- Email: [email protected]
Binocular interaction in the peripheral visual field of humans with strabismic and anisometropic amblyopia
0042-6989/81/071065-lOSOZ.OO/o Pcrgnmon PressLtd
Vision Rrsrarrh Vol. 21. pp. 106510 1074. 1981 Printed in Great Britain
BINOCULAR INTERACTION IN THE PERIPHERAL VISUAL FIELD OF HUMANS WITH STRABISMIC AND ANISOMETROPIC ‘AMBLYOPIA RUXAND~U SW~UNU,
Max-Planck-Institute
MARIA FRONIUS and WOLF SINGER
for Psychiatry, Department of Neurophysiology,
Munich, F.R. Germany
(Received 12 October 1980)
Abstract-Residual binocular interaction was tested across the visual field of 9 strabismic and 2 anisometropic amblyopes in threshold and suprathreshold conditions. Binocular summation and interocular transfer of adaptation afterc&cts, both absent or very much reduced in the central region of the visual field of squint amblyopes, were highly significant in the periphery. The regions of preserved binocularity were well correlated with the areas for which there was no acuity loss and no interocular suppression. In anisometropic amblyopes, both binocular summation and interocular transfer of adaptation were lost at all tested eccentricities. Dynamic local stereopsis was also present in the periphery, but not in the central field of both squint and anisometropic amblyopes.
INTRODUCTION
Amblyopia is characterized by a developmental loss of acuity in one or both eyes. Several conditions can lead to this loss: an early uncorrected strabismus (squint amblyopia), severe uncorrected refractive error in one or both eyes (anisometropic amblyopia) or the prevention of vision in early childhood through unilateral or bilateral cataracts (stimulus deprivation amblyopia). Regardless of its origin, the acuity loss in amblyopia is accompanied by a lack or severe reduction of binocular functions and stereopsis (DukeElder, 1973). In strabismic, but not in anisometropic amblyopes, the loss of acuity is confined to the central part of the visual field. Peripheral acuity is equal, and sometimes higher than that of the fellow, non-amblyopic eye (Avetisov, 1979: Hess er al., 1980; Sireteanu and Fronius, 1981). In the accompanying paper, we tried to explain this selective loss of acuity in squint amblyopia: the misalignment of the visual axes causes a mismatch of the corresponding retinal points in the two eyes. Due to the progressive diminution of acuity towards the periphery, the lack of correspondence of the two retinae is restricted to the center of the visual field. In order to overcome diplopia, this region is selectively suppressed in one of the eyes, usually the non-dominant one. This long-term suppression of early onset is thought to result in abnormal maturation of the suppressed pathways, and this in turn is belived to be the common cause for the multiple abnormalities characteristic for amblyopia. In esotropes, these disturbances are confined to the central and nasal retina of the amblyopic eye (Sireteanu and Fronius, 1981). On the basis of this hypothesis, we expect binocular cooperation to be preserved in the periphery of the visual field of squint amblyopes. The aim of the
present work was to test this prediction. Binocular interaction has been evaluated at diRerent eccentricities in the visual field of squint and anisometropic amblyopes. Three different methods were used for the assessment of binocularity: (a) Binocular summation: binocular grating acuity is significantly higher than monocular acuity (Campbell and Green, 1965); (b) Interocular transjk of grating adaptation: the selective raise of the contrast threshold after prolonged inspection of a high-contrast grating is transferred to the fellow, non-adapted eye (Blakemore and Campbell, 1969). (c) Dynamic local stereopsis: continuous changing of the local disparity of two identical monocular images creates an illusion of motion-in-depth (Regan and Beverly, 1978). The first two methods are testing binocularity in threshold conditions. The third method is designed to test suprathreshold binocular interaction, a situation more similar to everyday experience. Normal observers were also included to provide a baseline for these measurements. METHODS Binocular
summation
Apparatus and procedure. Observers and apparatus as well as the procedure for the assessment of grating acuity were the same as in the previous experiment (Sireteanu and Fronius, 1981). For the assessment of binocular summation, thresholds were first determined for either eye alone and then compared to the binocular threshold. The sequence of measurements was such that all measurements (right eye, left eye, both eyes) were completed at one particular eccentri-
1065
1066
RUXANDRA SIRETEANU et al.
city before proceeding to the next. This procedure allowed a direct comparison of monocular and binocular grating acuities at particular eccentricities. The ratio of the binocular acuity over the best of the two monocular acuities was taken as a measure of binocular summation. Interocular
transfer
. Apparatus. Vertical sine-wave gratings of constant spatial frequency (f = 2.3 c/deg) were produced on the screen of a Hewlett-Packard oscilloscope (Model 1304 A Display). The contrast of the gratings could be varied with the aid of a linear attenuator, the maximum contrast reaching 0.6. The gratings were shown intermittently in a cycle of 2 set: I set grating I set blank screen. Each grating presentation was accompanied by an auditory signal. Using a black mask. the size of the stimulus was reduced to a dia of 6”. White fixation marks were placed along the horizontal meridian at distances of 20” and 25” from the center in both directions. The average luminance of the oscilloscope display was 4 cd m-‘. The luminance of the blank screen equalled the mean luminance of the gratings. A square-wave grating of the same spatial frequency and orientation and of the high contrast (close to 1) was fixed below the oscilloscope screen. This grating was used for adaptation; its dimensions were lo” x 25”. Fixation marks were again placed at 20” and 25’ from the center of the grating on either side. Procedure. The subjects were placed in front of the screen at a distance of I. I4 m. The contrast sensitivity threshold for the right eye was assessed with a descending method of limits. Subsequently,‘the right eye was adapted to the high-contrast grating for 3min. The subjects were asked to scan the adapting grating in order to avoid an after-image. After adaptation, the contrast sensitivity threshold for the right eye was measured again. Only measurements that could be obtained within 15 set were used. The observers then adapted again for 3Osec before a new threshold measurement was performed. The difference between the thresholds before and after adaptation are a measure of the monoptic adaptation after-effect. After a pause of about I5 min the left eye was adapted for 3 min and the elevation of the contrast sensitivity threshold of the right eye was assessed (dichoptic adaptation after-effect). The ratio of the dichoptic over the monoptic adaptation after-effect is a measure of the interocular transfer of adaptation. This procedure was performed for fovea1 vision as well as for each of the eccentric fixation marks; five to ten measurements were made for each condition. In one normal subject the interocular transfer of adaptation was measured for either eye. Motion-in-depth Apparatus. Two oscillating light squares were projected on a white screen. They were presented separately to the subject’s left and right eyes by means of
polarizing filters. When the stimuli for the two eyes were made to move in opposite directions with the same speed, the fused stimulus seemed to be moving in depth along a line passing between the eyes. The size of the squares was 2.5” x 2.5’ and their luminance 3cdm-‘. The luminance of the screen was I cdm-*. The movement of the two squares was produced by a ramp function generator, with a period of 2 sec. The angular separation varied from complete superposition to 2.5’ between the centers of the squares. Only crossed disparities were used in this experiment. These parameters were chosen since they produced a powerful impression of motion-in-depth over the whole visual field of normal observers. Fixation marks were placed on the screen along the horizontal as well as vertical and diagonal meridians; they were also used as fusion stimuli. Procedure. The observers were placed at a distance of 1.14m from the screen. For each of the fixation marks, they had to state whether or not they had the illusion of motion-in-depth. At the eccentricities where the effect existed they were asked to rate the apparent intensity of the illusion. In order to control for possible artefacts, the subjects were asked to compare the monocular and binocular appearance of the squares (by closing one eye or covering one of the light beams). In addition, they were asked to state the apparent direction of motion (towards or away from the subject) under the control of a normal observer. Each measurement was performed at least twice. For the control experiment on artificial anisometropia, “plus” lenses were fixed in front of the left eye of one normal, emetropic observer. In order to ensure the same relative defocusing of the test square at all eccentricities. the subject was allowed to shift his gaze, while the head was kept fixed. RESULTS
Binocular
summation
In humans with normal stereoscopic vision, the fovea1 binocular acuity is usually between 5 and 10% higher than monocular acuity (Campbell and Green, 1965). This effect is absent in stereoblind observers (Lema and Blake, 1977). We extended this result by testing binocular acuity at different eccentricities along the horizontal meridian of 3 normal observers (R.S., J.B. and U.M.). The results, averaged for the three observers, are shown in Fig. I. As in the preceding paper, the fovea1 acuity of the right eye has been taken as unity; the other acuity values are referred to this standard. It can be seen that there is a small, but consistent binocular summation at all eccentricities tested. For all three subjects, summation was slightly higher in the right visual hemifield. Binocular summation was subsequently tested along the horizontal meridian of 3 stereoblind, microstrabismic amblyopes (M.F., H.E. and R.N.). The results, averaged for the three subjects, are presented
Binocularity in the peripheral visual field
1067
LEFT
NORMALOBSERVERS
LO
F&&N I&iE
510
20
Lo
SWL FIELD (degrees)
Fig. I. Binocular summation along the horizontal meridian of 3 normal observers. Circles open at the right: right eyes; circles open at the left: left eyes. Open circles: both eyes. Each point is based on 3-6 acuity measurements for each subject.
in Fig. 2. Since two of the subjects were left amblyopes (M.F. and H.E.), while the third was a right amblyope (R.N.), the results were combined in a way that superimposes the “dominant” (right for the left amblyopes and left for the right amblyope) and “nondominant” hemifields, respectively. The dominant hemifield is represented in the nasal retina of the nonamblyopic eye and in the temporal retina of the amblyopic eye; the non-dominant hemifield corresponds to the nasal retina of the amblyopic eye and to the temporal retina of the non-amblyopic eye.
NDN-DCMNANT
As expected, binocular summation was reduced in the central visual field of these subjects, when compared to normal observers. The peripheral summation was highly asymmetric: at 5” and lo” in the nondominant hemifield, binocular acuity was close to, and on occasion even lower than the acuity of the non-amblyopic eye; this region corresponds to the areas in which the amblyopic eye is deeply suppressed (Sireteanu and Fronius, 1981). In the far non-dominant periphery (20”40’3 the binocular acuity approximated that of the amblyopic eye; in this region, the
DDMINANT
mnm#yopicqa anwwc cyc both cycs
, LO
30
...... l
20 lo505K) 20 30 co POSITDN IN THE VlSUAL FIELD (degrees)
Fig. 2. Binocular summation along the horizontal meridian of 3 microstrabismic amblyopes. Continuous line: non-amblyopic eye. Interrupted line: amblyopic eye. Star symbols: both eyes. n = 6-12. The standard errors of the monocular values are omitted for clarity.
1068
RUXANDRA SIRETUNU
et al.
NORMAL 06sERvER
@ 2
LEFT
20r
RlGnT
POSIliON
(R.9 P
Q
N
THE WSLIAL FIELD !dmgmm)
Fig. 3. Threshold binocularity at different locations along the horizontal meridian of one normal observer (R.S.). (A) Binocular summation. The ordinate represents the advantage of the binocular acuity over the highest of the two monocular acuities in percent. n = 5-9. (B) Interocular transfer of grating adaptation. White columns: right eye tested: dashed columns: left eye tested. 11= 5-10.
amblyopic eye is not, or only weakly suppressed. By contrast, there was a highly significant summation at lo”-30” in the dominant hemifield (P < 0.01, according to a one-tailed r-test). In this area interocular suppression was absent, and the acuity of the amblyopic eye was normal (see Figs 2 and 3 of the accompanying paper). For the arrisonwtropic anddyope I.S., there was no sign of binocular summation at any of the tested eccentricities (Fig. 5A). This finding again correlates well with the uniform and symmetric patterns of acuity loss and suppression described for anisometropes (Sireteanu and Fronius, 1981, Fig: 5). laterocular
trari$er
ojgratitlg
adaptation
Prolonged inspection of a high-contrast squarewave grating produces a transient rise in the contrast threshold for a sinusoidal grating of the same orienta-
tion and spatial frequency as the inducing grating. This effect, known as the grating adaptation aftereffect, transfers interocularly: if one eye is adapted, the contrast threshold of the other eye is also selectively elevated; the dichoptic (interocularly transferred) after-effect is about ScrSoo/, of the monopt& after-effect (Blakemore and Campbell, 1969). For stereoblind observers (and in particular amblyopes), the interocular transfer of adaptation is absent or very much reduced (Lema and Blake, 1977; Anderson et al., 1980). All these findings apply for fovea1 vision. There are no data in the literature on interocular transfer of grating adaptation in the peripheral visual field. Therefore, we tested the interocular transfer at five positions along the horizontal meridian of one rrormal observer (R.S.). The results are shown in Fig. 3. The transfer from the left eye to the right eye (white SQUINTAhBLYOPE
LEFT
RMT
~
IM.FJ
RE-
POSIION
IN THE WSUAL FIELD
0
lhgrm)
Fig. 4. Threshold binocularity at different locations along the horizontal meridian of one squint amblyope (M.F.). (A) Binocular summation. II = 9-32. (B) lnterocular transfer of grating adaptation. Right eye tested at all eccentricities. tt = S-10. Symbols as in Fig. 3.
1069
Binocularity in the peripheral visual field ANtSOWlRWlC
@ s
LEFT
2Or
:
AMBLYOPE (I.S.)
RK3iT
RE- 0
POSITION
IN THE VISUAL
FIELD
Idq’rsl
Fig. 5. Threshold binocularity at different locations along the horizontal meridian of one anisometropic amblyope (1,s.). (A) Binocular summation. n = 3. (B) Interocular transfer of grating adaptation. Right eye tested. n = 5-10. Symbols as in Fig. 3.
columns) was tested foveally and at 25” both nasally and temporally. The transfer from the right to the left eye (dashed columns) was tested at 0” and 20”, both nasally and temporally. It can be seen that the transfer is approximately uniform (50-700/, over the tested eccentricities), with a slight advantage in the right visual hemifield. There are no significant interocular differences. The same measurements were performed at different eccentricities in the visual field of one squint amblyope (M.F.). At all eccentricities, we determined the transfer from the left (amblyopic) to the right (non-amblyopic) eye. As expected, the fovea1 interocular transfer was significantly below normal (32%; Fig. 4B). The periphery was again asymmetric: in the right hemifield, the transfer exceeded the value determined for the normal observer (SO-900/,), while in the left hemifield, the transfer remained at the level found for the fovea (20-3~4). In order to be able to compare the residual binocularity as determined by the two independent techniques in this subject, part of the results of the summation experiment were replotted in Fig. 4A. In both cases, binocularity was absent or abnormally low in the central and left visual field. The best binocular function was found at 20” in the right hemifield; more peripherally, binocularity tended to decline. Both indices for binocularity at 20” were higher than the values found for normal observers. At this eccentricity, the acuity of the amblyopic eye .significantly (P < 0.0005) exceeded the acuity of the non-amblyepic eye. We do not have an explanation for these supranormal values. Figure SB illustrates the results of the interocular transfer experiment for one anisometropic amblyope (IS.). The fovea1 transfer was again very much reduced (38%). For this subject, the periphery was practically V.I.21 74
symmetric: transfer was almost absent at both 25” left (12%) and 25” right. (13%) in the visual field. This result correlates well with the absence of binocular summation at all tested eccentricities in the visual field of this subject (Fig. 5A). Dynamic local stereopsis
In the preceding two sections we have established that, in squint amblyopt;Li, there is a significant residuai binocularity in those parts of the visual field where there is no interocular suppression. The residual binocularity has been assessed in threshold conditions. Since all but one of our subjects were stereoblind, we wondered whether there is any evidence that the spared peripheral binocular connections are used in everyday life. The following experiment is designed to test suprathreshold binocular interaction. The perception of depth in normal vision is based on the slightly different images perceived by the two eyes (Wheatstone, 1838). If two identical images with a small horizontal disparity are presented separately to the two eyes, the fused image appears to be floating in depth. Dynamic changes in the disparity of the’two retinal images create a strong illusion of motion in depth (Regan and Beverly, 1978). This effect is particularly salient in the visual periphery. We tested the motion-in-depth illusion at 19 positions in the two-dimensional visual field of 6 normal observers (RX, U.M., J.B., I.W., H.B. and W.S.). T&.mt pattern was a bright square, presented separately to the two eyes with the aid of polarizing filters. In spite of some local variability, the effect was present over the whole visual field. For 4 out of 6 subjects, the percept was stronger in the right visual hemifield. There was no consistent up-down asymmetry. For a small region at and around the fovea, the motion-indepth illusion was accompanied by an apparent change in the size of the square, its apparent size
1070
RUXANDRA SIRETEANUer al.
INT AMBLYa LEFT
(Ml?)
RIGHT
30
20 UP 10
0
10 DOWN 20
30 4030
20
K)
0
la
POSITION IN THE VISUAL FIELD
20
33ul
Megfees)
Fig. 6. Dynamic stereopsis at different locations in the visual field of one Dashed area: region m winch no apparent motion-m-depth was perceived.
squmt amblyope (M.F.).
-.
Ihe
number
^...
01 “plus..
symbols indicates the strength of the apparent depth perception. decreasing during the illusion of approach. We interpret this phenomenon as a manifestation of the size constancy mechanism. The dependence of the motion-
in-depth illusion on the position in the visual field for subject H.B. is illustrated in the first panel in Fig. 9. With the exception of H.E., all the amblyopes listed in Table 1 of the accompanying paper (Sireteanu and Fronius, 1981) participated in this experiment. The motion-in-depth illusion was present in the visual periphery of all but one of the squinr amblpopes. The subjective strength of this illusion for observer M.F. is shown in Fig. 6. Along the horizontal meridian the occurrence of the illusion was closely related to the persistence of binocularity as assessed with the threshold techniques. The strongest depth perception was at 38’ in the right visual field; more peripherally, the effect gradually decreased. In the central and the left field, there was no perception of apparent depth
region of no apparent depth was more restricted around the fovea than for subject M.F. Subject H.F., whose preoperative angle of squint was large, did not show a depth effect along the horizontal meridian; in the upper and lower periphery, however, the depth percept was compelling. For the operated subject D.S. (also large preoperative squint), the residual stereosensitive region was even smaller: only the lower right periphery showed a weak, and URGE-ANGLE Sam1
UP
dwm
(shaded area in Fig. 6). but a very clear effect was perceived in the upper and lower hemifield. There was considerable variation among the other subjects, but there seemed to be a correlation between
the angle of squmt during development, and the area of preserved bmocularity (Fig. 7). Sometimes, the motion-m-depth of the test square was not perceived as coming directly to the subject, but with a clear lateral component. although speed and amplitude of the two opposing movements were kept strictly symmetrical. This phenomenon is probably related to the relative dominance of the two eyes in different parts of the visual field. For subject D.H.C.. the only one to showalthough markedly reduced-stereopsis with conven-
tional tests, the depth illusion was present at all tested position in the visual field. For subjects M.R. and R.N., both less severely amblyopic than M.F., the
KI!XKlN
IN THE VlSU4L FIELD 1-s
)
Fig. 7. Dynamic local stereopsis at different locations in the visual field of 6 strabismic amblyopes. Left column: microstrabismic untreated amblyopes; right column: operated amblyopes with large preoperative squint angles. Orthoptic characteristics of the subjects are shown in Table 1 of the accompanying paper (Sireteanu and Fronius, 1981). Arrows indicate the apparent direction of the motion-in-depth. Other symbols as in Fig. 6.
1071
Binocularity in the peripheral visual field
LEFT
RIGHT
UP
l
*
DOWN
-
XII
LO
30
20 KBTION
lo 0 IN THE VISUAL
lo FIELD
20 30 (degreeal
I
40
Fig. 8. Dynamic local stereopsis at different locations in the visual field of one anisometropic amblyope (IS.). Symbols as in Fig. 7.
rather distorted depth perception. The only squint amblyope for whom the motion-in-depth effect was absent at all positions in the visual field was C.K. His large preoperative squint and rather turbulent history of successive operations and large consecutive divergent squint might provide an explanation of this.fact. The apparent intensity of the motion-in-depth effect was then tested across the visual field of two anisomerropic anblyopes. The result for one of them (IS.) is shown in Fig. 8. A virtually symmetric stereodeficient area was found in the central visual field of this subject. Both the right and left periphery, and especially the upper and lower field did, however, show a fair sensitivity for motion-in-depth. Similar results were obtained for a second anisometrope (H.O.); the stereoblind central area of this more severely amblyo-
pit subject was more extended, invading a larger portion of the periphery (not illustrated). The fact that the visual periphery of anisometropic amblyopes is able to perceive depth is rather surprising in view of the fact that neither binocular summation nor interocular transfer of adaptation were found for these subjects. However, it can be seen in Fig. 5 that the eccentricities in which the threshold binocularity was tested fell within the central, stereoblind region. A very similar loss of stereoscopic perception can be produced in normal observers rendered artificially anisometropic. Figure 9 shows this effect for one normal subject whose left eye was rendered myopic with the aid of plus lenses. Indeed, a mild refractive imbalance (3 D) reduces the motion-in-depth illusion for
EFFECTCF ARTIFICIALANISOMETROPIA (H.B.1
RXllKIN
IN M
VISWL
FIELD
(dagmes )
Fig. 9. EtTect of artificial anisometropia on the motion-in-depth e&t
for a normal observer (H.B.).
1072
RUXANDRASIRETMNUet al.
all tested eccentricities, but the effect is deeper in the central visual field. For S-7 D the illusion is disrupted in the central visual field, but maintained in the periphery. With a more severe refraction imbalance (1O-20 D), this disruption invades progressively larger portions of the visual field. In conclusion, for both strabismic and anisometropit amblyopes, binocular interactions were preserved in the peripheral visual field; apart from occasional distortions in the perception of motion-in-depth, these interactions were qualitatively and quantitatively similar to those found in the visual field periphery of normal observers.
DISCUSSION
In this study binocular functions, as assessed with threshold measurements and dynamic local stereopsis, were tested across the visual field of strabismic and anisometropic amblyopes. It has been found that: (I) &nocularity was absent or very much reduced in the central visual field of both types of amblyopes. (2) For squint amblyopes, there was a clear involvement of the visual periphery in binocular function and stereopsis. These functions were usually asymmetric. (3) Anisometropic amblyopes also show a peripheral, essentially symmetric, ability to perceive binocular depth. Binocularity irt the uisual periphery of ,lorntal observers
The binocular properties of the visual periphery of normal observers, as assessed by three independent psychophysical methods (binocular summation, interocular transfer of adaptation and local dynamic steropsis), appear to be roughly the same as in the central visual field. A small, but consistent asymmetry was found: all binocular indices were slightly higher in the right visual hemifield. This asymmetry might be related to handedness. Relatiorl to clinical and psychophysical studies
It has been known for a long time that strabismus usually interferes with the normal development of binocularity and stereopsis. In some cases, however, and especially for microstrabismic amblyopes, a limited stereoscopic perception was found, when tested with clinical methods (Duke-Elder, 1973). Similar results were obtained in more recent psychophysical investigations. The interocular transfer of a movement after-effect was reduced in some but not all strabismic amblyopes (Wade, 1976). The interocular transfer of grating adaptation was lost in one of the two squint amblyopes tested by Hess (1978) and consistently reduced for all 6 amblyopes tested by Anderson et al. (1980). Using a reaction time paradigm to suprathreshold gratings, Levi et al. (1979) did not find binocular summation, but sometimes interocular inhibition in 4 strabismic and/or anisometropit amblyopes. The inhibitory interocular connections
found by Levi et al. (1979) in 3 strabismic and/or anisometropic amblyopes were specific for spatial frequency and orientation. In all these studies, the binocular function was tested foveally; to our knowledge, no systematic pyschophysical examination of binocularity in the periphery of squint amblyopes has been attempted so far. Using the visually evoked potential, Apkarian et al. (I 979) found evidence for maintained cortical binocularity in the visual periphery, but not at the fovea of strabismic amblyopes. Interpretation of the results and correlation with the acuity and suppression experiments
The main result of the present study is the sparing of binocular interactions in the peripheral visual field of squint and anisometropic amblyopes. In view of the fact that the different tests employed are likely to produce different degrees of dissociation of the two eyes, there is a remarkable agreement between the results of three independent methods employed to assess binocularity. The regions for which the threshold determinations (binocular summation and interocular transfer of grating adaptation) suggested the existence of binocular connections were indeed found to be involved in the binocular perception of depth. This finding confirms and extends the results presented in the preceding paper (Sireteanu and Fronius, 1981). In spite of some interindividual variability. the visual field of squint amblyopes seems to be subdivided in regions of different degrees of visual loss. In the central field, binocular cooperation is absent or weak; the amblyopic eye is deeply suppressed and the acuity of this eye is reduced. In the periphery, binocular interaction and stereopsis are fully preserved. There is no interocular suppression,,and the acuity of the amblyopic eye is normal. Thus. it appears that, in squint amblyopes. not only the reduction of acuity, but also the loss of binocularity in the central part of the visual field is a consequence of the interocular suppression that selectively affects the fovea1 and, in esotropes, part of the nasal retina of the amblyopic eye. The situation is more complicated in anisometropic amblyopes. In these subjects, interocular suppression involves the whole visual field of the amblyopic eye. Visual acuity is reduced at all tested eccentricities; however, the acuity loss is progressively less pronounced in the peripheral visual field. For both anisometropes tested, the visual periphery retained the ability to perceive motion-in-depth. It thus appears that, in some instance& interocular suppression and stereopsis may coexist. A similar conclusion was recently reached by Blake et al. (1981), who investigated suppression occurring with binocular rivalry in normal subjects. Our finding of the maintenance of binocularity in the peripheral visual field of artificial anisometropes suggests an explanation of this fact: due to the nor-
1073
Binocularity in the peripheral visual field
mally lower resolution of the periphery, defocusing is less critical in this region, and the patterns transmitted by the two eyes are less dissimilar than in the high-resolution, central visual field. Therefore, the fusion of contours is disrupted at the fovea, but still possible in the periphery. The good correlation between the regions of disturbed binocularity and acuity loss in both types of amblyopia provides support for the hypothesis that the early disruption of binocular cooperation, induced by strabismus or anisometropia, is the common cause of the different disturbances in amblyopia, including the incomplete Correlation
development
with animal
of acuity.
studies
The first neurophysiological demonstration of the loss of cortical binocular connections as a result of artificial squint is due to Hubel and Wiesel (1965). Much later, Ikeda and Wright (1976) produced amblyopia in cats raised with a convergent squint; in these cats, cortical binocularity was lost along with the spatial resolution of cells with fovea1 receptive fields (Ikeda and Tremain, 1977). In none of these studies, however, was there any indication that the loss of binocularity was confined to the central part of the visual field. In the experiments described above, the squint was induced surgically; this operation produced a transient immobilization of the squinting eye, most closely resembling a paralytic squint. More recently, Smith et al. (1979) investigated the binocularity of kittens raised with a squint induced optically with the aid of prisms. Thus, a concomitant strabismus was produced, more similar to the clinical situation of humans with a developmental squint. They discovered that the residual binocularity depends on the power of the prism worn during development: the larger the deviation, the deeper the loss of binocularly activated cortical cells. This conclusion resembles the result of our motion-in-depth experiment. However, the authors found no difference in the binocularity of cells with central or peripheral receptive fields. More extensive studies are needed to clarify this point. In the only study of kittens raised with artificial anisometropia (Eggers and Blakemore, 1978), the proportion of binocularly driven cortical cells was reduced, the reduction being directly related to the refractive imbalance between the two eyes. The cats also became amblyopic; the resolution of the cells driven by the defocused eye dropped clearly. These findings refer to the central part of the visual field; almost all cells included in this paper had receptive fields located within 3” from the area centralis. Relationship between treatment of amblyopia
residual
binocularity
and
the
The residual stereoscopic function of the visual periphery in squint and anisometropic amblyopes is a proof of the unusual robustness of the functional connections between the two eyes. Indeed, these connec-
tions survived the large preoperative squints of subjects H.F. and D.S. and a refractive imbalance of 20 D in subject H.B; only for subject C.K., for whom a large-angle convergent squint was followed by a large divergent squint, the peripharal binocularity was irremediably lost. This aspect raises the question whether the longterm occlusion of the non-amblyopic eye, or the alternate occlusion of the two eyes, currently used for the treatment of amblyopia, interfere with the residual stereopsis of the periphery. Such manipulations, when performed early in life, are known to alter the binocular properties of cortical cells in the cat (Wiesel and Hubel, 1963; Hubel and Wiesel, 1965). We do not have the answer to this question, since none of the subjects included in this study had undergone a complete occlusion therapy. Since the local stereopsis test is quick to perform and apparatively rather uncomplicated, it might be useful to include this test in routine clinical examinations. Acknowledgements-Most of the subjects who participated in these experiments were members of our families, colleagues and friends. We wish to thank them for their amiable collaboration. We are indebted to G. Neumann for help in some of the calculations and to Mrs S. Zieglginsberger and M. Kremling for preparing the illustrations and typing of the manuscript. Financial support for this work was provided partly by the Deutsche Forschungsgemeinschaft and partly by the Fraunhofer Gesellschaft. REFERENCES
Apkarian P.. Brown B. and Tyler C. W. (1978) Binocular interactions in strabismic amblyopia. Invest. Ophthal. oisuol Sci. 17, 216. Apharian P., Brown B. and Tyler C. W. (1978) Binocular interactions in strabismic amblyopia. Invest. Ophrhal. visual Sci. 17, 216. Avetisov E. S. (1979) Visual acuity and contrast sensitivity of the amblyopic eye as a function of the stimulated region of the retina (Translated by Kirschen D., Shlyakkov E. and Flom M.). Am. J. Oprom. Physiol. Opr. 56. 465469. Blake R., Westendorf D. H. and Overton R. (I 980) What is suppressed during binocular rivalry? Perception 9. 223-233.
Blakemore C. and Campbell F. W. (1969) On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol., Lond. 203. 237-260.
Campbell F. W. and Green D. G. (1965) Monocular versus binocular visual acuity. Nature 208, 191-192. Duke-Elder S. (1973) System of Opthalmology, Vol. VI, Ocular motility and strabismus. Kimpton. London. Eggers H. M. and Blakemore C. (1978) Physiological basis of anisometropic amblyopia. Sciench 2Oi, 264567. Hess R. (1978) Interocular transfer in individuals with strabismic amblyopia; a cautionary note. Perception 7, 201-205.
Hess R. F., Campbell F. W. and Zimmem R. C. (1980) Differences in the neural basis of human amblyopias: the effect of mean luminance. Vision Res. 20. 295-306. Hubel D. H. and Wiesel T. N. (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 23, 1041-1059.
RUXANDRA SIRETEANUet al.
1074
lkeda H. and Wright M. J. (1976) Properties of LGN cells in kittens reared with convergent squint: A neurophysiological demonstration of amblyopia. Expl. Brain Res. 25. 63-77. Ikeda H. and Tremain K. E. (1977) Different causes for amblyopia and loss of binocularity in squinting kittens. J. Physiol.,
Lond.
269, 26-27.
Lema S. A. and Blake R. (1977) Binocular summation in normal and stereoblind humans. Vision Rex 17, 691-695. Levi D. M.. Harwerth R. S. and Manny R. E. (1979) Suprathreshold spatial frequency detection and binocular interaction in strabismic and anisometropic amblyopia. Inoest. Opthal. uisuol Sci. 28, 714-730. Levi D. M.. Harwerth R. S. and Smith E. L. III (1979) Humans deprived of normal binocular vision have bin: ocular interactions tuned to size and orientation. Science 206,852-854. Regan D. and Beverley K. I. (1978) Illusory motion in
depth: after-effect of adaptation to changmg size. Vision Res. 18. 209-212 Sireteanu R. and Fronius M. (1981) Naso-temporal asymmetries in amblyopic vision: consequence of long-term interocular suppression. Vision Res. 21, 1055-1063. Smith E. L., Benneth M. J.. Harwerth R. S. and Crawford M. L. J. (1979) Binocularity in kittens reared with optically induced squint. Science 204, 875-877. Wade N. J. (1976) On interocular transfer of the movement after-effect in individuals with and without normal vision. Perception 5. I 13-l 18. Wheatstone C. (1838) Contributions to the physiology of vision: on some remarkable and hitherto unobserved phenomena of binocular vision. Phil. Trans. R. Sot.. Lond.. A. 128. 371-394. Wiesel T. N. and Hubel D. H. (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26. IOO3-IOI 7.
Vision Rrsrarrh Vol. 21. pp. 106510 1074. 1981 Printed in Great Britain
BINOCULAR INTERACTION IN THE PERIPHERAL VISUAL FIELD OF HUMANS WITH STRABISMIC AND ANISOMETROPIC ‘AMBLYOPIA RUXAND~U SW~UNU,
Max-Planck-Institute
MARIA FRONIUS and WOLF SINGER
for Psychiatry, Department of Neurophysiology,
Munich, F.R. Germany
(Received 12 October 1980)
Abstract-Residual binocular interaction was tested across the visual field of 9 strabismic and 2 anisometropic amblyopes in threshold and suprathreshold conditions. Binocular summation and interocular transfer of adaptation afterc&cts, both absent or very much reduced in the central region of the visual field of squint amblyopes, were highly significant in the periphery. The regions of preserved binocularity were well correlated with the areas for which there was no acuity loss and no interocular suppression. In anisometropic amblyopes, both binocular summation and interocular transfer of adaptation were lost at all tested eccentricities. Dynamic local stereopsis was also present in the periphery, but not in the central field of both squint and anisometropic amblyopes.
INTRODUCTION
Amblyopia is characterized by a developmental loss of acuity in one or both eyes. Several conditions can lead to this loss: an early uncorrected strabismus (squint amblyopia), severe uncorrected refractive error in one or both eyes (anisometropic amblyopia) or the prevention of vision in early childhood through unilateral or bilateral cataracts (stimulus deprivation amblyopia). Regardless of its origin, the acuity loss in amblyopia is accompanied by a lack or severe reduction of binocular functions and stereopsis (DukeElder, 1973). In strabismic, but not in anisometropic amblyopes, the loss of acuity is confined to the central part of the visual field. Peripheral acuity is equal, and sometimes higher than that of the fellow, non-amblyopic eye (Avetisov, 1979: Hess er al., 1980; Sireteanu and Fronius, 1981). In the accompanying paper, we tried to explain this selective loss of acuity in squint amblyopia: the misalignment of the visual axes causes a mismatch of the corresponding retinal points in the two eyes. Due to the progressive diminution of acuity towards the periphery, the lack of correspondence of the two retinae is restricted to the center of the visual field. In order to overcome diplopia, this region is selectively suppressed in one of the eyes, usually the non-dominant one. This long-term suppression of early onset is thought to result in abnormal maturation of the suppressed pathways, and this in turn is belived to be the common cause for the multiple abnormalities characteristic for amblyopia. In esotropes, these disturbances are confined to the central and nasal retina of the amblyopic eye (Sireteanu and Fronius, 1981). On the basis of this hypothesis, we expect binocular cooperation to be preserved in the periphery of the visual field of squint amblyopes. The aim of the
present work was to test this prediction. Binocular interaction has been evaluated at diRerent eccentricities in the visual field of squint and anisometropic amblyopes. Three different methods were used for the assessment of binocularity: (a) Binocular summation: binocular grating acuity is significantly higher than monocular acuity (Campbell and Green, 1965); (b) Interocular transjk of grating adaptation: the selective raise of the contrast threshold after prolonged inspection of a high-contrast grating is transferred to the fellow, non-adapted eye (Blakemore and Campbell, 1969). (c) Dynamic local stereopsis: continuous changing of the local disparity of two identical monocular images creates an illusion of motion-in-depth (Regan and Beverly, 1978). The first two methods are testing binocularity in threshold conditions. The third method is designed to test suprathreshold binocular interaction, a situation more similar to everyday experience. Normal observers were also included to provide a baseline for these measurements. METHODS Binocular
summation
Apparatus and procedure. Observers and apparatus as well as the procedure for the assessment of grating acuity were the same as in the previous experiment (Sireteanu and Fronius, 1981). For the assessment of binocular summation, thresholds were first determined for either eye alone and then compared to the binocular threshold. The sequence of measurements was such that all measurements (right eye, left eye, both eyes) were completed at one particular eccentri-
1065
1066
RUXANDRA SIRETEANU et al.
city before proceeding to the next. This procedure allowed a direct comparison of monocular and binocular grating acuities at particular eccentricities. The ratio of the binocular acuity over the best of the two monocular acuities was taken as a measure of binocular summation. Interocular
transfer
. Apparatus. Vertical sine-wave gratings of constant spatial frequency (f = 2.3 c/deg) were produced on the screen of a Hewlett-Packard oscilloscope (Model 1304 A Display). The contrast of the gratings could be varied with the aid of a linear attenuator, the maximum contrast reaching 0.6. The gratings were shown intermittently in a cycle of 2 set: I set grating I set blank screen. Each grating presentation was accompanied by an auditory signal. Using a black mask. the size of the stimulus was reduced to a dia of 6”. White fixation marks were placed along the horizontal meridian at distances of 20” and 25” from the center in both directions. The average luminance of the oscilloscope display was 4 cd m-‘. The luminance of the blank screen equalled the mean luminance of the gratings. A square-wave grating of the same spatial frequency and orientation and of the high contrast (close to 1) was fixed below the oscilloscope screen. This grating was used for adaptation; its dimensions were lo” x 25”. Fixation marks were again placed at 20” and 25’ from the center of the grating on either side. Procedure. The subjects were placed in front of the screen at a distance of I. I4 m. The contrast sensitivity threshold for the right eye was assessed with a descending method of limits. Subsequently,‘the right eye was adapted to the high-contrast grating for 3min. The subjects were asked to scan the adapting grating in order to avoid an after-image. After adaptation, the contrast sensitivity threshold for the right eye was measured again. Only measurements that could be obtained within 15 set were used. The observers then adapted again for 3Osec before a new threshold measurement was performed. The difference between the thresholds before and after adaptation are a measure of the monoptic adaptation after-effect. After a pause of about I5 min the left eye was adapted for 3 min and the elevation of the contrast sensitivity threshold of the right eye was assessed (dichoptic adaptation after-effect). The ratio of the dichoptic over the monoptic adaptation after-effect is a measure of the interocular transfer of adaptation. This procedure was performed for fovea1 vision as well as for each of the eccentric fixation marks; five to ten measurements were made for each condition. In one normal subject the interocular transfer of adaptation was measured for either eye. Motion-in-depth Apparatus. Two oscillating light squares were projected on a white screen. They were presented separately to the subject’s left and right eyes by means of
polarizing filters. When the stimuli for the two eyes were made to move in opposite directions with the same speed, the fused stimulus seemed to be moving in depth along a line passing between the eyes. The size of the squares was 2.5” x 2.5’ and their luminance 3cdm-‘. The luminance of the screen was I cdm-*. The movement of the two squares was produced by a ramp function generator, with a period of 2 sec. The angular separation varied from complete superposition to 2.5’ between the centers of the squares. Only crossed disparities were used in this experiment. These parameters were chosen since they produced a powerful impression of motion-in-depth over the whole visual field of normal observers. Fixation marks were placed on the screen along the horizontal as well as vertical and diagonal meridians; they were also used as fusion stimuli. Procedure. The observers were placed at a distance of 1.14m from the screen. For each of the fixation marks, they had to state whether or not they had the illusion of motion-in-depth. At the eccentricities where the effect existed they were asked to rate the apparent intensity of the illusion. In order to control for possible artefacts, the subjects were asked to compare the monocular and binocular appearance of the squares (by closing one eye or covering one of the light beams). In addition, they were asked to state the apparent direction of motion (towards or away from the subject) under the control of a normal observer. Each measurement was performed at least twice. For the control experiment on artificial anisometropia, “plus” lenses were fixed in front of the left eye of one normal, emetropic observer. In order to ensure the same relative defocusing of the test square at all eccentricities. the subject was allowed to shift his gaze, while the head was kept fixed. RESULTS
Binocular
summation
In humans with normal stereoscopic vision, the fovea1 binocular acuity is usually between 5 and 10% higher than monocular acuity (Campbell and Green, 1965). This effect is absent in stereoblind observers (Lema and Blake, 1977). We extended this result by testing binocular acuity at different eccentricities along the horizontal meridian of 3 normal observers (R.S., J.B. and U.M.). The results, averaged for the three observers, are shown in Fig. I. As in the preceding paper, the fovea1 acuity of the right eye has been taken as unity; the other acuity values are referred to this standard. It can be seen that there is a small, but consistent binocular summation at all eccentricities tested. For all three subjects, summation was slightly higher in the right visual hemifield. Binocular summation was subsequently tested along the horizontal meridian of 3 stereoblind, microstrabismic amblyopes (M.F., H.E. and R.N.). The results, averaged for the three subjects, are presented
Binocularity in the peripheral visual field
1067
LEFT
NORMALOBSERVERS
LO
F&&N I&iE
510
20
Lo
SWL FIELD (degrees)
Fig. I. Binocular summation along the horizontal meridian of 3 normal observers. Circles open at the right: right eyes; circles open at the left: left eyes. Open circles: both eyes. Each point is based on 3-6 acuity measurements for each subject.
in Fig. 2. Since two of the subjects were left amblyopes (M.F. and H.E.), while the third was a right amblyope (R.N.), the results were combined in a way that superimposes the “dominant” (right for the left amblyopes and left for the right amblyope) and “nondominant” hemifields, respectively. The dominant hemifield is represented in the nasal retina of the nonamblyopic eye and in the temporal retina of the amblyopic eye; the non-dominant hemifield corresponds to the nasal retina of the amblyopic eye and to the temporal retina of the non-amblyopic eye.
NDN-DCMNANT
As expected, binocular summation was reduced in the central visual field of these subjects, when compared to normal observers. The peripheral summation was highly asymmetric: at 5” and lo” in the nondominant hemifield, binocular acuity was close to, and on occasion even lower than the acuity of the non-amblyopic eye; this region corresponds to the areas in which the amblyopic eye is deeply suppressed (Sireteanu and Fronius, 1981). In the far non-dominant periphery (20”40’3 the binocular acuity approximated that of the amblyopic eye; in this region, the
DDMINANT
mnm#yopicqa anwwc cyc both cycs
, LO
30
...... l
20 lo505K) 20 30 co POSITDN IN THE VlSUAL FIELD (degrees)
Fig. 2. Binocular summation along the horizontal meridian of 3 microstrabismic amblyopes. Continuous line: non-amblyopic eye. Interrupted line: amblyopic eye. Star symbols: both eyes. n = 6-12. The standard errors of the monocular values are omitted for clarity.
1068
RUXANDRA SIRETUNU
et al.
NORMAL 06sERvER
@ 2
LEFT
20r
RlGnT
POSIliON
(R.9 P
Q
N
THE WSLIAL FIELD !dmgmm)
Fig. 3. Threshold binocularity at different locations along the horizontal meridian of one normal observer (R.S.). (A) Binocular summation. The ordinate represents the advantage of the binocular acuity over the highest of the two monocular acuities in percent. n = 5-9. (B) Interocular transfer of grating adaptation. White columns: right eye tested: dashed columns: left eye tested. 11= 5-10.
amblyopic eye is not, or only weakly suppressed. By contrast, there was a highly significant summation at lo”-30” in the dominant hemifield (P < 0.01, according to a one-tailed r-test). In this area interocular suppression was absent, and the acuity of the amblyopic eye was normal (see Figs 2 and 3 of the accompanying paper). For the arrisonwtropic anddyope I.S., there was no sign of binocular summation at any of the tested eccentricities (Fig. 5A). This finding again correlates well with the uniform and symmetric patterns of acuity loss and suppression described for anisometropes (Sireteanu and Fronius, 1981, Fig: 5). laterocular
trari$er
ojgratitlg
adaptation
Prolonged inspection of a high-contrast squarewave grating produces a transient rise in the contrast threshold for a sinusoidal grating of the same orienta-
tion and spatial frequency as the inducing grating. This effect, known as the grating adaptation aftereffect, transfers interocularly: if one eye is adapted, the contrast threshold of the other eye is also selectively elevated; the dichoptic (interocularly transferred) after-effect is about ScrSoo/, of the monopt& after-effect (Blakemore and Campbell, 1969). For stereoblind observers (and in particular amblyopes), the interocular transfer of adaptation is absent or very much reduced (Lema and Blake, 1977; Anderson et al., 1980). All these findings apply for fovea1 vision. There are no data in the literature on interocular transfer of grating adaptation in the peripheral visual field. Therefore, we tested the interocular transfer at five positions along the horizontal meridian of one rrormal observer (R.S.). The results are shown in Fig. 3. The transfer from the left eye to the right eye (white SQUINTAhBLYOPE
LEFT
RMT
~
IM.FJ
RE-
POSIION
IN THE WSUAL FIELD
0
lhgrm)
Fig. 4. Threshold binocularity at different locations along the horizontal meridian of one squint amblyope (M.F.). (A) Binocular summation. II = 9-32. (B) lnterocular transfer of grating adaptation. Right eye tested at all eccentricities. tt = S-10. Symbols as in Fig. 3.
1069
Binocularity in the peripheral visual field ANtSOWlRWlC
@ s
LEFT
2Or
:
AMBLYOPE (I.S.)
RK3iT
RE- 0
POSITION
IN THE VISUAL
FIELD
Idq’rsl
Fig. 5. Threshold binocularity at different locations along the horizontal meridian of one anisometropic amblyope (1,s.). (A) Binocular summation. n = 3. (B) Interocular transfer of grating adaptation. Right eye tested. n = 5-10. Symbols as in Fig. 3.
columns) was tested foveally and at 25” both nasally and temporally. The transfer from the right to the left eye (dashed columns) was tested at 0” and 20”, both nasally and temporally. It can be seen that the transfer is approximately uniform (50-700/, over the tested eccentricities), with a slight advantage in the right visual hemifield. There are no significant interocular differences. The same measurements were performed at different eccentricities in the visual field of one squint amblyope (M.F.). At all eccentricities, we determined the transfer from the left (amblyopic) to the right (non-amblyopic) eye. As expected, the fovea1 interocular transfer was significantly below normal (32%; Fig. 4B). The periphery was again asymmetric: in the right hemifield, the transfer exceeded the value determined for the normal observer (SO-900/,), while in the left hemifield, the transfer remained at the level found for the fovea (20-3~4). In order to be able to compare the residual binocularity as determined by the two independent techniques in this subject, part of the results of the summation experiment were replotted in Fig. 4A. In both cases, binocularity was absent or abnormally low in the central and left visual field. The best binocular function was found at 20” in the right hemifield; more peripherally, binocularity tended to decline. Both indices for binocularity at 20” were higher than the values found for normal observers. At this eccentricity, the acuity of the amblyopic eye .significantly (P < 0.0005) exceeded the acuity of the non-amblyepic eye. We do not have an explanation for these supranormal values. Figure SB illustrates the results of the interocular transfer experiment for one anisometropic amblyope (IS.). The fovea1 transfer was again very much reduced (38%). For this subject, the periphery was practically V.I.21 74
symmetric: transfer was almost absent at both 25” left (12%) and 25” right. (13%) in the visual field. This result correlates well with the absence of binocular summation at all tested eccentricities in the visual field of this subject (Fig. 5A). Dynamic local stereopsis
In the preceding two sections we have established that, in squint amblyopt;Li, there is a significant residuai binocularity in those parts of the visual field where there is no interocular suppression. The residual binocularity has been assessed in threshold conditions. Since all but one of our subjects were stereoblind, we wondered whether there is any evidence that the spared peripheral binocular connections are used in everyday life. The following experiment is designed to test suprathreshold binocular interaction. The perception of depth in normal vision is based on the slightly different images perceived by the two eyes (Wheatstone, 1838). If two identical images with a small horizontal disparity are presented separately to the two eyes, the fused image appears to be floating in depth. Dynamic changes in the disparity of the’two retinal images create a strong illusion of motion in depth (Regan and Beverly, 1978). This effect is particularly salient in the visual periphery. We tested the motion-in-depth illusion at 19 positions in the two-dimensional visual field of 6 normal observers (RX, U.M., J.B., I.W., H.B. and W.S.). T&.mt pattern was a bright square, presented separately to the two eyes with the aid of polarizing filters. In spite of some local variability, the effect was present over the whole visual field. For 4 out of 6 subjects, the percept was stronger in the right visual hemifield. There was no consistent up-down asymmetry. For a small region at and around the fovea, the motion-indepth illusion was accompanied by an apparent change in the size of the square, its apparent size
1070
RUXANDRA SIRETEANUer al.
INT AMBLYa LEFT
(Ml?)
RIGHT
30
20 UP 10
0
10 DOWN 20
30 4030
20
K)
0
la
POSITION IN THE VISUAL FIELD
20
33ul
Megfees)
Fig. 6. Dynamic stereopsis at different locations in the visual field of one Dashed area: region m winch no apparent motion-m-depth was perceived.
squmt amblyope (M.F.).
-.
Ihe
number
^...
01 “plus..
symbols indicates the strength of the apparent depth perception. decreasing during the illusion of approach. We interpret this phenomenon as a manifestation of the size constancy mechanism. The dependence of the motion-
in-depth illusion on the position in the visual field for subject H.B. is illustrated in the first panel in Fig. 9. With the exception of H.E., all the amblyopes listed in Table 1 of the accompanying paper (Sireteanu and Fronius, 1981) participated in this experiment. The motion-in-depth illusion was present in the visual periphery of all but one of the squinr amblpopes. The subjective strength of this illusion for observer M.F. is shown in Fig. 6. Along the horizontal meridian the occurrence of the illusion was closely related to the persistence of binocularity as assessed with the threshold techniques. The strongest depth perception was at 38’ in the right visual field; more peripherally, the effect gradually decreased. In the central and the left field, there was no perception of apparent depth
region of no apparent depth was more restricted around the fovea than for subject M.F. Subject H.F., whose preoperative angle of squint was large, did not show a depth effect along the horizontal meridian; in the upper and lower periphery, however, the depth percept was compelling. For the operated subject D.S. (also large preoperative squint), the residual stereosensitive region was even smaller: only the lower right periphery showed a weak, and URGE-ANGLE Sam1
UP
dwm
(shaded area in Fig. 6). but a very clear effect was perceived in the upper and lower hemifield. There was considerable variation among the other subjects, but there seemed to be a correlation between
the angle of squmt during development, and the area of preserved bmocularity (Fig. 7). Sometimes, the motion-m-depth of the test square was not perceived as coming directly to the subject, but with a clear lateral component. although speed and amplitude of the two opposing movements were kept strictly symmetrical. This phenomenon is probably related to the relative dominance of the two eyes in different parts of the visual field. For subject D.H.C.. the only one to showalthough markedly reduced-stereopsis with conven-
tional tests, the depth illusion was present at all tested position in the visual field. For subjects M.R. and R.N., both less severely amblyopic than M.F., the
KI!XKlN
IN THE VlSU4L FIELD 1-s
)
Fig. 7. Dynamic local stereopsis at different locations in the visual field of 6 strabismic amblyopes. Left column: microstrabismic untreated amblyopes; right column: operated amblyopes with large preoperative squint angles. Orthoptic characteristics of the subjects are shown in Table 1 of the accompanying paper (Sireteanu and Fronius, 1981). Arrows indicate the apparent direction of the motion-in-depth. Other symbols as in Fig. 6.
1071
Binocularity in the peripheral visual field
LEFT
RIGHT
UP
l
*
DOWN
-
XII
LO
30
20 KBTION
lo 0 IN THE VISUAL
lo FIELD
20 30 (degreeal
I
40
Fig. 8. Dynamic local stereopsis at different locations in the visual field of one anisometropic amblyope (IS.). Symbols as in Fig. 7.
rather distorted depth perception. The only squint amblyope for whom the motion-in-depth effect was absent at all positions in the visual field was C.K. His large preoperative squint and rather turbulent history of successive operations and large consecutive divergent squint might provide an explanation of this.fact. The apparent intensity of the motion-in-depth effect was then tested across the visual field of two anisomerropic anblyopes. The result for one of them (IS.) is shown in Fig. 8. A virtually symmetric stereodeficient area was found in the central visual field of this subject. Both the right and left periphery, and especially the upper and lower field did, however, show a fair sensitivity for motion-in-depth. Similar results were obtained for a second anisometrope (H.O.); the stereoblind central area of this more severely amblyo-
pit subject was more extended, invading a larger portion of the periphery (not illustrated). The fact that the visual periphery of anisometropic amblyopes is able to perceive depth is rather surprising in view of the fact that neither binocular summation nor interocular transfer of adaptation were found for these subjects. However, it can be seen in Fig. 5 that the eccentricities in which the threshold binocularity was tested fell within the central, stereoblind region. A very similar loss of stereoscopic perception can be produced in normal observers rendered artificially anisometropic. Figure 9 shows this effect for one normal subject whose left eye was rendered myopic with the aid of plus lenses. Indeed, a mild refractive imbalance (3 D) reduces the motion-in-depth illusion for
EFFECTCF ARTIFICIALANISOMETROPIA (H.B.1
RXllKIN
IN M
VISWL
FIELD
(dagmes )
Fig. 9. EtTect of artificial anisometropia on the motion-in-depth e&t
for a normal observer (H.B.).
1072
RUXANDRASIRETMNUet al.
all tested eccentricities, but the effect is deeper in the central visual field. For S-7 D the illusion is disrupted in the central visual field, but maintained in the periphery. With a more severe refraction imbalance (1O-20 D), this disruption invades progressively larger portions of the visual field. In conclusion, for both strabismic and anisometropit amblyopes, binocular interactions were preserved in the peripheral visual field; apart from occasional distortions in the perception of motion-in-depth, these interactions were qualitatively and quantitatively similar to those found in the visual field periphery of normal observers.
DISCUSSION
In this study binocular functions, as assessed with threshold measurements and dynamic local stereopsis, were tested across the visual field of strabismic and anisometropic amblyopes. It has been found that: (I) &nocularity was absent or very much reduced in the central visual field of both types of amblyopes. (2) For squint amblyopes, there was a clear involvement of the visual periphery in binocular function and stereopsis. These functions were usually asymmetric. (3) Anisometropic amblyopes also show a peripheral, essentially symmetric, ability to perceive binocular depth. Binocularity irt the uisual periphery of ,lorntal observers
The binocular properties of the visual periphery of normal observers, as assessed by three independent psychophysical methods (binocular summation, interocular transfer of adaptation and local dynamic steropsis), appear to be roughly the same as in the central visual field. A small, but consistent asymmetry was found: all binocular indices were slightly higher in the right visual hemifield. This asymmetry might be related to handedness. Relatiorl to clinical and psychophysical studies
It has been known for a long time that strabismus usually interferes with the normal development of binocularity and stereopsis. In some cases, however, and especially for microstrabismic amblyopes, a limited stereoscopic perception was found, when tested with clinical methods (Duke-Elder, 1973). Similar results were obtained in more recent psychophysical investigations. The interocular transfer of a movement after-effect was reduced in some but not all strabismic amblyopes (Wade, 1976). The interocular transfer of grating adaptation was lost in one of the two squint amblyopes tested by Hess (1978) and consistently reduced for all 6 amblyopes tested by Anderson et al. (1980). Using a reaction time paradigm to suprathreshold gratings, Levi et al. (1979) did not find binocular summation, but sometimes interocular inhibition in 4 strabismic and/or anisometropit amblyopes. The inhibitory interocular connections
found by Levi et al. (1979) in 3 strabismic and/or anisometropic amblyopes were specific for spatial frequency and orientation. In all these studies, the binocular function was tested foveally; to our knowledge, no systematic pyschophysical examination of binocularity in the periphery of squint amblyopes has been attempted so far. Using the visually evoked potential, Apkarian et al. (I 979) found evidence for maintained cortical binocularity in the visual periphery, but not at the fovea of strabismic amblyopes. Interpretation of the results and correlation with the acuity and suppression experiments
The main result of the present study is the sparing of binocular interactions in the peripheral visual field of squint and anisometropic amblyopes. In view of the fact that the different tests employed are likely to produce different degrees of dissociation of the two eyes, there is a remarkable agreement between the results of three independent methods employed to assess binocularity. The regions for which the threshold determinations (binocular summation and interocular transfer of grating adaptation) suggested the existence of binocular connections were indeed found to be involved in the binocular perception of depth. This finding confirms and extends the results presented in the preceding paper (Sireteanu and Fronius, 1981). In spite of some interindividual variability. the visual field of squint amblyopes seems to be subdivided in regions of different degrees of visual loss. In the central field, binocular cooperation is absent or weak; the amblyopic eye is deeply suppressed and the acuity of this eye is reduced. In the periphery, binocular interaction and stereopsis are fully preserved. There is no interocular suppression,,and the acuity of the amblyopic eye is normal. Thus. it appears that, in squint amblyopes. not only the reduction of acuity, but also the loss of binocularity in the central part of the visual field is a consequence of the interocular suppression that selectively affects the fovea1 and, in esotropes, part of the nasal retina of the amblyopic eye. The situation is more complicated in anisometropic amblyopes. In these subjects, interocular suppression involves the whole visual field of the amblyopic eye. Visual acuity is reduced at all tested eccentricities; however, the acuity loss is progressively less pronounced in the peripheral visual field. For both anisometropes tested, the visual periphery retained the ability to perceive motion-in-depth. It thus appears that, in some instance& interocular suppression and stereopsis may coexist. A similar conclusion was recently reached by Blake et al. (1981), who investigated suppression occurring with binocular rivalry in normal subjects. Our finding of the maintenance of binocularity in the peripheral visual field of artificial anisometropes suggests an explanation of this fact: due to the nor-
1073
Binocularity in the peripheral visual field
mally lower resolution of the periphery, defocusing is less critical in this region, and the patterns transmitted by the two eyes are less dissimilar than in the high-resolution, central visual field. Therefore, the fusion of contours is disrupted at the fovea, but still possible in the periphery. The good correlation between the regions of disturbed binocularity and acuity loss in both types of amblyopia provides support for the hypothesis that the early disruption of binocular cooperation, induced by strabismus or anisometropia, is the common cause of the different disturbances in amblyopia, including the incomplete Correlation
development
with animal
of acuity.
studies
The first neurophysiological demonstration of the loss of cortical binocular connections as a result of artificial squint is due to Hubel and Wiesel (1965). Much later, Ikeda and Wright (1976) produced amblyopia in cats raised with a convergent squint; in these cats, cortical binocularity was lost along with the spatial resolution of cells with fovea1 receptive fields (Ikeda and Tremain, 1977). In none of these studies, however, was there any indication that the loss of binocularity was confined to the central part of the visual field. In the experiments described above, the squint was induced surgically; this operation produced a transient immobilization of the squinting eye, most closely resembling a paralytic squint. More recently, Smith et al. (1979) investigated the binocularity of kittens raised with a squint induced optically with the aid of prisms. Thus, a concomitant strabismus was produced, more similar to the clinical situation of humans with a developmental squint. They discovered that the residual binocularity depends on the power of the prism worn during development: the larger the deviation, the deeper the loss of binocularly activated cortical cells. This conclusion resembles the result of our motion-in-depth experiment. However, the authors found no difference in the binocularity of cells with central or peripheral receptive fields. More extensive studies are needed to clarify this point. In the only study of kittens raised with artificial anisometropia (Eggers and Blakemore, 1978), the proportion of binocularly driven cortical cells was reduced, the reduction being directly related to the refractive imbalance between the two eyes. The cats also became amblyopic; the resolution of the cells driven by the defocused eye dropped clearly. These findings refer to the central part of the visual field; almost all cells included in this paper had receptive fields located within 3” from the area centralis. Relationship between treatment of amblyopia
residual
binocularity
and
the
The residual stereoscopic function of the visual periphery in squint and anisometropic amblyopes is a proof of the unusual robustness of the functional connections between the two eyes. Indeed, these connec-
tions survived the large preoperative squints of subjects H.F. and D.S. and a refractive imbalance of 20 D in subject H.B; only for subject C.K., for whom a large-angle convergent squint was followed by a large divergent squint, the peripharal binocularity was irremediably lost. This aspect raises the question whether the longterm occlusion of the non-amblyopic eye, or the alternate occlusion of the two eyes, currently used for the treatment of amblyopia, interfere with the residual stereopsis of the periphery. Such manipulations, when performed early in life, are known to alter the binocular properties of cortical cells in the cat (Wiesel and Hubel, 1963; Hubel and Wiesel, 1965). We do not have the answer to this question, since none of the subjects included in this study had undergone a complete occlusion therapy. Since the local stereopsis test is quick to perform and apparatively rather uncomplicated, it might be useful to include this test in routine clinical examinations. Acknowledgements-Most of the subjects who participated in these experiments were members of our families, colleagues and friends. We wish to thank them for their amiable collaboration. We are indebted to G. Neumann for help in some of the calculations and to Mrs S. Zieglginsberger and M. Kremling for preparing the illustrations and typing of the manuscript. Financial support for this work was provided partly by the Deutsche Forschungsgemeinschaft and partly by the Fraunhofer Gesellschaft. REFERENCES
Apkarian P.. Brown B. and Tyler C. W. (1978) Binocular interactions in strabismic amblyopia. Invest. Ophthal. oisuol Sci. 17, 216. Apharian P., Brown B. and Tyler C. W. (1978) Binocular interactions in strabismic amblyopia. Invest. Ophrhal. visual Sci. 17, 216. Avetisov E. S. (1979) Visual acuity and contrast sensitivity of the amblyopic eye as a function of the stimulated region of the retina (Translated by Kirschen D., Shlyakkov E. and Flom M.). Am. J. Oprom. Physiol. Opr. 56. 465469. Blake R., Westendorf D. H. and Overton R. (I 980) What is suppressed during binocular rivalry? Perception 9. 223-233.
Blakemore C. and Campbell F. W. (1969) On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol., Lond. 203. 237-260.
Campbell F. W. and Green D. G. (1965) Monocular versus binocular visual acuity. Nature 208, 191-192. Duke-Elder S. (1973) System of Opthalmology, Vol. VI, Ocular motility and strabismus. Kimpton. London. Eggers H. M. and Blakemore C. (1978) Physiological basis of anisometropic amblyopia. Sciench 2Oi, 264567. Hess R. (1978) Interocular transfer in individuals with strabismic amblyopia; a cautionary note. Perception 7, 201-205.
Hess R. F., Campbell F. W. and Zimmem R. C. (1980) Differences in the neural basis of human amblyopias: the effect of mean luminance. Vision Res. 20. 295-306. Hubel D. H. and Wiesel T. N. (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 23, 1041-1059.
RUXANDRA SIRETEANUet al.
1074
lkeda H. and Wright M. J. (1976) Properties of LGN cells in kittens reared with convergent squint: A neurophysiological demonstration of amblyopia. Expl. Brain Res. 25. 63-77. Ikeda H. and Tremain K. E. (1977) Different causes for amblyopia and loss of binocularity in squinting kittens. J. Physiol.,
Lond.
269, 26-27.
Lema S. A. and Blake R. (1977) Binocular summation in normal and stereoblind humans. Vision Rex 17, 691-695. Levi D. M.. Harwerth R. S. and Manny R. E. (1979) Suprathreshold spatial frequency detection and binocular interaction in strabismic and anisometropic amblyopia. Inoest. Opthal. uisuol Sci. 28, 714-730. Levi D. M.. Harwerth R. S. and Smith E. L. III (1979) Humans deprived of normal binocular vision have bin: ocular interactions tuned to size and orientation. Science 206,852-854. Regan D. and Beverley K. I. (1978) Illusory motion in
depth: after-effect of adaptation to changmg size. Vision Res. 18. 209-212 Sireteanu R. and Fronius M. (1981) Naso-temporal asymmetries in amblyopic vision: consequence of long-term interocular suppression. Vision Res. 21, 1055-1063. Smith E. L., Benneth M. J.. Harwerth R. S. and Crawford M. L. J. (1979) Binocularity in kittens reared with optically induced squint. Science 204, 875-877. Wade N. J. (1976) On interocular transfer of the movement after-effect in individuals with and without normal vision. Perception 5. I 13-l 18. Wheatstone C. (1838) Contributions to the physiology of vision: on some remarkable and hitherto unobserved phenomena of binocular vision. Phil. Trans. R. Sot.. Lond.. A. 128. 371-394. Wiesel T. N. and Hubel D. H. (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26. IOO3-IOI 7.