Respuestas acomodativa y pupilar a los estereogramas de puntos aleatorios
Disparidad; Resumen Investigamos la dinámica de las respuestas acomodativa y pupilar a los estereogra-mas de puntos aleatorios (RDS) que se presentaron en disparidad cruzada y no cruzada en
∗ Corresponding author at: Department of Computer Science and Engineering, 4700 Keele Street, Toronto, Ontario M3J1P3, Canada.E-mail addresses: [email protected], [email protected] (R. Suryakumar).
The pupil is an important oculomotor system that isaffected by a diverse set of stimuli including changes inretinal luminance,1,2 sudden changes in stimulus motion,3
emotional4 and cognitive factors,5 grating stimulus param-eters and color.6,7 In addition, changes in accommodation8,9
and/or vergence10 have also been shown to result in pupilconstriction (miosis) via the near triad.11 Functionally, theconstriction of the pupil limits the amount of light enteringthe eye, reduces optical aberrations (until the eye becomesdiffraction limited) and improves the depth of focus. Theselatter changes also have strong effects on the performanceof other oculomotor systems. For example, pupil constric-tion improves the depth of focus of the eye and this reducesthe demand for precise accommodation.12 Pupil responsesto optical blur, changes in ambient luminance and fusionalvergence eye movements have also been shown to exhibit astrong nonlinearity in their response characteristics depend-ing on the pupil’s initial diameter. Specifically, pupil miosisis larger in amplitude when initiated from intermediatestarting diameters (4---5 mm) compared to larger or smallerdiameters.13,14 It has been suggested that this effect reflectsa non-linearity within the iris motor plant.
It has been reported that pupil responses can beelicited by disparity in dynamic random-dot stereograms.Li et al.15,16 studied pupil responses to dynamic random-dot stereograms (DRDS) that changed from depicting a flatsurface to a sinusoidal corrugation in depth (appearing inuncrossed retinal disparity) using an infrared pupillometer.In all three subjects, there was transient constriction ofthe pupil concomitant with the change in disparity. Thepupillary response was characterized by a long reaction
time (∼500 ms) and was not accompanied by a change invergence.16 The constriction was not apparent with monoc-ular viewing of one half-image of the DRDS and, under
fee
inocular viewing, its magnitude increased with increasen the spatial-frequency and amplitude of the corrugation.ince there were no changes in either blur or luminance, theependence on the disparity-defined form led the authorso suggest that ‘stereo information’ drove the pupil con-triction although they did not speculate whether this mighterve any behavioral purpose.15,16
When such step changes in retinal disparity arentroduced in a random-dot stereogram (RDS), the per-eption changes from a flat surface without depth to aurface with stereoscopic apparent depth. The direction ofhe apparent depth depends on the sign of retinal dispar-ty. Crossed disparities depict depth in front of a fixationlane and uncrossed disparities depict depth extendingeyond the fixation plane. The magnitude of the simulatedepth increases with increase in the disparity in the RDS.ntroducing a mean uncrossed or crossed disparity simulatesncreases or decreases (respectively) in the mean distances well as the depth of the stimulus. This apparent distancehange could induce proximal accommodation, even if fixa-ion distance were held constant, assuming spatial poolingf the retinal stimulus to accommodation.17,18 While ear-ier studies recorded changes in pupil size, measurements ofccommodation were not attempted. It is possible that, dueo the commonalities in the neural control, pupil responseso stereoscopic stimuli such as RDS could be accompanied byoncomitant changes in accommodation. It is also possiblehat the oculomotor system works to achieve more accurateccommodation in response to a large range of appar-nt depth, resulting in an increase in the accommodativeesponse to partially or fully offset the typical accommoda-ive lag for the stimulus demand or the increased depth ofocus from pupil constriction could decrease the demand
or accurate accommodation. In either case, it would bexpected that such changes in ocular focus would be mod-st in the interest of maintaining a clear perception of the
bject seen in depth (which of course remains optically inhe plane of the display regardless of disparity).
To obtain a better understanding of these issues, wenvestigated the dynamics of pupil and accommodationesponses to either crossed or uncrossed disparities pre-ented within a random-dot stereogram. To the best ofur knowledge, both accommodation and pupil responseso cyclopean stimuli (such as RDS) have not been reportedefore. While Li et al.15,16 studied only pupil responses toncrossed retinal disparities; we investigated accommoda-ion and pupil responses to both crossed and uncrossedisparity. Furthermore, our experimental paradigm wasmproved on the earlier work by using a mirror stereoscopeisplay, which avoids the cross-talk artifacts associated withhe time-sequential shutter glasses used in the experimentsy Li et al.15,16
ethods
ubjects and experimental set-up
ix adult subjects (Mean age = 25.8 ± 3.1 years) participatedn the study. All subjects had a best-corrected visual acu-ty of at least 6/6 in each eye and normal binocular vision.he experimental procedure was conducted with the under-tanding and consent of the subjects and followed the tenetsf the Declaration of Helsinki. The random-dot stimuli wereenerated on a G4 Power Macintosh computer using Python.3. Stereoscopic half images were displayed on a pair ofomputer monitors (Clinton DS2000HB, 14.25′′ × 10.7′′), oneor each eye, placed at 60 cm set and viewed through pel-icle beam splitters (03 PBS 003, Melles Griot, USA) in aheatstone stereoscope arrangement. The monitors were
alibrated and set to a resolution of 1024 × 768 at 100 Hz. custom built eccentric photorefraction system providedeasures of accommodation and pupil responses at a samp-
ing rate of 100 Hz. The photorefractor consisted of a CCDrewire camera (EC 750, Prosilica Inc., Canada), which
maged the right eye from a distance of 70 cm, and annfrared illuminator LED array (OP290A, Optek Technologies,X, USA), which provided eccentric illumination of the eyeue to its vertical offset from the center of the camera aper-ure. The photorefractor recorded a video file (292 × 263ixel resolution, 8 bit monochrome image) which capturedhe dynamic changes in pupil size and accommodation. Theideo file was exported to custom software (Dynamic Pho-orefraction System) which provided a calibrated output ofupil size and accommodation.19
timuli
he stimuli were random-dot stereograms with a fixationoint in the center. The RDS subtended 5.71◦ and with a dotensity of 15% black pixels on a white background (Fig. 1A).he stereoscopic half-images were generated using MATLABR2006b, Mathworks Inc, USA) and Adobe Photoshop 7.01Adobe Inc., USA). During the experiment, the RDS changed
rom depicting a zero disparity flat surface to a stationary.5 cpd, 30 arcmin peak disparity, sinusoidal corrugation inepth. The sinusoidal corrugation was offset from fixationo that it appeared to extend in front of the fixation plane
orpc
R. Suryakumar, R. Allison
or crossed disparity trials and to extend behind the fixationlane for uncrossed disparity. In both conditions, the fixa-ion point in the center of the RDS remained at the planef the computer monitors and at a peak (for the uncrossedase, with the remainder of the corrugation lying beyond thecreen plane) or trough (for the crossed case) of the corru-ation. Thus, in all trials, the vergence required to fixatehe target remained at the screen distance for both the flatnd corrugated stereograms (Fig. 1A). The nearest point onhe uncrossed corrugated stimulus and the farthest point onhe crossed corrugated stimulus laid at the screen plane.
alibration trials
upil and accommodation data from the photorefractorere analyzed and calibrated using custom software. For
he pupil, a scale factor was used to convert pixels (in themage) to millimeters. A metal rule was placed in the planef the pupil and imaged using the photorefractor. From thesemages the number of pixels per mm was estimated visuallyor each mm interval over 1 cm on the rule. This resultedn 10 measures which were then averaged to yield one finalpatial calibration factor. For the image resolution used inhis study, the spatial calibration factor was 16.9 pixels perillimeter.The procedure for accommodative calibration using the
hotorefractor was similar to previous investigations.19---21
riefly, the subjects held an infrared glass filter (R-72 Hoyaptics, USA) in front of one eye (right) which blocked visible
ight while the other eye (left) fixated on a high contrast tar-et set at a distance of 65 cm. Ophthalmic lenses (1D stepsor a range of +1.5 to +3.5D) were introduced in front of theight eye to induce refractive errors while the photorefrac-or recorded the brightness profile across the pupil in theight eye. The rate of change of pupil brightness (slope) washen plotted as a function of the induced refractive error (D)nd this provided the calibration equation for each subject.ig. 1B shows the calibration data for all the subjects.
rocedure
ollowing calibration, subjects were seated at the appara-us with head restrained with a chin and forehead rest. Onach trial, they were required to fixate the central fixationoint. Initially the correlated RDS appeared as a flat surfaceithout depth and after a random time interval of 2---3 s theat RDS changed to a sinusoidal corrugation in depth. Duringhis transition, the subjects continued to maintain fixationt the central fixation point in the RDS. The photorefractorecorded the accommodation and pupil responses from theight eye during this stimulus transition as a video file at aampling rate of 100 Hz.
nalysis
nce the raw accommodation and pupil responses were
btained from the photorefractor software, an analysis algo-ithm was used to determine the response amplitude andeak velocity. Complete details on this analysis algorithman be found elsewhere.21 Briefly, the raw accommodation/
Accommodation and pupil responses to random-dot stereograms 43
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Figure 1 (A) Stereo half images presented to each eye shown in crossed disparity (with cross-eyed fusion). Subjects were instructedto maintain fixation on the center dot while the stimulus changed from a flat presentation to a stereoscopic corrugation. (B)Photorefractor calibration showing the slope of the brightness profile across the pupil as of function induced refractive error (+1.5to −3D). Linear regression was used to define an individual calibration equation for each subject which was used to convert slope ofthe brightness profile to refractive error in the vertical meridian (accommodation). (C) Dynamic pupil and accommodation responsesduring uncrossed and crossed disparity demands. The raw accommodation (shown by filled circles) and pupil responses (shown byfilled squares) were filtered to remove noise artifacts and the resulting smoothed profile is shown as a solid green and red line,respectively. The start and end coordinates of the two responses were identified using a velocity threshold criterion and the ratio ofpupil change to accommodation was determined and compared. Note that the scales for two pupil plots for crossed and uncrossed
feren
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disparity were offset, albeit with the same intervals, due to dif
pupil position were differentiated using a two-pointdifferentiator22 and then the velocity and position responseswere filtered/smoothed using a ten-point FFT low-pass fil-ter. The start and end co-ordinates of the response to changein apparent depth were then identified using a velocity
threshold criterion. This criterion has been frequently usedto determine the start and end coordinates of oculomotorresponses like saccades, vergence and accommodation.23---25
For example, the response onset for accommodation was
aace
ces in starting pupil size for the example traces.
efined as the first point where velocity exceeded 0.5 D/snd continued to do so (in a consistent direction) for theext 100 ms. An opposite/inverse criterion where velocityell below 0.5 D/s and continued to do so for the next 100 msas used to define the response end. The response onset
nd end points identified by this procedure were also visu-lly inspected to ensure accuracy and consistency. A similarriterion of 0.20 mm/s was used for estimating the start andnd points for the pupil responses. The difference between
4 R. Suryakumar, R. Allison
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y = –0.08x + 0.83, R2 = 0.21, p<0.05
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Figure 2 (A) The amplitude of pupil response plotted as afunction of initial (starting) pupil diameter. Peak velocity ofpupil responses as a function of response amplitude (B) andstarting position (C). Amplitude of pupil constriction was sig-ns
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4
he start and end point measures was defined as the responsemplitude and this was individually determined for bothupil and accommodation responses. Also, the ratio of themplitude of pupil change to accommodative change wasetermined separately for crossed and uncrossed disparityonditions. In addition, for the pupil response, the peakelocity (mm/s) was plotted as a function of amplitudemain sequence) and as a function of the initial (starting)upil diameter.
esults
ig. 1C shows typical changes in pupil diameter and accom-odation after the stimulus changed from a flat surface
o a sinusoidal corrugation in depth (for both crossed andncrossed disparity). Under both disparity conditions, thereas a pupil constriction and this change in pupil size waslso accompanied by a concomitant increase in accommoda-ion. The mean amplitude of the pupil and accommodationhange were 0.28 ± 0.12 mm and 0.23 ± 0.09D, respectively,or step changes in uncrossed disparity and 0.41 ± 0.36 mmnd 0.29 ± 0.19D, respectively, for step changes in crossedisparity. The magnitude of the change in pupil size orccommodation was not significantly different betweenrossed and uncrossed disparity (paired student t-test,
> 0.05) but was significantly greater than zero (p < 0.05).he mean ratio of the change in pupil size to change
n accommodation was 1.39 mm/D and 1.43 mm/D forncrossed and crossed disparity, respectively. The ratio wasot statistically different between the two disparity typespaired student t-test, p > 0.05).
As pupil changes were similar regardless of the typef retinal disparity, the responses to both crossed andncrossed disparity were pooled and three separate plotsere generated to examine the effect of starting diame-
er of the pupil (initial pupil diameter at response onset)n response dynamics. The amplitude of the pupil constric-ion was plotted as a function of starting diameter of theupil (Fig. 2A). In addition, the peak velocity of the pupilesponses was plotted as a function of response magnitudeFig. 2B) and as a function of initial pupil position (Fig. 2C).he results show there was a significant effect of the start-
ng pupil diameter on response dynamics. Amplitude of pupilonstriction and its velocity varied inversely as a function oftarting pupil diameter suggesting larger and faster pupilonstrictions were associated with smaller starting pupiliameters. Also, the main sequence of pupil showed a lin-ar increased in peak velocity of the pupil responses as aunction of response amplitude.
iscussion
his experiment provides a more complete description ofupil and accommodation dynamics in response to a sud-en change in apparent stereoscopic depth. We confirm thatisparity-specified depth changes introduced in random-dottereograms elicit pupil constriction15,16 and also found a
reviously unreported small but concomitant increase inccommodation for both crossed and uncrossed disparitytimuli. We extend the earlier studies by measuring theynamic properties of accommodation and pupil responses
biNb
ificantly lower for larger initial starting pupil diameters. Also,uch responses were significantly slower.
or both crossed and uncrossed disparity demands. Theotor responses had the same sign regardless of the sign
f stimulus disparity.For introduction of both crossed and uncrossed disparity
nto the stimulus, pupil size decreased and accommodationncreased. This suggests that the responses were driven byhe apparent depth signal in the fused stimulus and not byhe simulated distance. Normally, retinal disparity signalshe range of depth over the target stimulus (RDS in thistudy). A large disparity range within the target would sig-al a need for a greater depth of field in order to maintainlarity and avoid defocus especially at the proximal or distalnds of the depth interval. A decrease in pupil size would
e an effective optical strategy to deal with this need ast provides clear focus over an extended depth interval.ote that in the RDS stimuli used, depth was signaled solelyy disparity --- in the current experiment fixation remained
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Accommodation and pupil responses to random-dot stereogr
stable at the plane of the monitor and all stimuli were opti-cally at this distance. Thus, unlike natural stimuli, therewas no actual demand for increased depth of field associ-ated with the disparity. Pupil constriction would not reduceblur in the stereoscopic stimulus and this lack of feedbackmay explain the transient nature of the pupil response.
The concomitant changes in accommodative responseobserved in this study may be due to commonalities in theneural control of accommodation and pupil responses under-lying the near triad. The motor impulses for both responsesoriginate in the Edinger---Westphal nucleus, a subdivisionof the oculomotor nucleus, located in the midbrain. TheEdinger---Westphal nucleus contains first-order parasympa-thetic neurons which synapse in the ciliary ganglion whilethe second-order neurons travel from the ganglion to theglobe, eventually innervating the ciliary muscle and sphinc-ter pupillae, thus causing accommodation and constriction,respectively.26 Although one might expect that an increasein accommodation would cause the retinal image to defocus,it should be noted that the magnitude of the accommoda-tive response during both crossed and uncrossed disparitypresentation was well within the normal depth of focusinterval.27---29 In addition, the accommodative system isknown to exhibit a physiological lag in its response for agiven stimulus demand30 and based on age, refractive errorof the subjects and the experimental set-up used in thisstudy, a physiological accommodative lag of up to 0.5D couldbe expected.31 Hence, the small increase in accommoda-tion following the onset of the disparity stimulus would beexpected to decrease the physiological lag and increase theaccuracy of accommodation. Hence, the changes in accom-modation observed in this study would not be expected toadversely affect the clarity of the image.
It should be noted that Li et al.15,16 excluded accommo-dation changes. In their study, only pupil size and ocularvergence were monitored continuously. Hence, it is notknown if accommodation changed during binocular condi-tions since it was not measured. Their basis for excluding arole for accommodation was based on observations obtainedwhen the stereoscopic images were viewed monocularly. Asaccommodation is active monocularly, it was concluded thatthe lack of change in pupil responses under these condi-tions provides evidence against a role of accommodation.However, this is an incorrect presumption. Under monocularconditions, the disparity signal is absent and hence there isno stereoscopic depth to drive the pupil response. In otherwords, the apparent depth signal which triggers a changein the pupil size is absent under monocular conditions andhence, it is not surprising that pupil constriction was notobserved monocularly by Li et al.15,16 On the other hand, inour study, both accommodation and pupil responses weremonitored using the photorefraction system. During bothcrossed and uncrossed disparity presentations, accommoda-tion and pupil showed a consistent change.
The third aspect of the near triad is convergence. Oneof the limitations of the present study is that the ver-gence response of the eyes was not continuously monitored.Although, stimulus vergence remained constant throughout
the experiment and the subjects were instructed to carefullymaintain the fixation, small errors in vergence state (i.e.,fixation disparity) cannot be ruled out. In this case, the syn-ergistic links of the near triad could have also triggered a
mrmb
45
hange in pupil size. However, it is unlikely that this couldroduce the pattern of results we found in this study for twoeasons. First, as noted above, Li et al.15,16 monitored ver-ence with similar stimuli and found no consistent vergencehanges. Second, one would expect any stimulus driven ver-ence response to reflect the sign of the stimulus disparity.he fact that our accommodative and pupil responses weref the same sign regardless of disparity suggests that theyere not elicited by vergence error.
A reviewer asked us to speculate on the possible resultsf this experiment in subjects with central scotomas. Depthf field increases with eccentricity reflecting the varia-ion in visual acuity across the visual field.32 Similarly, theffectiveness of defocus blur as an accommodative stimu-us should also decrease with eccentricity as acuity declinesand effective depth of focus increases).33 Consistent withhis prediction, White and Wick34 found that accommo-ation response to defocus blur was reduced in juvenileacular degeneration (Stargardt’s disease). The degree of
eduction was generally greatest in those with the poo-est acuity. Interestingly, when provided with proximal andinocular cues to accommodation, the subjects respondedith more accurate accommodation than with defocus blurlone. Thus, we might speculate that this increased sen-itivity to cues other than defocus blur might produce aarger response to binocularly disparate stimuli in observersith central scotomas compared to our normal subjects.uane35 reported that patients with small, faint centralcotomas often present with signs resembling accommoda-ive insufficiency and our results suggest that these signsight be reduced in the presence of stereoscopic cues.onversely, due to the decreased acuity in the periphery,he demand for increased depth of focus with increasedepth in the stimulus might be reduced producing a smallerffect in central field loss than we found in normal subjects.etermining the effects of disparity on pupil size and accom-odation in subjects with central field loss must be resolvedy experimental research. The functional implications ofhese findings need to be investigated further to under-tand if clinically, the drive for increased accommodation,oncomitant increase in depth of field and conflict betweenhe accommodation and vergence systems might causeifficulties in viewing stereoscopic displays and moviesn normal subjects and in subjects with binocular visionnomalies.
Finally, another important result of this study was thathe dynamic characteristics of the pupil responses, specif-cally amplitude and peak velocity, appear to depend onhe initial (starting) pupil diameter. Amplitude of pupilonstriction was significantly less when responses startedrom larger pupil diameters. Such responses were also sig-ificantly slower. While these dynamic properties of pupilesponses have been reported for other stimuli such as blur,hanges in ambient light levels and also for accommoda-ive and fusional vergence responses,14 our results havextended this finding to pupil responses driven by apparentepth in stereoscopic stimuli. Together, the findings sug-est that the starting position or initial state of the iris
otor plant has a strong influence on the final pupil response
egardless of the nature of the sensory stimulus. This com-onality suggests that the source of this non-linearity coulde attributed to the iris motor plant.
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34. White JM, Wick B. Accommodation in humans with juvenile
6
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pparent depth in random-dot stereograms producesynamic pupil and accommodation responses. While theagnitudes of these changes are small, the responses have
he same sign regardless of the sign of the horizontal reti-al disparity. When viewing stereoscopic images, the visualystem appears to employ a strategy to control ocular focusithin the apparent depth interval by decreasing pupil sizend increasing depth of focus.
onflicts of interest
he authors have no conflicts of interest to declare.
cknowledgements
his study was funded by Natural Sciences and Engineer-ng Research Council of Canada (RA) and Canadian Institutesf Health Research (CIHR) Strategic Training Grant in Visionealth Research (RS). The authors would like to thank thewo anonymous reviewers who provided constructive com-ents that helped improve the manuscript.
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