Contour Integration in Anisometropic Amblyopia

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1 Pergamon PII: (97) Viion Re., Vol. 38, No. 6, pp , Elevier cience Ltd. All right reerved Printed in Great Britain /98 $ Contour Integration in Aniometropic Amblyopia ROBERT F. HE,*t RITA DEMANIN* Received 11 December 1996; in revied form 14 April 1997 Contour integration wa meaured in a group of aniometropic amblyope to tet the idea recently put forward that poitional uncertainty et a fundamental limit to contour integration in amblyopia. Aniometropic amblyopia, unlike trabimic amblyopia, ha little or no poitional uncertainty once the initial filtering lo ha been taken into account. Therefore, according to the explanation put forward to explain trabimic amblyopia, aniometrope hould exhibit normal contour integration. We how that thi expectation i realized for five of our ix aniometropic amblyope Elevier cience Ltd. All right reerved. Amblyopia Aociation Poitional uncertainty Contour integration INTRODUCTION In a recent tudy, it wa hown that contour integration i anomalou in trabimic amblyopia (He, McIlhagga & Field, 1997). However, thi wa due olely to the accompanying internal poitional uncertainty aociated with the condition. The fellow dominant eye with an equivalent level of external poitional uncertainty exhibited comparable level of performance on the contour integration tak (Field, Haye & He, 1993). An appealing explanation for the poitional uncertainty in trabimic amblyopia i a diordered cortical repreentation due to the failure of elf-calibrating procee in early viual development a the reult of the eye mialignment (He, Campbell & Greenhalgh, 1978; He, Field & Watt, 1990; He & Field, 1994; but alo ee Levi & Klein, 1986). Thi ugget that there are normal interaction between cell whoe poition are diordered. Aniometropic amblyope, unlike their trabimic counterpart do not exhibit meaurable amount of poitional uncertainty either at the limit of reolution (Levi & Klein, 1982, 1985, 1990) or for target well within the reolution limit (He & Holliday, 1992; Demanin & He, 1996) once their filtering loe have been taken into account. Auming that the major difference between the two condition i poitional uncertainty, one would expect contour integration to be normal in aniometropic amblyopia. Here we examine thi iue uing the paradigm of Field et al. (1993). McGill Viion Reearch Unit, Department of Ophthalmology, McGill Univerity, 687 Pine avenue Wet, Room H4-14, Montreal, Quebec, Canada H3A IAI. tto whom all correpondence hould be addreed [Fax: ; rhe@bradman.viion.mcgill.ca]. 889 METHOD In all experiment the oberver' tak wa to identify which of two preentation contained the "path timulu". A path timulu conited of a et of oriented Gabor element aligned along a common contour, embedded in a background of imilar, but randomly oriented Gabor element. A no-path timulu conited of jut randomly placed and randomly oriented Gabor element. Gabor element were ued to control the patial frequency compoition of the timuli o that the path could not be extracted by a ingle broad band detector. By uing uch timuli we hope to gain a better undertanding of the combinatorial rule which govern the output of viual neurone ued in the extraction of the path from the background element. timuli Oriented patial frequency bandpa element were ued in thi tudy; the oriented Gabor element were defined by the equation: g(x, y, O)c in(27rf (xin0 + yco0))exp ( x2 +y2-2~ J' where 0 i the element orientation, from 0 to 360 deg, (x,y) i the ditance in degree from the element centre, and c i the contrat. The inuoidal frequency f= 0.05 c/pixel, the pace contant ~ = 0.4 x 2. The contrat wa 90%. The patial frequency varied for the particular amblyope (ranging from 3 to 12 c/d; ee Appendix of He et al., 1997 for complete timulu parameter). A no-path timulu wa contructed in the following way. A 624 pixel wide quare wa divided into a 13 by 13 grid of equally ized cell. A Gabor element of random orientation wa placed randomly in each diplay cell, (1)

2 890 R.F. HE and R. DEMANIN A B C D FIGURE 1. A path compriing eight micropattern (end point indicated by arrow) i embedded in a field of randomly oriented micropattern of the ame form. Path are hown for different path angle (ee Fig. 2). (A) 0 deg; (B) 10 deg; (C) 20 deg and (D) 30 deg. with the retriction that each cell contain the centre of only one Gabor element. Thi eliminate the clumping of element due to random placement. The element were alo placed to avoid overlap a much a poible. An empty cell occurred if the cell' Gabor patch could not be placed without ignificantly overlapping any of it neighbour (i.e. crowded out by it neighbour). There were fewer than 4 per image. A path timulu conited of two part; the path itelf and the background (Fig. 1). The contruction of the path i decribed in detail elewhere (He et al., 1997). The path had a backbone of eight inviible line egment; each line egment wa of length 67 pixel and the line egment joined at an angle uniformly ditributed from -4 to ~ + 4 deg. ~ I called the path angle. Gabor element were then placed at the middle of each line egment. The orientation 0 of each element wa the ame a the orientation of the line egment on which it wa placed. The element angle which i defined a the angle that the oriented element make with the inviible backbone would be zero in thi cae (ee He et al., 1997 for more detail). Apparatu and experimental procedure All timuli were diplayed on a ony Trinitron monitor driven by a un parc tation 2 computer, which generated timuli on-line and controlled diplay and data collection. The mean luminance wa 35 cd/m 2 (ee He et al., 1997 for more detail). An experimental run conited of a block of 50 trial. During each trial, two image were preented (a path in a noie background and a noie background image alone) in random order. The ubject' tak wa to indicate with a button pre which preentation contained the path. In each run, the path angle ~ wa et to 0, 5, 10, 20, 30, 40deg etc. Each preentation wa of a 2 ec duration. Typically, each block wa repeated twice to obtain at leat trial per path angle. Poitional uncertainty We meaured the poitional uncertainty of the amblyopic eye uing a 2AFC dicrimination tak between a path compoed of accurately poitioned element (a pedetal of zero uncertainty) and an identical path

3 CONTOUR INTEGRATION IN ANIOMETROPIC AMBLYOPIA 891 TABLE 1. Clinical data for the ix aniometropic amblyope Age Letter Ocular ubject (year) ex Eye Refraction acuity alignment Hitory JC anlo TK amo VA anlo CP anlo LC anlo CA anlo 34 M RE plano 6/4.5 ortho LE D 6/36 40 F RE / / ortho LE plano 6/ F RE 1.25 D 6/4.5 ortho LE / /9 37 F RE / /18 ortho LE / x 170 6/6 40 F RE plano 6/6 ortho LE D 6/30 23 F' RE plano 6/6 + 2 ortho LE / 2.00 x 005 6/90 amblyopia diagnoed age 7 year, no Rx, no patching, no urgery diagnoed aged 9 year, Rx age 9 year, no orthoptic, no urgery amblyopia age 8 year, firt Rx age 8 year, patching at 8 year for le than 1 year, no urgery intermittent RXT with firt Rx age 5 year, orthoptic age 5 year, no urgery diagnoed aged 8 year, no treatment diagnoed aged 6 year, patched at age 6 year, Rx never worn RE, right eye; LE, left eye; XT, exotropia; Rx, refractive correction. compoed of element aligned along the path with a variable amount of poitional uncertainty (2-D gauian ditributed). For thee meaurement there were no background element (jut the path element in iolation on a mean luminance background). A taircae procedure (200 trial) wa ued to collect pychometric data in the critical range and parameter were etimated by fitting a Weibull function to the pychometric data. Thi function had the form: p(x) exp -, (2) where p(x) i the probability of correctly dicriminating between the two path at a jitter variance of x. c Repreent the 81% correct threhold and b the lope of the pychometric function. Unequal trial were handled by the fitting procedure which ued maximum likelihood. From thi determination we obtained the delta uncertainty for one of a number of different path angle for each ubject. If thi wa ignificantly elevated, which did occur for one of our aniometropic amblyope, we went on to meaure the aociated intrinic uncertainty. To determine the level of intrinic uncertainty (within the amblyopic viual ytem) we revered the above procedure for the normal fellow eye. Thi time the increment wa held fixed at the level previouly determined for the fellow amblyopic eye and the pedetal uncertainty wa adjuted in the manner decribed above. The threhold which wa derived in a manner identical to that decribed above repreented the internal pedetal of uncertainty in the amblyopic eye, which correponded to the previouly determined incremental enitivity of the amblyopic eye. We are auming that the function decribing poitional uncertainty/pedetal uncertainty for the amblyopic eye i merely a laterally hifted verion of that for the normal eye. In other word, external and internal uncertainty are additive (for upport ee He & Watt, 1990 for normal viion and Watt & He, 1987 for amblyopic viion). We undertook thi determination for at leat three different path angle (ee He et al., 1997 for further explanation). Practice effect and experimental deign The practice that wa given on thi tak wa minimal and wa deigned to familiarize the ubject with the tak. We have found that 50 trial i ufficient to acertain that the ubject undertand the tak. Each ubject had a minimum of 50 trial, after which two et of 50 trial were collected. In two ubject, four et of 50 trial were collected. Run were alternated between the eye, alway beginning with the dominant eye. We did not ee any improvement in performance between the firt and final et of 50 trial for any of the amblyopic eye teted. The path angle wa elected randomly for each ubject. Acuity meaurement We determined the grating acuity for each ubject' amblyopic eye uing a 2AFC tak in which the ubject had to chooe which of two timuli were vertically oriented. The timuli compried a field of randomly poitioned Gabor element whoe carrier were either vertically or horizontally oriented. The creen parameter of thee Gabor were identical to thoe ued in ubequent path experiment. We meaured the maximal viewing ditance for which the orientation of our timuli wa viible. A viewing ditance which correponded to one half thi ditance wa choen for each ubject to enure that the element fell well within their retricted patial paband. The dominant eye of each amblyope wa teted at thi ame ditance. In caling path timuli of thi kind, one need to be mindful of the fact that larger timulu field invade more eccentric area, which may introduce an added difficulty into the tak becaue path falling in the periphery of the diplay may not be detected within a hort preentation time. pecial feature To overcome thi we introduced two feature into the timulu. The firt wa the contraint that the central

4 892 R.F. HE and R. DEMANIN A 9O rc cc OO 80- B o dominant eye amblyopic eye dominant eye fit e fit,,~ 70- n-" o w n T.K. I I I! C - ~ 90- rr c) ~ 70- (D ~ 60- D -,, 9O rr 6o To g o_ 60 dominant eye + amblyopic uncertainty E C.P. I I I I I F 50 CA! i! ~ 9o w rr ~ 80- b- m z 70- c~ 90 ~ 80- ~ 70- w a_ 60- ~ 60- I I I I I PATH ANGLE (decl) L.C. I I I I I I PATH ANGLE (de~l FIGURE 2. Contour integration of dominant (open ymbol) and fellow amblyopic eye (filled ymbol) are compared for ix aniometropic amblyope. The curve repreent the bet fitting olution to equation (2) (ee Method) for the dominant (dahed) and fellow amblyopic eye (olid). In one cae (CA) poitional uncertainty wa abnormal in the amblyopic eye and reult (bowtie) are hown for the dominant eye with timulu uncertainty equivalent to that etimated for the amblyopic eye. Error bar repreent the 95% confidence limit. element of the path had to fall within a defined central zone which wa et to a radiu of 30 pixel. Thi enured that path retricted to the peripheral region of the diplay were not diplayed. econdly, we et the expoure duration to 2 ec, wherea previouly we had ued 200 mec for normal viion. Thi enured that there wa plenty of time for an eye movement by the amblyopic eye hould that be neceary. Our previou reult had hown that there wa only a light improvement in performance between expoure duration of 50 mec and 2 ec. Clinical detail Table 1 lit the clinical detail of our group of ix aniometropic amblyope. They all were given a trial practice eion to familiarize themelve with the tak prior to data collection. REULT AND DICUION Contour integration wa compared between the dominant and fellow amblyopic eye of each aniometropic amblyope at a teting ditance for which the carrier frequency of individual Gabor micropattern wa a factor of 2 lower than the reolution capabilitie of each amblyopic eye. Reult are diplayed in Fig. 2 a percent correct a a function of path angle for dominant (open ymbol) and fellow amblyopic eye (filled ymbol). In each cae, the bet fitting error function are diplayed a dahed and olid curve, repectively (ee Table 2 for parameter). In all but one cae (CA: whoe acuity deficit

5 CONTOUR INTEGRATION IN ANIOMETROPIC AMBLYOPIA 893 TABLE 2. Parameter value for the fit of equation (2) to the contour integration pychometric data of dominant (DE) and fellow amblyopic eye (AE) Centering of ubject Eye function lope of function TK DE AE VA DE AE JC DE AE CP DE AE LC DE AE CA DE AE DE + ambly uncertainty wa the mot evere), there wa no ignificant difference between the bet fitting pychometric function for the dominant and fellow amblyopic eye. At the contrat and patial cale ued, the individual micropattern were approximately equally viible to the dominant and fellow amblyopic eye and under thee condition, performance on thi contour integration tak wa alo equivalent. In a eparate tak in which only the path wa viible, devoid of any background element, we meaured the incremental poitional uncertainty of both the dominant and fellow amblyopic eye at each of two path angle by dicriminating between perfectly aligned path (i.e., on a zero pedetal) and one in which a gauian ditributed 2- D poitional diplacement wa added to each path element. Thee reult are hown in Fig. 3. Data falling on the olid loping line ugget that the incremental poitional uncertainty of the dominant and fellow amblyopic eye i imilar, data falling below thi line ugget that the incremental poitional uncertainty of the anablyopic eye i depreed. In all but one cae (CA), the incremental poitional uncertainty wa equal in dominant and fellow amblyopic eye. For CA, the amblyopic eye (olid ymbol) diplayed a mall (le than a factor of 2) but ignificant lo in incremental poitional uncertainty. In order to take thi into account in our interpretation of the aociated anomalou contour integration (Fig. 2), we meaured in a eparate experiment uing the fellow dominant eye, the pedetal of poitional uncertainty aociated with thi level of incremental uncertainty (ee Method) in the amblyopic eye. Thi we took to be the raied level of internal uncertainty in the amblyopic eye reponible for the previouly meaured lo of incremental uncertainty (ee Method and He et al., 1997 for a more detailed dicuion). Uing the dominant eye, we then re-meaured performance on the contour integration tak with each path element now having thi degree of poitional uncertainty. From thi we hoped to deduce the extent to which the non-zero pedetal of internal poitional uncertainty exhibited by thi amblyope could account for the reduced performance hown previouly in Fig. 2 for contour integration. The hourgla ymbol in Fig. 2 repreent performance of the fellow dominant eye for a level of timulu uncertainty correponding to that 10 c- "~ 8- T~ 0 iij._j < 6- Z _o I-- 0 u.i 4- >- IJ.I I--- z < z ~ 2-0 c3 $ --t 0 - P I I I I I /3 10 AMBLYOPIC EYE POITIONAL ERROR (rain) FIGURE 3. Comparion of the poitional uncertaintie of dominant and fellow amblyopic eye of the ix aniometropic amblyope at two repreentative path angle. The loping line i the prediction for equivalent poitional uncertainty in each eye. Error bar repreent 67% confidence limit.

6 894 R.F. HE and R. DEMANIN of the amblyopic eye. ince thee reult for the dominant eye (hourgla) are not comparable with the previou anomalou contour integration performance of the amblyopic eye (filled ymbol), we conclude that contour integration per e i abnormal in thi ubject. trabimic amblyope exhibit ignificant level of poitional uncertainty for their amblyopic eye (Levi & Klein, 1982, 1985, 1990; He & Holliday, 1992; Demanin & He, 1996) which ha been attributed to a diarray in the topological cortical map (He et al., 1978: He & Field, 1994; but alo ee Levi & Klein, 1986). It ha been hown previouly that when thi elevated level of poitional uncertainty i taken into account, their performance on thi particular contour integration tak i normal (He et al., 1997 but alo ee Kov~ic, Polat & Norcia, 1996), Thi ugget that the integration proce (e.g., the lateral connection) in the amblyopic eye may be equivalent to the dominant eye but becaue the connection in the amblyopic eye are between the inappropriately poitioned cell (i.e., the neural diarray), the reult i a perceived ditortion which in turn make the path more difficult to detect. Aniometropic amblyope, on the other hand, are known to exhibit either normal or only marginally anomalou level of poitional uncertainty for their amblyopic eye for equi-viible timuli (He & Holliday, 1992). According to the above reaoning, one would expect contour integration to be normal. The preent reult bear out thi expectation for 5 of our 6 aniometrope. Field, D. J., Haye, A. & He, R. F. (1993). Contour integration by the human viual ytem: evidence for a local "aociation field". Viion Reearch, 33, He, R. F., Campbell, F. W. & Greenhalgh, T. (1978). On the nature of the neural abnormality in human amblyopia: neural aberration and neural enitivity lo. PflUger Archiv, J~tr die geamte Phyiologie, 377, He, R. F. & Field, D. J. (1994). I the patial deficit in trabimic amblyopia due to lo of cell or an uncalibrated diarray of cell?. Viion Reearch, 34, He, R. F., Field, D. J. & Watt, R. J. (1990). The puzzle of amblyopia. In C. Blakemore (Ed.), Viion coding and efficiency, Chap. 25, pp Cambridge: Cambridge Univerity Pre. He, R. F. & Holliday, I. E. (1992). The patial localization deficit in amblyopia. Viion Reearch, 32, He, R. F., Mcllhagga, W. & Field, D. J. (1997). Contour integration in trabimic amblyopia: the ufficiency of an explanation baed on poitional uncertainty. Viion Reearch, 37, He, R. F. & Watt, R. J. (1990). Regional ditribution of the mechanim that underlie patial localization. Viion Reearch, 30, Kovfic, 1., Polat, U. & Norcia, A. M. (1996). Breakdown in binding mechanim in amblyopia. Invetigative Ophthahnology and Viual cience (upplement 670). Levi, D. M. & Klein,. A. (1982). Hyperacuity and amblyopia. Nature. 298, Levi, D. M. & Klein,. A. (1985). Vernier acuity, crowding and amblyopia. Viion Reearch, 25, Levi, D. M. & Klein,. A. (1986). ampling in patial viion. Nature, 320, Levi, D. M. & Klein,. A. (1990). Equivalent intrinic blur in amblyopia. Viion Reearch, 30, Watt, R. J. & He, R. F. (1987). patial information and uncertainty in aniometropic amblyopia. Viion Reearch, 27, REFERENCE Demanin, R. & He, R. F. (1996). Poitional lo in trabimic amblyopia: inter-relationhip of alignment threhold, bia, patial cale and eccentricity. Viion Reearch, 36, Acknowledgement--Thi work wa upported by a grant (#MT ) from the Medical Reearch Council of Canada to RFH and an MRC of Canada fellowhip to RD. We are very grateful to Dr W E Connolly and R Polomeno for referral.

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