

1. Drugs. d-Tubocurarine S. canicula and M. mustelus

mechanism

chloride

had an inhibitory

effect on the dark

response

of

(Figs. 1 and 3, C). Pupil dilation in darkness reached only 0.40 of the normal maximum. Dark-adapted Scyliorhinus were also injected. The light response was found to be unaffected. Light-adapted Scyliarhinus injected with prostigmine

dilated to a variable extent, even under overhead illumination. Control animals injected with sea-water remained constricted.

1400

Mtisteius

5

FIG.4.

10

ca!:,orrvcus I

15 20 25 TIME -min

30

Pupil& response Of Musreiusqfgiy

45

to light and

60

darkness (mean curves

for 4

-.

Dasyatis

0’ FIG.5.

’

5

L

10

.

.

pas:.naca

15 20 25 TIME-min

30

.

45

4

60

Pupillary response of Dasyatispasthaca (L,N,D, as in S. canida; mean curves for 2 animais).

In darkness, the drugged animals took about I5 min to dilate maximally, as opposed to 30 min for controIs. Dark-adapted animals constricted more slowly than controls when illuminated, and never achieved maximum constriction. 2. Denervution. Animals were anesthetized with MS222 (Methan sulfonate, 1: loo0 in sea-water), the roof of the cranium was removed and the cranial nerves were severed intracranially. Animals were tested upon recovery from the anesthttic. Severing the third cranial nerve (III) resulted in a decrease in the rate and extent of dilation in Scyliorhinus(Fig. 1, D), Mustelus (Fig. 3, D), Dasyatis(Fig. 5, D), and Myliobatis

The Elasmobranch

Pupiuary Response

Myliobatls

5

10

15 20 25 TIME -min

1401

aquila

30

FIG. 6. Pupillary response of ~yljoba~~saqtrila(L,PIJ animals).

45

60

as in 27. cattic&; mean curves for 2

(Fig. 6, D). When III was severed under overhead illumination an immediate constriction was noted in the Musrelus pupil, and occasionally for Scyliorhinus, especially when the latter was moderately dark adapted. No such constrictions were noted when the nerve was severed in Dusyatis or Myliobatis. Severing III also had a pronounced effect on constriction. The nerve of Scyliorhinus was severed in darkness and the response upon subsequent illumination took about I min to attain a maximum constriction, as opposed to 2-3 min for the normal animal. For all four species the extent of the light response was greater than for the normal eye. According to YOUNG (1933), the sympathetic system sends no branches into the head of selachians. Thus, the spinal nerves were not considered. The remaining cranial nerves of obvious interest are II, IV, V, VI. Severance of these had no effect on the dilation or constriction of the Scyliorhinus or Mustelus pupil. 3. Electrical stimulation. Animals were anesthetized with MS222, decapitated, and the heads cut bilaterally so that two sections were obtained, each containing an eye, one to be used as a control, the other for the nerve stimulation tests. The brain was cIeared away, leaving the ends of the cranial nerves exposed. A d.c. current strong enough to evoke a just noticeable twitch of the eye when the o~lomotor was stimulated was used in the tests. Stimulation of III of Scyl~orhjn~ and Mustefus, even under overhead illumination of 1 x lo3 ergs/cm2-sec., caused dilation. Complete dilation, however, was never achieved electricaily. Stimulation of III of Dasyatis or Myliobatis produced no noticeable effect. Stimulation of other cranial nerves caused no dilation. 4. Tests with a small point of light, Light from a microscope lamp was condensed and focused to a point 1 mm in dia. at lo5 ergs/cm2-sec. Animals were dark-adapted and the effect of this point of light on various areas of the iris, as well as directly on the retina, was tested. Results are summarized in Table 2. In all cases of sphincter stimulation it was also possible to get very local responses around the extreme edge of the pupil, co&red only to the region of the point of light. “1510Y il/lZ--r

KARL P. KUC~OW

l-102

Otherwise, contraction was virtually absent, as when the dilator region was illuminated, or was manifested as a general pupillary constriction with the greatest contraction occurring in the immediate field of the point of light. Thus, if the ventral sphincter field was illuminated, the entire pupil constricted, but asynchronously, the greatest contraction occurring ventrally. If the retina was illuminated, through the pupil, the entire pupil constricted rapidly and synchronously. DISCUSSION

AND CONCLUSIONS

The rate and extent of the pupillary response to both light and darkness of a variety of elasmobranchs were determined, and the nature of the factors controlling the responses investigated. The extremely mobile elasmobranch pupil, deep-sea species excepted, showed a range of response of about one order of magnitude for both sharks and rays. The rates of response, however, were relatively slow. The time to attain a maximum constriction following dark adaptation varied from 1 to 5 min for the sharks and from 15 to 30 min for the rays. Dilation was even slower, varying from 10 to 60 min from a light-adapted state. Only the semi-pelagic Carcharhinus galapagensis had a rapid dark response of 1 min. The light responses lend themselves well to FRANZ’S(1906) classification of elasmobranchs (see Table 1). The nocturnal species all reached a minimum and maintained it for the duration of the test. Two diurnal species, Mustelus californicus and M. mustelus, reached a minimum and then reopened to a varying extent. This phenomenon also occurs in the diurnal Negaprion brevirostris (KUCHNOWand GILBERT,1967), and it is possible that Carcharhinus galapagensis falls into this category, although no reopening was observed in the short time span of the tests. The deep-sea Apristurus and Oxynotus had immobile pupils, while another deep-sea shark, Squalus blainville, showed very limited mobility. TABLE 2. POINT-LIGHT TESTSON Scyliorhinus canicda

Region ihuminated

Conditions

Dilator

Sphincter

Retina

Intact eye

No noticeable response

Immediate rapid constriction, but never achieved double pupil : Stimulated region constricted most, but non-stimulated areas also contracted

Immediate rapid contraction to double pupil in 3 min

Excised bulb

No noticeable response

Same as for the intact eye

Similar to intact eye, but not always get double pupil

Excised iris

No noticeabie response

Excision always caused the pupil to constrict a great deal; stimulation resulted in intense local constriction, as well as constriction in non-stimulated regions

The reasons for this diversity in response must lie in the relative strengths of the various sphincter and dilator muscles and the development and importance of associated neural mechanisms. The absence of response in deep-sea species is probably best explained on the basis of the decline of the appropriate muscular elements and the absence of nerves. Sphincter muscles are present in the immobile iris of the deep-sea Spinax and Chimaera (FRANZ, 1913), while the iris of Heptanchus appears to be amuscular (KOGANEI,1885). YOUNG(1933) suggested that the reopening of the Mustefus pupil was due to fatigue and relaxation of the sphincter, or to a reversal of the photochemical process responsible for constriction. The fact that the pupil will close immediately upon application of slightly

The Elasmobranch Pupillary Response

1403

stronger light and constricts sharply when the third cranial nerve is cut seems to negate the possibility of fatigue. It is probable that the pupillary size at any given light level is the net result of two opposing forces, the action of the light (and nervous stimulus) on the sphmcter, and the tonus of the neurally controlled dilator. Pupillary threshold studies (KUCHNOW, 1970) on both Scyliorhinus and Mustelus have shown that the pupillary aperture is dependent on the light level and that the ins of the diurnal Mlrstefus is 2-j times less sensitive than the nocturnal ScyIiorhinus iris. Nervous control of the dilatory mechanism was substantiated pharmacologically, by denervation, and by electrical stimulation. Earlier concepts of the nervous role in smooth muscle tissue have not been concerned with a myoneural junction (VON EULER. 1959). Recent electron microscopic studies, however, on a variety of smooth muscle tissues have shown that definite nerve-muscle junctions do occur (EVANS and EVANS,1964; RICH;\RDSON, 1964; THAEMERT,1963). Curare had a definite inhibitory action on the dilatory mechanism of Scyliorhinus and Mustehu. Prostigmine, on the other hand, an acetylcholinesterase inhibltor, enhanced the dilatory process. HAJIASAKI, BRIDGES and MENEGHISI(1967) obtained dilation with topical application of acetylcholine. The denervation tests on Scyliorhinus, Mustelus, Dasyatis, and Myliobatis showed that dilation was controlled by the third cranial nerve. None of the other cranial nerves tested had any effect on either dilation or constriction. Pupillary constriction, however, was more rapid and extensive when the effect of the third cranial nerve was removed, resulting in the loss of dilatory tonus and free action of the sphincter. It is possible that there is a constant dilatory stimulus at all times. When III was severed, in both Scyfiorhinus and Mustelus, a sudden constriction resulted which probably represented the loss of dilatory tonus, present even under illumination. Electrical stimulation of III effected dilation, even under overhead illumination of 1 X lo4 ergs/cm2-sec. The tests with a point of light suggest that the sphincter mechanism does not act as a simple direct effector, sensitive only to light, as proposed by earlier workers. Light incident directly on the retina, through the pupil, caused rapid maximal constriction, both in the intact eye and the excised bulbus. A retinal-iridial reflex is suggested. A similar mechanism has been proposed for the supposedly directly excitable amphibian iris (VON CXMPENHAUSEN,1963). Moreover, light incident on a particular sphincter field caused contraction, not only in that field, but, to a lesser extent in the remainder of the iris. Electron microscopy of the iris (KUCHNOWand MARTIX, 1970) has demonstrated the presence of nemes and neuromuscular junctions in the sphincter of a variety of elasmobranchs. These findings, together with the physiological results, cast serious doubt on direct excitability to light of the sphincter fibers as the sole mechanism for constriction. Thus, for elasmobranchs in general, the pupillary mechanism appears to consist of dilatory control by the third cranial nerve, with the sphincter directly excitable to light. The possibility of retinal-reflex nervous control of the sphincter can, at present, be proposed only for Scyliorhinus and Mustelus. The relative importance of the two sphincter mechanisms, direct excitability and nervous reflex, cannot be determined with the present data, but a proposal can be forwarded on the basis of physiological response rates (Table 1). Most rapid constriction occurs in diurnal sharks, conceivably due to a greater influence of the nervous mechanism. The net result may be an initial rapid constriction in bright light, followed by a redilation as the retina adjusts to the ambient light level. Nocturnal selachians show intermediate rates and batoids the slowest response rates, both with no redilation. A decrease in the predominance or absence of nervous control in the latter is suggested.

14M

KARL P. KUCHNOW

SUMMARY

selachians, Scyliorhinus canicula and Heterodontus franc&i, constricted in 5-15 min and dilated in 30-60 min. 2. Diurnal selachians, Mustelus caiifornicus, M. mustelus, and Carcharhinus galapagensis, constricted in 1-2 min and dilated in l-30 min. 3. Mustelus californicus and M. musteius demonstrated a varying amount of pupillary redilation following initial constriction. 4. Batoid elasmobranchs required 10-15 min for constriction and 15-30 min for dilation. 5. A consensual pupillary reflex was lacking in all species tested. 6. Deep-sea selachians Oxynotus centrina and Apristurus brunneus had immobile pupils, while Squalus blainville had slight mobility. 7. The pupillary dilator muscle was found to be controlled by the third cranial nerve. 8. The sphincter muscle was found to be an independent effector to light, and under the influence of an iridial nervous reflex for at least Mustelus mustelus and Scyliorhinus canicula. 9. Evidence was found for a constant dilatory tonus under all light conditions. 1. Nocturnal

study was supported by a NATO Postdoctoral Fellowship, administered by the National Research Council of Canada and an AIBS Tables Grant at the Stazione Zoologica di Napoli. The co-operation and assistance of the administration and staff of the Stazione Zoologica is greatly appreciated. Acknowledgements-This

REFERENCES BATSON, W. (1890). Contractility of the iris in fishes and cephalopods. J. mar. biol. Ass. U.K. 1,215-216. BEER,T. (1894). Die Akkomodation des Fischauges. pprlpets Arch. ges. Physiol. 58,523-650. BROWN-S~QUARD, E. (1847). R&herches exp&rimentales sur l’action de la lumiere et sur ccIle d’un changement de temperature sur l’iris dans cinq classes d’animaux vert&br&. C.r. hebd. S&mc. Acad. Sci., Paris 25,482-483.

BROWN-S~QUARD, E. (1859). R&herches exptrimentales sur l’influence de la Iumiere, du froid et de la chaleur sur l’iris dans cinq classes d’animaux vertbbrts. J. Physlol. Path. gin. 2,281-294. BUDGE,J. (1852). uber die Bewegang &r Iris. Braunschweig. CAR&RE,L. (19%). Le sphincter de l’iris chez les s&achiens. C.r. hebd. S&c. Acad. Sci., Paris 175,409411. CARR&E,L. (192213).Le dilateur de la pupille chez les sClachien.s. C.r. hebd. S&nc. Acad. Sci., Paris 175, 50@501. CARR&E, L. (1923). Les muscles de l’iris chez les stlachiens. Archs Anat. Histof. Embtyol. 2,344-380.

Evm, D. H. L. and Evm, E. M. (1964). The membrane relationships of smooth mnscles: An electron microscope study. J. Anat. %, 37-46. FRANZ,V. (1905). Zur Anatomie, Histologie und functionellen Gestaltung des Selachierauges. 2. Nutunv. 40,697-840. FRANZ,V. (1906). Beobachtungen am lebenden Selachierauge. 2. Naturw. 41,429-471. FRANZ, V. (1913). Seheorgan. Iris. In Lehrbuch von der vergleichenden und mikroskopirchrn Anatomie der Wirbeltiere (edited by A. OPPEL),pp. 215-238. Jena. FRANZ,V. (1931). Die Akkomodation des Selachierauges und seine Abblendungsapparate, nebst Befunden an der Retina. 2001. Jahrb., Abt. A&. Zool. 49,323-462. GR~LLT, E. (1909). Les muscles de l’iris chez les t&ostiens. Bibfiphie anat. 20,265-332. GRYNFELLT, E. and DEMELLE, A. (1908). R&herches anatomiques et histologiques sur l’opercule pupillaire des poissons. Btb&hie anat. 18,119-l 35. GRIJBER,S. H. (1967). A behavioral measurement of dark adaptation in the Lemon Shark, Negoprin brevirostris. In Sharks, Skates and Rays (edited by D. P. RALL,P. W. GILBERTand R. F. MA-N), pp. 479-490, John Hopkins Press, Baltimore, Maryland. GUI-H. E. (1901). Untersuchum iiber die direkte motorische Wiikung des Lichtes auf den Sphincter Pupillae des Aal- und Froschauges. Ppuscrs Arch. ges. Physiol. 85,119-142. HAMASAIU,D. I., B-m. C. D. B. and Mteraoffpn, K. A. (1967). The electroretinogram of three species of elasmobranchs. In Sharks, Skutes and Rays (edited by D. P. RALL,P. W. GILBERT and R. F. MAT-HEWWN). pp. 447-463, Johns Hopkins Press, Baltimore, Maryland.

The Elasmobranch

KCIG~XEI,F. (1885). Untersuchungen

1405

Pupillary Response

iiber den Bau der Iris des ?vlenschen und der Wirbeltiere.

Arch.

mikrosk. Anat. 25, 117.

KXHNOW. K. P. (1970). Threshold

and action spectrum

of the elasmobranch

pupillary response.

Vision

Rer. 10,955-964.

KUCHXOW, K. P. and GILBERT, P. W. (1967). Preliminary in vivo studies on pupillary and tapetal pigment responses in the Lemon Shark. !Ve,eaorion brevirostris. In Sharks. Skates and Rays (edited by D. P. RALL. P. W. GILBERTand R. F. MA&&&), pp. 465-477, Johns Hopkins Press, Baltimore, Garyland. KIXHXOW, K. P. and &~IARTIN, R. (1970). Fine structure of elasmobranch iris muscle and associated nervous structures. Expl. Eye Res. 10, 345-351. LAGLER,K. F., BARDACH,J. E. and MILLER, R. R. (1962). Ichthyology. John Wiley, New York. IMAGNUS,R. (1899). Beitrage zur Pupillarreaktion des Aal- und Froschauges. Z. Biol. 38, 567-606. MULLER,H. (1859). Bewegung der Iris an ausgeschnittenen Fischaugen. PLrh. Phys. .tfed. Besels. CCitrzburg 10, 50-51.

RICMRDSOS, K. C. (1964). The fine structure of the Albino Rabbit iris, with special reference to the identification of adrenergic and cholinergic nerves and nerve endings in its intrinsic muscles. Am. J. &at. 114, 173-205. SELIGER,H. H. (1962). Direct action of light in naturally pigmented muscle fibers. I. Action spec:rum for contraction in eel iris sphincter. J. gen. Physiol. 46, 333-342. STEIXACH, E. (1890). Untersuchungen zur vergleichenden Physiologie der Iris. P’ijgers Arch. ges. Physiol. 47,289-340.

STEINACH,E. (1892). Untersuchungen

zur vergleichenden

Physiologie der Iris. P/Tigers Arch. ges. Physiol.

52,495--5X.

THWART, J. C. (1963). The ultrastructure

and disposition of vesiculated nerve processes in smooth muscle.

J. Ceil. Biol. 16, 361-377.

VOX CA~EX-LNSEN, C. (1963). Quantitativen Beiziehungen zwischen Lichtreiz und Kontraktion des Musculus sphincter pupillae vom Scheibenziingler (Discoglossuspictas). Kybernetik 1,249-267. VON EULER, U. S. (1959). Autonomic neuroeffector transmission. In Handbook of Physiology: Neurophysiology, Vol. 1 (edited by J. FELL, H. W. MAGOUX and V. E. HALL). Amer. Physiol. Sot., Washington, D.C. VOX STUDNTTZ,G. (1932). Beitrage zur Adaptation der Teleostier. Studien zur vergleichenden Physiologic der Iris II. Z. vergl. Physiol. 18, 307-338. VOX Srunh-rri!, G. (1933). Studien zur vergleichendrn Physiologie der Iris. III Selachier. 2. cergi. Physiol. 19,619-631.

WALLS, G. L. (1942). The Vertebrate Eye and Its Adaptive Radiation, 785 pp. Cranbrook Press, Bloomfield Hills, Michigan. YOUNG,J. Z. (1931). The pupillary mechanism of the teleostean fish, Uranoswpus scaber. Proc. R. Sot. B. 107,464-485. YOUNG, J. Z. (1933). Comparative studies on the physiology of the iris. I. Selachians. Proc. R. Sot. B. 109,228-241.

Abstract-The rate and extent of the pupillary response to light and darkness were determined for a variety of sharks and rays. Dilation required l-60 min and constriction l-30 t-nits, depending on the species. All responses were non-consensual. The dilator muscle was controlled by the third cranial nerve, which probably exerts a constant dilatory tonus at all times. The sphincter, on the other hand, was directly responsive to light for all species studied. Evidence for a retinal-iridal nervous retlex, however, was found for the sphincter of Scyliorhinus canicrtla.

R&m&-La vitesse et l’amplitude de la riponse pupillaire a la lumiere et l’obscurite sont mesurees pour divers requins et raies. La dilatation demande I-60 min et la constriction l-30 min, selon les esptces. Aucune reponse n’est consensuelle. Le muscle dilatateur est contrBlC par le troisieme neri c:anien, qui exerce probablement un tonus dilatatoire constant dans tous les cas. Au contraire le sphincter rtpond directement a la lumiere dans toutes les espZces etudiees. Cependant pour le sphincter de Scyliorhinus canicula, on trouve un reflexe retinoiridien.

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KARL P. KUCXNOW

Zusammwg-Umfang und AusmaD der Pupillenreaktion auf Licht und Dunkelheit werden fii verschiedene Haifische und Rochen bestimmt. Erweiterung beniitigt l-60 Min. und Verenrung l-30,Min. abhtingig von der Species. Alle Antworten waren nicht konsensueIl. Der M. dilatator wurde vom III. Himnerv kontrolliert. der immer einen konstanten Dilatator tonus aussendet. Der M. sphincter andererseits reagierte direkt auf Licht in allen untersuchten Gruppen. Wahrscheinlichkeit fiir einen nerviisen Retina-Iris Reflex jedoch wurde fiir den Sphincter Scyliorhinus canicula gefunden.

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