Vision Rex Vol. 30, No. 5, pp. 653457, 1990 F’rintcd in Great Britain. All rights reamed

00424989/‘90 53.00 + 0.00 Copyright Q 1990 Pcrgmon Pma pk

LOWER-FIELD MYOPIA IN BIRDS: AN ADAPTATION THAT KEEPS THE GROUND IN FOCUS W~LIAM HODOS’ and JONATHAN

T. Eatc?rss~~

‘Department of Psychology, University of Maryland, Colkp Park, MD 20742 and ‘Depertment of Neurobiology and Behavior, SUNY, Stony Brook, NY 11794, U.S.A. (Received 8 May 1989; in revisedform 20 October 1989) Abstract-In the lower visual field of pigeons, a myopia (near-sightedness) has been reported that progressively increases with the angle below the horizon. Previous data suggested that this lower-field myopia may be an adaptation that permits pigeons to keep the ground in focus while they forage, and simultaneously, to monitor the horizon and sky for predators. We report here a lower-field myopia in other species of birds that have a wide range of heights. A geometric model of this adaptation predicts that the amount of myopia should be systematically related to the distance from the pupil to the ground. ‘J’heeyes of quail, chickens and cranes of various heights (7.0-104.1 cm) were refracted at 60 deg below the horizon. Their myopia was close to the predicted value at each height. Refraction

Wysiological optics

Visual fields

Myopia

Birds

the world to each side, have been reported to be emrnetropic; i.e. without refractive error Although usually regarded as a defect of vision, (Glickstein & Millodot, 1970). For a pigeon myopia can have adaptive consequences. For with as much as MD of myopia around its example, an uncorrected myope is able to focus bill, objects beyond l/3-1/4m would be out on a closer object than an emmetrope and of focus on the retina. Since pigeons are known consequently can obtain a magnified retinal to be excellent fliers and navigators, this image (Curtin, 1985). The data reported here would seem to be equivalent to a myopic pilot concern another adaptive consequence of flying without corrective glasses. pigeons, myopia, in this case a peripheral myopia that however, do not fly with their bills horizontal, was recently described in pigeons. We now but rather keep them at an angle well below report this peripheral myopia in three other the horizon (Erichsen, Hodos, Evinger, Bessette species of ground-foraging birds. Rather than & Phillips, 1989). Several reports indicate that being an error of refraction in the usual sense, pigeons are emmetropic in the frontal field this peripheral myopia, which is limited to the when the bill is well below the horizon (Erichlower visual field, is a specialized visual adap sen, 1979; Fitzke, Hayes, Ho&s & Holden, tation that permits the birds to keep nearby 1985a). In this head position, the bird’s eye is objects on the ground in focus while at the same emmetropic for the horizon and the entire upper time monitoring the distant horizon and sky for visual 8eld. Below the horizon, however, a predators; all of this being accomplished gradient of myopia develops that reaches a without changing the accommodative state of maximum in the extreme lower field. This the eye. The results also have implications for gradient is not due to an optical aberration the mechanism by which the ground is kept in since the pigeon eye, unlike the human eye, focus on the upper retina as a young bird grows is free of peripheral astigmatism and spherical aberration (Erichsen, 1979; Fitxke et al., and thus increases in height. Several investigators have reported that 1985a). pigeons, which have laterally placed eyes, are Fit&e, Hayes, Hodos, Holden and Low myopic in their frontal visual fields, which in- (1985b) described a model that predicts the clude the region of the bill (Catania, 1964; degree of this lower&ld myopia from the angle Millodot & Blough, 1971; Nye, 1973; Erichsen, of elevation below the horizon for an animal of 1979).The lateral visual fields, which encompass a given height. Their model, which we shall refer INTRODUCTION

653

WILLIAMHobos and JONATHAN T. ERICHSEN

654 0

D f_--_-_______

Fig. 1. A d’qrammatic representation of the relationship between the variables in equation (1). The refractive state (R) in diopters (D) is a function of the height of the pupil center from the ground (H) and the sine of the angle of elevation below the horizon (A). The refractive state also can be obtained from the linear viewing distance (V) from the pupil to the ground at angle A below the horizon. Along the vertical meridian (A = 9Odeg), V = H.

to as the sine

model, may be expressed by the

equation: sin A R=H=‘;

1

(1)

in which R is the refractive state of the eye in diopters (D), A is the angle of elevation below the horizon, H is pupil height (the distance in metres from the center of the pupil to the groundwhenthebirdisstandingerect)and I/ is the viewing distance to the ground at angle A. In the ver&al plane (A -9Odeg), V-H. In simpk terms, the closer the ground is to the eye, the more myopic the eye must be in order to keep the ground in focus without aazommod&on. Thus, as shown in Fig. 1, a pigeon with a pupil height of 20 cm would have 5 D of myopia in the extreme lower visual field (90 deg); 4 D at 53 deg below the horizon; 3 D at 37 deg, which is in the vicinity of the bill (Erichsen et al., 1%9), 2 D at 24 dcg, etc. These preditions have been supported by the observations of Fitxke et al. (l%Sb) at different elevations in pigeons of roughly the same height. Moreover, Fit&e et al. were able to fit the refractions at diit elevations to the predicted sine curve in an individual pigeon. The sine model, however, further predicts that short birds should be more myopic in the lower field and tall birds should be correspondingly less myopic. Thus, a bird, such as a sparrow with a pupil height of 1Ocm should have a maximum of 10 D of lower-&&I myopia and an ostrich should be very nearly emmetropic. The study described here reports lower-

geld myopia in three other ground-foraging species of birds of various ages and over a wide range of heights. These results and previously published data for pigeons are consistent with the predictions of the sine model.

The subjects (unsexed) were five adult Japanese quail (COW jfysonicu), three adult broiler chickens (G&us g&w), three &weak old broiler chickens, three l-day ok-l broiler chicks and four adult &&hill Cranes (Gnus crmocconsis).The distance from the center of the pupil to the ground was measured w&h a cm scale as each bird stood fully erect. The mean (A standard error) pupil heights are presented in Table 1. The birds were deeply anesthetized with 65 mg/kg of Ketamine and 10 mg/kg Rompun, i.m., except for the adult clsidcens, which were given 20 mgjkg of Ketamine and 3.3 rug/kg of Rompun, and the cranes, which were anesthetized with isofturane inhalent. under deep anesthesia, mydriasis and miosis were indu*ed, the lower lid was grasped with a pair of fomeps and extended to form a cup into which a mixture of d-tubomuarine, benzalkonium adoride and atropine was introduced (CampeIl & Smith, 1962). The cup pe&tted a large v&me ofthecufaremixturetoramainincontactwith the cornea. The lid was hdd retrW& for about 1 min and then was returned slowly to its normal position. Maximal pupi&uy &I&ion usually occurred in about 15 min.

Lower-field myopia in birds

655

Table I. Mean (f SEM) pupil height, retinoscopy artifact, lower-field refraction and observed and @i&d refractions at elevation -60 deg

Bird

n

One-day chicks Adult quail Adult pigeons* Six-week chicks Adult chickens Adult cranes

3 5 3 3 4

Pupil height (cm) 7.5 (iO.3) 13.O(iO.3) 20.0 37.7 (*0.3) 54.0 (kO.6) 94.6(*3.3)

Artifact of retinoscopy (D)

Lower field refraction @)

+5.8 (kO.8) +3.0(*0.4)

-2.o(*o.l) -2.6 (i2.0)

+5.0(*2.0) +0.3 (f0.4) + 1.1 (*o.l)

+2.3 (kO.8) - 1.1 (iO.2) +l.o(*o.2)

Observed myopia 0) -7.8 (kO.8) -5.6(&2.0) -3.9 -2.6(&1.3) -1.4(*0.3) -0.1 (fO.l)

PredicM myopia @) -11.5 -6.7 -4.3 -2.3 -1.6 -0.9

*Previously oublished data from Erichsen (1979) and Fitzke et al. (1985b), but not included in the statisti&ianalyses reported here. .

After pupillary dilation was achieved, the bird was placed in a Kopf stereotaxic instrument located within an American Optical perimeter that permitted measurement of azimuth and elevation of the visual field. The midline of the bird defined 0 deg azimuth; the interpupillary line defined 90deg azimuth and Odeg elevation. The bill was positioned at an elevation of -40 deg (Erichsen et al., 1989). The perimeter was used to position the observer at azimuths of 30-75 deg (i.e. centered approximately on the optic axis; e.g. Burns & Wallman, 1981) and at an elevation of 60 deg below the horizon. An ophthalmoscopic examination was performed to ensure that the optic media were clear, after which a Copeland-Gptek 360 streak retinoscope and a trial-lens set were used to determine the refractive state of the eye. In order to avoid observer bias, the retinoscopy was performed by one of us while the other selected the trial lenses and placed them in front of the eye. The retinoscopist was unaware of the power of any of the lenses until after the retinoscopic examination had been completed; i.e. until after the neutral point had been determined. The refractions were made at distances of 35-75 cm. The retinoscopic results were corrected for distance in each case. The refractions of the right and left eyes were averaged. In order to compensate for the small-eye artifact in retinoscopy (Glickstein & Millodot, 1970), refractions also were made along the horizon (elevation f: 10 deg). The eyes of pigeons and chicks have been shown to be emmetropic along the horizon and the upper field when measured with the Fitzke optometer and pattern electroretinography, a method that does not have the small-eye artifact (Fitzke et al., 1985a, b; Fitzke, Sheen & Holden, 1985c; Hodos, Fitzke, Hayes & Holden, 1985). Therefore, the extent of hypermetropia (far-sightedtress) observed along the horizon was assumed to be approximately equal to the small eye

artifact. This apparent hypermetropia was subtracted from the refractive state observed in the lower field to yield a corrected refractive state. The amount of apparent hypermetropia that was subtracted is shown for each group of birds in Table 1. All procedures of this experiment were in accordance with the Guidefor the Care and Use of L&oratory Animals of the National Institutes of Health, NIH Publication Number 85-23, and were carried out with the approval of the University of Maryland, College Park Animal Care and Use Committee. RENLTS

AND DISCUSSION

Figure 2 shows the results of the experiment. Each solid symbol represents the mean corrected refractive state (the right and left eyes averaged) of a group of birds at elevation -60 deg (60 deg below the horizon). The vertical error bars indicate the standard error of the mean. The open symbols represent comparable published data from pigeons (Erichsen, 1979; Fitzke et al., 1985b), which are presented here for purposes of comparison but were not included in the statistical analyses. The curve represents the refractive state predicted by the sine model of Fitzke et al. (1985b) at an elevation of -60 deg for birds varying in height from 7 to 1lOcm (see equation 1 above). The data points are consistent with the general prediction that the shorter the bird, the more myopic will be the lower visual field. Moreover, the observations also support the more specific prediction that the relationship between lower-field myopia and height is directly related to the sine of the angle of elevation within the lower field (Fitzke et al., 1985b). In particular, the sine model predicts: (a) a linear relationship between the size of the refractive error and the reciprocal of the height of the eye; and (b) that the slope of this line will be equal

656

WILLIAM Hooos

and

JONATHANT. ERICHSEN

ELEVATION -60 deg

0

2-o - 40 - 60 .

lie -

l&t

PUP& HEIGHT(cm) Fig. 2. Mean refractive state of the lower visual tieid piottcd as a function of the vertical distance from the pupil center to the gound for IS birds that ran@ in h&&t from 7.0 to 104.1 cm. Solid symbotc mpresent the means of each group of birds (right and I& eyes averaged)_ Error bars indicate standard errors of the mean. Open symbols represent previously published data (Wchsen, 1979; Fitzke et al., 1985b). The smooth curve represents the lower-field myopia at elevation 60 &g below horizon as pMicted by a model based on pupil height and the sine of the angle of elevation (Fit&c et al.. 1985b). !3aeequation (I).

to the sine of the angle of elevation (i.e. sin -60deg or -0.87). A Model II regression analysis (Sokal & Rohlf, 1981) of the data in Fig. 2 revealed a linear relationship between R and l/H(r= -0.75, P < 0.001). The reduced major axis has a slope of -0.81, which is not signifkantly different (Ricker, 1973) from -0.87. The model further predicts that as the height of the pupil approaches infinity, the refractive errors should approach xero (emmetropia). The intercept (a’) of the reduced major axis (i.e. the value of R when l/H = 0) was not significantly different from zero. A linear regression between R and H also was significant (r = 0.72, P < 0.001). Therefore, a linear relationship between the refractive state and pupil height cannot be ruled out. Two points, however, argue against it. The first is that no known principles of optics would predict such a linear relationship. Second, a linear regression based on our present data predicts that birds above a height of 79cm should become increasingly hyperopic. Our data reveal no such trend toward hyperopia in the cranes, which were about 1 m in height. Table 1 presents the predicted refractive state at an elevation of -60 deg at each mean height for each group of birds as well as the corresponding mean observed refraction. A x2 test between the predicted and observed refractions was not significant. The optical mechanism that can account for the progressive lower-field myopia remains

obscure. One possibility could be that the curva-

ture of the upper retina is such that the entire plane of the ground as it extends towards the bird is simultaneously in focus on the photoreceptor layer. This phenomenon sometimes has been described in other animals as a “ramp” retina (Walls, 1942; Sivak & Allen, 1975;Sivak, 1976). A second, and not mutually exclusive, possibility would involve systematic variations in one or more of the refractive elements of the eye. Such variations could exist in the r&active index, the radius of curvature or some combination of the two. Progressive changes in the alignment of the refracting surfaces of the lerts and/or cornea also might be involved (Marshall, Mellerio & Palmer, 1973). At present, virtually no data exist that would help to evaluate these possibilities in birds. The systematic relationship between a birds height and the extent of myopia in its lower viaud field suggests that rather than being a refractive error, as myopia usually is regarded, this phenomenon is a powerful adaptation that maintains points along the ground at various distances in focus on the upper retina without requiring a change in the accommodative state of the eye. This would permit the bird to walk in a fully erect posture whik examining the ground for possible food obhts. At the same time, the relaxed aocommodafive state would leave the emmetropit upper visual &Id focused at infinity, thereby permitting the bird to monitor the horizon and sky for possible predators. Accommodation

Lower-field myopia in birds

would be used once an interesting object had been located on the ground; the bird then could bend towards the object, accommodate, and have an in-focus, enlarged retinal image. A gradient of myopia occurs in the lower visual field of a number of ground-foraging birds. The sine model not only predicts the amount of lower-field myopia in adult birds of four different species, it also predicts the refractive state in chickens of three very different ages and heights. Thus, as a bird grows and its height increases, the ground would remain conjugate with the upper retina. This process may be related to the mechanism that produces experimental myopia in chicks in which retinal images have been blurred or otherwise degraded (Wallman, Turkel & Trachtman, 1978; Yinon, 1984; Hodos & Kuenzel, 1984), i.e. persistently out-of-focus visual images regulate ocular growth that brings the images back into focus. Many ground-foraging animals have laterally placed eyes, presumably to provide a panoramic view of the world in response to predation pressures. If such an animal were to accommodate to look at objects on the ground, it temporarily would lose the advantage of its panoramic vision. Lower-field myopia permits the animal to maintain an in-focus panoramic view while foraging or otherwise inspecting the ground. A suggestion of the existence of this adaptation in ground-foraging mammals may be found in the work of De Graauw and van Hof (1980), which reported a frontal-field myopia in rabbits. Clearly, much work remains to be done to determine the optical mechanism that underlies this important visual adaptation. The term myopia implies refractive error, but the data reported here suggest that lower-field myopia, rather than being an error in the focal length of the eye, represents an adaptive matching of focal length to the eye-to-ground distance. Indeed, for ground-foraging birds, the myopia of the lower visual field would be a refractive error only during flight. AcknowIedgetnenrs-We thank F. J. Rohlf for statistical advice, F. A. Miles and C. Evinger for comments on the manuscript, E. Penland and A. Kimrey for technical aasistance and G. Olsen of the Patuxent Wildlife Research titer for providing the cranes and assistance with their mfractions. This study was supported by grants from the National Eye Institute to W. H. (EY-04742) and to J. T. E. (EY-04587). REFERENCES Burns, S. & Wallman, J. (1981). Relationship of single unit properties to the oculomotor function of the nucleus of

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Lower-field myopia in birds: an adaptation that keeps the ground in focus.

In the lower visual field of pigeons, a myopia (near-sightedness) has been reported that progressively increases with the angle below the horizon. Pre...
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