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Eye torsion and visual tilt are mediated by different binocular processes
EYE TORSION AND VISUAL TILT MEDIATED BY DIFFERENT BINOCULAR
ARE PROCESSES
JEREMYM. WOLFE and RICHARD HELD Department of Psychology. ElO-138C. Massachusetts Institute of Technology. Cambridge. MA 02139, U.S.A. (Received 24 October 1978) Abstract-Viewing a large. patterned field rotating about the line of sight produces two measurable effects: cyclotorsion of the eyes (torsion) and a perceived displacement of vertical and horizontal (tilt). Experiments examining binocular interaction for these effects show: (1) both effects demonstrate summation in normal individuals and thus both involve a binocular process: (2) the process for tilt is different than that for torsion. since summation lor torsion is spared in stereodeficient individuals while that for tilt is eliminated
INTRODUCI’ION
METHOD
Looking at the center of a large display rotating in a frontal plane around the line of sight produces a number of perceptual, oculomotor, and postural phenomena. Most readily apparent to the observer is the postural effect, i.e. a clockwise rotation of the field will usually produce a sensation of counterclockwise self-motion (vection). Other changes are less obvious but are of an easily measurable magnitude. For example, the orientation of the apparent horizontal (or vertical) will tilt in opposition to the direction of field rotation (tilt). Furthermore, the observer’s eyes will show several degrees of cyclotorsion in the same direction as that of the rotating field (torsion). Previous papers have described many of the characteristics of these latter two effects (Dichgans er al, 1972; Held ef al., 1975; Finke and Held, 1978). Results of these experiments have suggested that torsion and tilt might be mediated by different visual processes. For example, we have noted informally that the magnitudes of torsion and tilt do not seem well correlated over time. The experiments reported here seek to better specify the nature of the processes underlying these effects. Two questions have been addressed: First, do either tilt or torsion use binocular channels? Second, if binocularity can be shown how does this pattern of results change if stereodeficient subjects are used? It has been theorized that stereodeficiencies represent a loss of binocular channels at a cortical level (Movshon et al., 1972).
The method used here takes advantage of our observation that the magnitude of tilt and torsion induced by a rotating display viewed under stroboscopic illumination (flash duration < 25 gsec) varies with the repetition rate of that illumination. If the strobe rate is very slow ( c 8 Hz) little or no motion will be seen in the rotating display and no torsion or tilt will be produced. If the rate is fast enough to approach critical flicker frequency ( : JO Hz). the effects will be similar to those obtained under conditions of continuous illumination. In the range of frequencies between 8 and 20Hz. the magnitude of torsion and tilt increases monotonically as a function of strobe frequencv. At higher frequencies the magnitude reaches an asymptotic level equal to that for steady illumination. If each eye is presented with a IOHz rate of flicker in such a way that flashes to one eye bisect the interval between successive flashes to the other eye (i.e. they are out of phase by 1809, a “cyclopean” (Julesz. 1971) 20 HZ signal will be produced (see the right side of Fig. 1). Viewing the rotating display at 10 Hz produces small torsion and tilt magnitudes. while viewing the display at 20 Hz produces a much stronger effect. IT either torsion or tilt is mediated via a binocular site, then the out of phase dichoptic 10 Hz signal, producing a cyclopean 20 Hz should result in either more tilt or more torsion than a monocular 10 Hz. If the effects are generated before the inputs from the two eyes converge. then the cyclopean 20Hz should show no advantage over the monocular 10 Hz. A cyclopean signal is produced by having the input to one eye out of synchrony with the input to the other eye (henceforth: the “out of phase” condition). If this condition produces a larger effect than monocular presentation, it
“IN PULSES TO THE LEFT EVE
PWSE'
CONDITION
"OUT OF PHASE' CONOlTION
10 Hz
10 Hz
IIIIIIIIII
*,1,1,1111
PULSES TO THE RIGHT EVE
I 10 HZ
PULSES AVAILABLE TO THE 'CYCLOPEAN" EVE
, 10 HZ
I
I
,p 20 HZ
Fig. I. Diagram of a method by which two strobes. each set for IO Rashes per sec. can be made to produce either in the visual system. The only difference between the in relation between the flashes to the V.R.19 8-f
I
10 n;
917
providing light to only one eye and each 10 or 20 Hz signals in binocular processes and out of phase conditions is the phase left and right eyes.
JFREVY M. WOLFE anlf RICH.ARD HELD
Ql?:
m($ht be proposed that mere btnocuiar presentation. but not the cyclopean doubling of the frequency was responsible. Thus. a better control would be to hate the inputs !o the two eyes still separate but not dichopric (henceforth: the “in phase” condition). Using the previous example, that would be a IOHz signal to each eye but with every flash lo one eye occurring simultaneously with a Hash to the other. In both of these conditions, each eye alone receives the same signal. The information differentiating the two conditions is available oniy when excitation from the two eyes converges on one binocular channel. Hence. the existence of a binocular process prior to the production of tilt or torsion would be demonstrated if the out of phase condition produced a larger effect than the in phase condition for a range of monocular frequencies (see Fig. 1). (Note: In pilot studies we have found that in phase stimuli produce the same effects as monocular stimuli.)
.Anaglyphic presentation was produced by using two strobe units (Grass Model PS-2. General Radio. Strobotac type 1531-A); one with a red filter and the other with a green filter. The subject wore goggles with a red filter over the left eye and a green filter over the right eye. Filters For strobes and goggles were chosen so that the “red” eye saw no light reflected from the rotating disk save that emitted by the .red” strobe. Likewise, the “green” eye saw only light from the “green” strobe. The four filters were composites of Edmund colored filters. Their peak responses were as follows: 13) The red goggle filter transmitted a maximum of 580, at 630nm. ib) The green goggle filter transmitted a maximum of 36” at 575 nm. (PI The red strobe tiller transmitted a maximum of 58’; at 635 nm. (d) The green strobe filter transmitted a maximum of 77’,, at 495 nm. The iollowing 2 x 3 table lists the peak transmittance of available white light by ail four combinations of a strobe filter and a goggle filter: Strobe Red
Green
Red
43” 0 at 645 nm
< I:,, at all wavelengths
Green
< I”, at all wavelengths
31”~ at 52Onm
Goggles __
A selenium photoceil, calibrated to a Macbeth illuminometer and with spectral sensitivities similar to that of the human visual system. was used to equate the red and green channels for luminance. Strobe frequencies were set by the Grass strobe. The strobotac was yoked to the Grass strobe via a device designed to vary the delay between the gashes from the two units. Five monocular frequencies were used: 5. 10. 12. 15, and 2OHz. Both in phase and out of phase conditions were run at each frequency. Subjects viewed a randomly patterned display subtending IOO of visual angle in stroboscopic light while wearing goggles as described above. Stable head position was maintained by the use of a bite board. Subjects fixated the stationary point at the center of the field. Detailed description of the rotating display apparatus has been published elsewhere (Held er cii.. 1975). For the present experimentation. rotation was always counterclockwise at a velocity of 27’!sec. With the goggles on. the subject’s field of view was 100”. ail of which was tilled by the disk at the viewing distance of 25cm. The goggles provided 60” of binocular overlap.
the apparent hortzontai posttron with the rield stlrlonsr). The S.5. by i.3 cursor bar was mounted un a dtsk located tn the center ol the rotating tieid. The target disk moved independently ol the larger rotating display. -\fter the initial stationary horizontai setting. the display was set in counterclockwise rotation at a velocity ol’ 27-, set The subject viewed the moving display under stroboscoptc iiiummation for at least 20sec before making any response ,After that delay. with the field still rotating. fire settings were made for the apparent horizontal, displacing the cursor away from the horizontal between each setting. The experimenter, who was recording each setting, requested extra settings if the first one was substantially htgher or lower than the subsequent readings or if the values continuously decreased or increased. This was done in order to obtain five readings at an asymptotic level of the effect in a given condition. Most of the extra readings %erz required to compensate for an extremely tow tirst reading. In these cases the first reading was ignored rn later analyses. After takmg the readings. the field was stopped and the subject waited at least 20sec for motion aftereffects to decay and then made a second reading with the field stationary. The magnitude of tilt was computed us the average of the readings during motion minus the averaee of the two stationary readings and was expressed in degrees. Resolution of measurement was 0.1’. Torsion measurements were taken in a similar fashron. To track the turning of the eyes. a photoflash unit was used to create an afterimage of a horizontal line on both retinae while the disk was at rest. When the display was set in rotation. cyclotorsion of the eyes produced a shift in the apparent locus of the afterimage relative to the cursor bar. The subject aligned the cursur with the afterimage. thus giving a reading for torsion. Again. a reading was taken before the display began to rotate. Five readings were taken wrth the field in rotation. Finally. a second reading was taken with the field again at rest and magnitude of torsion computed in the same way as that for tilt. A single session consisted of torsion and trlt measurements for the in and out of phase conditions for live strobe hequencies (8. IO. 12, 15, and 20 Hz,. To mimmize within and across session variability. in phase and out of phase conditions for a single frequency were run successively. The order of frequencies was random within a session and the order of in and out of phase conditions was random within a frequency. A session took approximately 45 min.
Three males. familiar with the apparatus and the cxperiment and between the ages of 23 and 30, ran three sessions of torsion and tilt each. One female. age 20. naive as to the nature of the experiment and unfamilar with the apparatus. ran one session of tilt and torsion. Ail these subjects had normal acuity (Sneilen 20’20 or better). stereovision. and no sign of any abnormality of vision at the 25 cm viewing distance. Three males and three females. judged to be stereodeficient by their faiiure on the Army vtsron test for stereoacuity (Bausch and Lomb Armed Forces Vision Tester Type 71-21-10) ran one session each of tilt and torsion. In these subjects. the stereodeficiencies could be traced to childhood visual anomalies such as strabismus. “lazy eye”. and so forth. Most of them had reduced acuity in the nondominant eye. A&ties were never worse than 204O with correction. Thus, their acuity was sufficient t@ resolve motion of the display. RESULTS
Normnl subjecrs
Ths magnitude having
the subject
of the perceived tiit was measured by first manually rotate a cursor bar to
Figures 2a and 2b present the mean three normal subjects for tilt and torsion
data for the respectively.
Eye torsion and visual tilt are mediated by different binocular processes
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Fig. 2. In each of figures Za-d, magnitude of tilt or torsion is plotted as a function of monocular strobe frequency. In the out of phase condition the binocular frequency would be twice the monocular frequency. Binocular summation is indicated when the magnitude of an effect at a specific frequency is greater for the out of phase condition than for the in phase condition. Summation is clearly evident in Za, b, and d. Only in Zc, Tilt-Stereoblind subjects, is there no evidence for summation.
As was noted in the Methods section, the magnitude of both torsion and tilt increases as the strobe frequency is increased from 8 to 20 Hz. Within a given session, the subject’s five readings at a specific frequency generally had a range of kO.5”. There were session-to-session differences, moderate differences within a single subject’s three sessions, larger differences among subjects. However, the relation of the in and out of phase results remained constant across sessions and subjects and justifies the presentation of average data. Figures 2a and 2b show that for normal subjects the magnitude of tilt and torsion is greater in the out of phase condition than in the in phase condition. Taking each of the ten sessions as an independent trial, the binomial test shows the differences to be significant at the 0.01 level for all frequencies in the tilt data and for all but the 8 Hz condition in the torsion data. The 8 Hz torsion effect is significant at the 0.05 level. The finding that the out of phase condition produced a larger effect than the in phase condition at each strobe frequency is consistent with the hypothesis that the production of tilt and torsion in normal subjects involes binocular processes. Stereodeficienr subjects Figures 2c and 2d present the averaged data for the stereodeficient subjects. In graph Zc, it is obvious that there is no significant difference. between the in phase and the out of phase conditions. This pattern of results was found in ail six of the stereodeficient subjects. Figure Zd, however, shows a very different pattern of results for torsion. The average data show
that the out of phase condition consistently produced more torsion at a given strobe frequency than did the in phase condition. This indicates that stereodeficient subjects still show binocular summation for torsion. This pattern of results was produced by all six of the stereodeficient subjects. In fact, the results produced by these subjects are indistinguishable from those produced by the stereonormal subjects. Apparently the stereodeficiency shared by these six subjects did not disrupt the binocular process mediating torsion. DISCUSSION
Three conclusions may be drawn from these results: First, in normal subjects, the production of both tilt and torsion is mediated in part by binocular processes. Since this experimental design did not eliminate all monocular cues, it is not yet known if these effects are mediated in cooperation with a monocular process. Second, the binocular process for torsion is different than that for tilt. This result was shown by comparing the results for stereodeficient subjects to those for normal subjects. Third, the stereodeficient individuals seem to lack the process required for binocular summation in tilt, but possess the process required for summation of torsion. It appears, then. that the binocular process involved in torsion is resistant to some forms of early binocular deprivation. It could be argued that the pattern of results found in these subjects arose not from the loss of a binocular process for tilt but, rather, from the effects of some other visual pathology. Several such hypotheses may
3_‘0
JEREZII
11. M.OLFE.
be considered and discarded. One possibility is that the stereodeficient subjects could not fuse the rotating disk. If the disk was seen as double. the observer would not see simple rotary motion but some complicated form of apparent motion that might be insuhicient to produce binocular summation for tilt. None of the subjects, however. reported diplopia except at the slowest flicker rates. At these frequencies stereonormal subjects also noted some transient diplopia. Furthermore. this hypothesis and any other proposai not based on the notion of separate processes for torsion and tilt must account for the preservation of binocular interactions in torsion. Diplopia should have a similar elect on both tilt and torsion. Several of the stereodeticient subjects were amblyopic. It might be proposed that the lack of binocular summation in these subjects was due to the suppression of the amblyopic eye. An effectively monocular subject could not be expected to show bmocuiar summation. As vvith the diplopia hypothesis, this explanation would have difficulty accounting for the continued presence of binocular summation for torsion. Moreover. at Least two of the stereodefrcient subjects had equivalent acuities in their two eyes. In general, if pathology is to be used as an explanation of the data. that pathology must have two characteristics: (I) it must be present in all of the stereodeficient subjects; and. (2) it must be sufficient to explain the loss of summation for tilt while accounting for the sparing of torsion. The only shared pathology meeting these requirements is the reduction in stereoacuity shown by all six stereodeficient subjects. It. therefore, seems reasonable to conclude that the condition responsible for this lack of stereo ability is also responsible for the loss of summation for tilt and that this condition does not produce a foss of binocular summation for torsion. The description of the paradigm used in this experiment stated that a 10 Hz out of phase condition would produce a 20 Hz cyclopean signal. It is obvious from the data presented that. while IO Hz out of phase does produce more of an effect than 10H.z in phase. it does not produce as much of an effect as 20 Hz monocular or in phase signal (Fig. 2). This indicates that the binocular interaction is not simply a linear summation. Over the range of frequencies from 8 to ‘0 Hz. an out of phase signal of “N” Hz is not equivalent to “ZN” Hz monocular or in phase. It is equal to a 1.X-1.4 N Hz signal. Several workers have proposed “vector-sum” for binocular interactions (e.g. for brightness: Curtis and Rule, 1978). If the binocular interaction in the out of phase condition is seen as the summation of two orthogonal vectors of equal length, then their sum is not 2 K but t ‘2 N = 1.4 N. This is very close to the observed summation and provides a potential clue for future work. It is of some interest to speculate about the nature of the neuronal mechanisms that might underly the results described above. The binocular process must be one that is capable of performing a correlation between the two eyes when the two inputs are slightly displaced in space and time but are otherwise identical. l_!l]man (1977) has discussed the constraints on such a process in theoretical terms. Two such mechanisms would appear to be present here, one
Ind
RICHARD HELI)
ijr torsion and one for tilt. The bmocular tilt mechanisms must be sensitive to the abnormalitres introduced by defects like stabismus because such abnormalities seem to cripple this binocular process. On the other hand. the torsion mechanism is less sensitive to such changes. as its binocularity is not Impaired by those defects. In this light, it is interesting to consider the results of artificially induced strabismus in animals. Hubel and Wiesel ( 1965) have shown that normally binocular cells in areas 17 and IS of the cat become prsdominantly monocular in cats reared with only alternating monocular exposure to light. Interestingly. Gordon and Presson (1977) found that similar rearing does not reduce the proportion of binocular units in the superior colticuii. Their cats did show the prepoderance of monocular units in the correx but the coilicuii appeared to be normal. Bmocular units hate also been found in various nuclei of the accessory optic tract (Hoffman and Schoppman. 1975) but the response of such units to artificial strabismus IS not knou-n. ,At least one physiological investigation. that of Gordon and Presson (1977). shows that artiticial strabismus can eliminate one binocular process while sparing another, a pattern of results similar in kind to that found in the experiments reported here. IVe may speculate that the separation of the two processes corresponds to the existence of two scparst? sites in the visual nervous system. .Icknot\lrciymlmrs-The authors would like to thank D. ,a. Owens. J. A. Bauer. J. Thomas. f. H. Sandelf. and J. Gwiazda for consultation on this project. This research was supported in part by grants from X.4S.A (No. NGL-22-009-308) and NIH {No. I-Roi-EY011649,).J. Wolfe had support from NIH-l-T31-GXfOi-tS4.
REFERENCES
Curtis D. W. and Rule S. J. (1978) Binocular processing of brightness information: A vector-sum model. J.E.P.: H.P.P. 1. 133-143. Dichgans J., Held R.. Young L. R. and Brandt T. (IV?) Moving visual scenes influence the apparent dirtcrivn of gra;tty. Science; S.Y. i38, IZt7-1319. Finke R. and Held R. (1975) State reversals of oprictillq induced tilt and torsional eye movements. Percrpr. Pi!,chophys.
23(-t). 337-340.
Gordon B. and Presson J. (1977) EfTectj of alternattnd occlusion on receptive fields in cat superior colliculus. J. i~guru~h~sio~. 40, 14061414. Held R., Dicheans J. and Bauer J. (1974) Characteristics of moving hsual scenes influence spatiai orientation. k’ision Rex 15, 357-365. Hoffman K.-P. and Schoopman A. (1974) Retinal Input .. to direction selective cells in the nucleus tractus opticus of the cat. Brain Res. 99. 359-366. H ubel D. H. and Wiesel T. N. (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J. Xew~ph~~id. 28, 1011-1059. Julesz B. (1971) Foundarions o/ C~clopeuh Percrprion. The University of Chicago Press. Chicago. Xiovshon J. A_ Chambers B. E. I. and Blakemore C. I 19721 Interocular transfer in normal humans. and those *ho lack stereopsis. Prrception 1, 483-490. Ulfman S. (1977) The interpretation of visual motion. DOCtoral dissertation. M.I.T.. Cambridge. 31.4.
ARE PROCESSES
JEREMYM. WOLFE and RICHARD HELD Department of Psychology. ElO-138C. Massachusetts Institute of Technology. Cambridge. MA 02139, U.S.A. (Received 24 October 1978) Abstract-Viewing a large. patterned field rotating about the line of sight produces two measurable effects: cyclotorsion of the eyes (torsion) and a perceived displacement of vertical and horizontal (tilt). Experiments examining binocular interaction for these effects show: (1) both effects demonstrate summation in normal individuals and thus both involve a binocular process: (2) the process for tilt is different than that for torsion. since summation lor torsion is spared in stereodeficient individuals while that for tilt is eliminated
INTRODUCI’ION
METHOD
Looking at the center of a large display rotating in a frontal plane around the line of sight produces a number of perceptual, oculomotor, and postural phenomena. Most readily apparent to the observer is the postural effect, i.e. a clockwise rotation of the field will usually produce a sensation of counterclockwise self-motion (vection). Other changes are less obvious but are of an easily measurable magnitude. For example, the orientation of the apparent horizontal (or vertical) will tilt in opposition to the direction of field rotation (tilt). Furthermore, the observer’s eyes will show several degrees of cyclotorsion in the same direction as that of the rotating field (torsion). Previous papers have described many of the characteristics of these latter two effects (Dichgans er al, 1972; Held ef al., 1975; Finke and Held, 1978). Results of these experiments have suggested that torsion and tilt might be mediated by different visual processes. For example, we have noted informally that the magnitudes of torsion and tilt do not seem well correlated over time. The experiments reported here seek to better specify the nature of the processes underlying these effects. Two questions have been addressed: First, do either tilt or torsion use binocular channels? Second, if binocularity can be shown how does this pattern of results change if stereodeficient subjects are used? It has been theorized that stereodeficiencies represent a loss of binocular channels at a cortical level (Movshon et al., 1972).
The method used here takes advantage of our observation that the magnitude of tilt and torsion induced by a rotating display viewed under stroboscopic illumination (flash duration < 25 gsec) varies with the repetition rate of that illumination. If the strobe rate is very slow ( c 8 Hz) little or no motion will be seen in the rotating display and no torsion or tilt will be produced. If the rate is fast enough to approach critical flicker frequency ( : JO Hz). the effects will be similar to those obtained under conditions of continuous illumination. In the range of frequencies between 8 and 20Hz. the magnitude of torsion and tilt increases monotonically as a function of strobe frequencv. At higher frequencies the magnitude reaches an asymptotic level equal to that for steady illumination. If each eye is presented with a IOHz rate of flicker in such a way that flashes to one eye bisect the interval between successive flashes to the other eye (i.e. they are out of phase by 1809, a “cyclopean” (Julesz. 1971) 20 HZ signal will be produced (see the right side of Fig. 1). Viewing the rotating display at 10 Hz produces small torsion and tilt magnitudes. while viewing the display at 20 Hz produces a much stronger effect. IT either torsion or tilt is mediated via a binocular site, then the out of phase dichoptic 10 Hz signal, producing a cyclopean 20 Hz should result in either more tilt or more torsion than a monocular 10 Hz. If the effects are generated before the inputs from the two eyes converge. then the cyclopean 20Hz should show no advantage over the monocular 10 Hz. A cyclopean signal is produced by having the input to one eye out of synchrony with the input to the other eye (henceforth: the “out of phase” condition). If this condition produces a larger effect than monocular presentation, it
“IN PULSES TO THE LEFT EVE
PWSE'
CONDITION
"OUT OF PHASE' CONOlTION
10 Hz
10 Hz
IIIIIIIIII
*,1,1,1111
PULSES TO THE RIGHT EVE
I 10 HZ
PULSES AVAILABLE TO THE 'CYCLOPEAN" EVE
, 10 HZ
I
I
,p 20 HZ
Fig. I. Diagram of a method by which two strobes. each set for IO Rashes per sec. can be made to produce either in the visual system. The only difference between the in relation between the flashes to the V.R.19 8-f
I
10 n;
917
providing light to only one eye and each 10 or 20 Hz signals in binocular processes and out of phase conditions is the phase left and right eyes.
JFREVY M. WOLFE anlf RICH.ARD HELD
Ql?:
m($ht be proposed that mere btnocuiar presentation. but not the cyclopean doubling of the frequency was responsible. Thus. a better control would be to hate the inputs !o the two eyes still separate but not dichopric (henceforth: the “in phase” condition). Using the previous example, that would be a IOHz signal to each eye but with every flash lo one eye occurring simultaneously with a Hash to the other. In both of these conditions, each eye alone receives the same signal. The information differentiating the two conditions is available oniy when excitation from the two eyes converges on one binocular channel. Hence. the existence of a binocular process prior to the production of tilt or torsion would be demonstrated if the out of phase condition produced a larger effect than the in phase condition for a range of monocular frequencies (see Fig. 1). (Note: In pilot studies we have found that in phase stimuli produce the same effects as monocular stimuli.)
.Anaglyphic presentation was produced by using two strobe units (Grass Model PS-2. General Radio. Strobotac type 1531-A); one with a red filter and the other with a green filter. The subject wore goggles with a red filter over the left eye and a green filter over the right eye. Filters For strobes and goggles were chosen so that the “red” eye saw no light reflected from the rotating disk save that emitted by the .red” strobe. Likewise, the “green” eye saw only light from the “green” strobe. The four filters were composites of Edmund colored filters. Their peak responses were as follows: 13) The red goggle filter transmitted a maximum of 580, at 630nm. ib) The green goggle filter transmitted a maximum of 36” at 575 nm. (PI The red strobe tiller transmitted a maximum of 58’; at 635 nm. (d) The green strobe filter transmitted a maximum of 77’,, at 495 nm. The iollowing 2 x 3 table lists the peak transmittance of available white light by ail four combinations of a strobe filter and a goggle filter: Strobe Red
Green
Red
43” 0 at 645 nm
< I:,, at all wavelengths
Green
< I”, at all wavelengths
31”~ at 52Onm
Goggles __
A selenium photoceil, calibrated to a Macbeth illuminometer and with spectral sensitivities similar to that of the human visual system. was used to equate the red and green channels for luminance. Strobe frequencies were set by the Grass strobe. The strobotac was yoked to the Grass strobe via a device designed to vary the delay between the gashes from the two units. Five monocular frequencies were used: 5. 10. 12. 15, and 2OHz. Both in phase and out of phase conditions were run at each frequency. Subjects viewed a randomly patterned display subtending IOO of visual angle in stroboscopic light while wearing goggles as described above. Stable head position was maintained by the use of a bite board. Subjects fixated the stationary point at the center of the field. Detailed description of the rotating display apparatus has been published elsewhere (Held er cii.. 1975). For the present experimentation. rotation was always counterclockwise at a velocity of 27’!sec. With the goggles on. the subject’s field of view was 100”. ail of which was tilled by the disk at the viewing distance of 25cm. The goggles provided 60” of binocular overlap.
the apparent hortzontai posttron with the rield stlrlonsr). The S.5. by i.3 cursor bar was mounted un a dtsk located tn the center ol the rotating tieid. The target disk moved independently ol the larger rotating display. -\fter the initial stationary horizontai setting. the display was set in counterclockwise rotation at a velocity ol’ 27-, set The subject viewed the moving display under stroboscoptc iiiummation for at least 20sec before making any response ,After that delay. with the field still rotating. fire settings were made for the apparent horizontal, displacing the cursor away from the horizontal between each setting. The experimenter, who was recording each setting, requested extra settings if the first one was substantially htgher or lower than the subsequent readings or if the values continuously decreased or increased. This was done in order to obtain five readings at an asymptotic level of the effect in a given condition. Most of the extra readings %erz required to compensate for an extremely tow tirst reading. In these cases the first reading was ignored rn later analyses. After takmg the readings. the field was stopped and the subject waited at least 20sec for motion aftereffects to decay and then made a second reading with the field stationary. The magnitude of tilt was computed us the average of the readings during motion minus the averaee of the two stationary readings and was expressed in degrees. Resolution of measurement was 0.1’. Torsion measurements were taken in a similar fashron. To track the turning of the eyes. a photoflash unit was used to create an afterimage of a horizontal line on both retinae while the disk was at rest. When the display was set in rotation. cyclotorsion of the eyes produced a shift in the apparent locus of the afterimage relative to the cursor bar. The subject aligned the cursur with the afterimage. thus giving a reading for torsion. Again. a reading was taken before the display began to rotate. Five readings were taken wrth the field in rotation. Finally. a second reading was taken with the field again at rest and magnitude of torsion computed in the same way as that for tilt. A single session consisted of torsion and trlt measurements for the in and out of phase conditions for live strobe hequencies (8. IO. 12, 15, and 20 Hz,. To mimmize within and across session variability. in phase and out of phase conditions for a single frequency were run successively. The order of frequencies was random within a session and the order of in and out of phase conditions was random within a frequency. A session took approximately 45 min.
Three males. familiar with the apparatus and the cxperiment and between the ages of 23 and 30, ran three sessions of torsion and tilt each. One female. age 20. naive as to the nature of the experiment and unfamilar with the apparatus. ran one session of tilt and torsion. Ail these subjects had normal acuity (Sneilen 20’20 or better). stereovision. and no sign of any abnormality of vision at the 25 cm viewing distance. Three males and three females. judged to be stereodeficient by their faiiure on the Army vtsron test for stereoacuity (Bausch and Lomb Armed Forces Vision Tester Type 71-21-10) ran one session each of tilt and torsion. In these subjects. the stereodeficiencies could be traced to childhood visual anomalies such as strabismus. “lazy eye”. and so forth. Most of them had reduced acuity in the nondominant eye. A&ties were never worse than 204O with correction. Thus, their acuity was sufficient t@ resolve motion of the display. RESULTS
Normnl subjecrs
Ths magnitude having
the subject
of the perceived tiit was measured by first manually rotate a cursor bar to
Figures 2a and 2b present the mean three normal subjects for tilt and torsion
data for the respectively.
Eye torsion and visual tilt are mediated by different binocular processes
x 31 c s
.
I” l“.SE
.
I” c*.,c
.
WI
.
OUT 01 C”.M
oc ,*.sc
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FREOUENCY
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FREQUENCY
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/
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.
L. FREOUENCY
(Hz)
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MONOCULAR
(Hz)
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MONOCULAR
I IZ
1,
FREOUENCY
20
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Fig. 2. In each of figures Za-d, magnitude of tilt or torsion is plotted as a function of monocular strobe frequency. In the out of phase condition the binocular frequency would be twice the monocular frequency. Binocular summation is indicated when the magnitude of an effect at a specific frequency is greater for the out of phase condition than for the in phase condition. Summation is clearly evident in Za, b, and d. Only in Zc, Tilt-Stereoblind subjects, is there no evidence for summation.
As was noted in the Methods section, the magnitude of both torsion and tilt increases as the strobe frequency is increased from 8 to 20 Hz. Within a given session, the subject’s five readings at a specific frequency generally had a range of kO.5”. There were session-to-session differences, moderate differences within a single subject’s three sessions, larger differences among subjects. However, the relation of the in and out of phase results remained constant across sessions and subjects and justifies the presentation of average data. Figures 2a and 2b show that for normal subjects the magnitude of tilt and torsion is greater in the out of phase condition than in the in phase condition. Taking each of the ten sessions as an independent trial, the binomial test shows the differences to be significant at the 0.01 level for all frequencies in the tilt data and for all but the 8 Hz condition in the torsion data. The 8 Hz torsion effect is significant at the 0.05 level. The finding that the out of phase condition produced a larger effect than the in phase condition at each strobe frequency is consistent with the hypothesis that the production of tilt and torsion in normal subjects involes binocular processes. Stereodeficienr subjects Figures 2c and 2d present the averaged data for the stereodeficient subjects. In graph Zc, it is obvious that there is no significant difference. between the in phase and the out of phase conditions. This pattern of results was found in ail six of the stereodeficient subjects. Figure Zd, however, shows a very different pattern of results for torsion. The average data show
that the out of phase condition consistently produced more torsion at a given strobe frequency than did the in phase condition. This indicates that stereodeficient subjects still show binocular summation for torsion. This pattern of results was produced by all six of the stereodeficient subjects. In fact, the results produced by these subjects are indistinguishable from those produced by the stereonormal subjects. Apparently the stereodeficiency shared by these six subjects did not disrupt the binocular process mediating torsion. DISCUSSION
Three conclusions may be drawn from these results: First, in normal subjects, the production of both tilt and torsion is mediated in part by binocular processes. Since this experimental design did not eliminate all monocular cues, it is not yet known if these effects are mediated in cooperation with a monocular process. Second, the binocular process for torsion is different than that for tilt. This result was shown by comparing the results for stereodeficient subjects to those for normal subjects. Third, the stereodeficient individuals seem to lack the process required for binocular summation in tilt, but possess the process required for summation of torsion. It appears, then. that the binocular process involved in torsion is resistant to some forms of early binocular deprivation. It could be argued that the pattern of results found in these subjects arose not from the loss of a binocular process for tilt but, rather, from the effects of some other visual pathology. Several such hypotheses may
3_‘0
JEREZII
11. M.OLFE.
be considered and discarded. One possibility is that the stereodeficient subjects could not fuse the rotating disk. If the disk was seen as double. the observer would not see simple rotary motion but some complicated form of apparent motion that might be insuhicient to produce binocular summation for tilt. None of the subjects, however. reported diplopia except at the slowest flicker rates. At these frequencies stereonormal subjects also noted some transient diplopia. Furthermore. this hypothesis and any other proposai not based on the notion of separate processes for torsion and tilt must account for the preservation of binocular interactions in torsion. Diplopia should have a similar elect on both tilt and torsion. Several of the stereodeticient subjects were amblyopic. It might be proposed that the lack of binocular summation in these subjects was due to the suppression of the amblyopic eye. An effectively monocular subject could not be expected to show bmocuiar summation. As vvith the diplopia hypothesis, this explanation would have difficulty accounting for the continued presence of binocular summation for torsion. Moreover. at Least two of the stereodefrcient subjects had equivalent acuities in their two eyes. In general, if pathology is to be used as an explanation of the data. that pathology must have two characteristics: (I) it must be present in all of the stereodeficient subjects; and. (2) it must be sufficient to explain the loss of summation for tilt while accounting for the sparing of torsion. The only shared pathology meeting these requirements is the reduction in stereoacuity shown by all six stereodeficient subjects. It. therefore, seems reasonable to conclude that the condition responsible for this lack of stereo ability is also responsible for the loss of summation for tilt and that this condition does not produce a foss of binocular summation for torsion. The description of the paradigm used in this experiment stated that a 10 Hz out of phase condition would produce a 20 Hz cyclopean signal. It is obvious from the data presented that. while IO Hz out of phase does produce more of an effect than 10H.z in phase. it does not produce as much of an effect as 20 Hz monocular or in phase signal (Fig. 2). This indicates that the binocular interaction is not simply a linear summation. Over the range of frequencies from 8 to ‘0 Hz. an out of phase signal of “N” Hz is not equivalent to “ZN” Hz monocular or in phase. It is equal to a 1.X-1.4 N Hz signal. Several workers have proposed “vector-sum” for binocular interactions (e.g. for brightness: Curtis and Rule, 1978). If the binocular interaction in the out of phase condition is seen as the summation of two orthogonal vectors of equal length, then their sum is not 2 K but t ‘2 N = 1.4 N. This is very close to the observed summation and provides a potential clue for future work. It is of some interest to speculate about the nature of the neuronal mechanisms that might underly the results described above. The binocular process must be one that is capable of performing a correlation between the two eyes when the two inputs are slightly displaced in space and time but are otherwise identical. l_!l]man (1977) has discussed the constraints on such a process in theoretical terms. Two such mechanisms would appear to be present here, one
Ind
RICHARD HELI)
ijr torsion and one for tilt. The bmocular tilt mechanisms must be sensitive to the abnormalitres introduced by defects like stabismus because such abnormalities seem to cripple this binocular process. On the other hand. the torsion mechanism is less sensitive to such changes. as its binocularity is not Impaired by those defects. In this light, it is interesting to consider the results of artificially induced strabismus in animals. Hubel and Wiesel ( 1965) have shown that normally binocular cells in areas 17 and IS of the cat become prsdominantly monocular in cats reared with only alternating monocular exposure to light. Interestingly. Gordon and Presson (1977) found that similar rearing does not reduce the proportion of binocular units in the superior colticuii. Their cats did show the prepoderance of monocular units in the correx but the coilicuii appeared to be normal. Bmocular units hate also been found in various nuclei of the accessory optic tract (Hoffman and Schoppman. 1975) but the response of such units to artificial strabismus IS not knou-n. ,At least one physiological investigation. that of Gordon and Presson (1977). shows that artiticial strabismus can eliminate one binocular process while sparing another, a pattern of results similar in kind to that found in the experiments reported here. IVe may speculate that the separation of the two processes corresponds to the existence of two scparst? sites in the visual nervous system. .Icknot\lrciymlmrs-The authors would like to thank D. ,a. Owens. J. A. Bauer. J. Thomas. f. H. Sandelf. and J. Gwiazda for consultation on this project. This research was supported in part by grants from X.4S.A (No. NGL-22-009-308) and NIH {No. I-Roi-EY011649,).J. Wolfe had support from NIH-l-T31-GXfOi-tS4.
REFERENCES
Curtis D. W. and Rule S. J. (1978) Binocular processing of brightness information: A vector-sum model. J.E.P.: H.P.P. 1. 133-143. Dichgans J., Held R.. Young L. R. and Brandt T. (IV?) Moving visual scenes influence the apparent dirtcrivn of gra;tty. Science; S.Y. i38, IZt7-1319. Finke R. and Held R. (1975) State reversals of oprictillq induced tilt and torsional eye movements. Percrpr. Pi!,chophys.
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Gordon B. and Presson J. (1977) EfTectj of alternattnd occlusion on receptive fields in cat superior colliculus. J. i~guru~h~sio~. 40, 14061414. Held R., Dicheans J. and Bauer J. (1974) Characteristics of moving hsual scenes influence spatiai orientation. k’ision Rex 15, 357-365. Hoffman K.-P. and Schoopman A. (1974) Retinal Input .. to direction selective cells in the nucleus tractus opticus of the cat. Brain Res. 99. 359-366. H ubel D. H. and Wiesel T. N. (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J. Xew~ph~~id. 28, 1011-1059. Julesz B. (1971) Foundarions o/ C~clopeuh Percrprion. The University of Chicago Press. Chicago. Xiovshon J. A_ Chambers B. E. I. and Blakemore C. I 19721 Interocular transfer in normal humans. and those *ho lack stereopsis. Prrception 1, 483-490. Ulfman S. (1977) The interpretation of visual motion. DOCtoral dissertation. M.I.T.. Cambridge. 31.4.