Recovery of stereopsis through perceptual learning in PNAS PLUS human adults with abnormal binocular vision

Jian Dinga,b,1 and Dennis M. Levia,b aSchool of Optometry and bThe Helen Wills Neuroscience Institute, University of California, Berkeley, CA 94720 AUTHOR SUMMARY

Stereopsis, the perception of therefore, the monocular and depth based on the binocular binocular cues are consistent disparity of the images projected and reinforce each other in the to the retinas of the two eyes, perception of depth (4). adds richness to our perception Stereo training began by first of our 3D world. However, 3– establishing binocular fusion 5% of the population is stereo- and alignment—through which blind and is unable to use bin- the brain sees a single, unified ocular disparity to perceive image for both eyes—by re- depth or has a condition called ducing the contrast of the DE’s “stereoanomaly” that results in frame (Fig. P1A, Left) until both seriously impaired stereovision. frames were visible through Stereoblindness and stereo- a stereoscope (Fig. P1A, Left anomaly often result from and Center) and adjusting the a “turned eye” or “lazy eye” vertical and horizontal positions during early childhood. If not of the two frames separately.

treated early enough, these Once fusion and alignment were COGNITIVE SCIENCES PSYCHOLOGICAL AND conditions could lead to reduced achieved (Fig. P1A, Right), two or no stereopsis. Although pairs of vertical gratings (Fig. treatment is seldom undertaken P1B, Left and Center) were pre- Fig. P1. Stimuli. (A) Each training trial began with frames that assist in adults, we show here that fi sented to the two eyes stereo- — an observer with fusing images from two eyes into a single uni ed ’ perceptual learning the re- image in the brain. (B) Once fusion was achieved, vertically aligned scopically. The observer s task petitive practice of a demanding target gratings (Upper) and reference gratings (Lower) were presented was to indicate the relative visual task—can induce the re- to the two eyes stereoscopically until a response was given. RE, right depth of the top grating (i.e., covery of stereopsis in adults eye; LE, left eye. whether it was closer or farther with abnormal binocular vision. away than the bottom grating) Under everyday viewing con- (Fig. P1B, Right). For training, ditions, individuals with abnormal binocular vision typically feedback was provided after each trial, and the stimuli contained view the world through their dominant eye (DE); signals from monocular position cues that were correlated perfectly with the other eye, the nondominant eye (NDE), are suppressed binocular disparity cues. To rule out monocular artifacts and strongly in the brain. In the laboratory, however, it is possible to ensure that our observers achieved stereopsis, we applied stereo present separate images to each eye through a stereoscope (Fig. tests with stimuli that contained no monocular cues (pure dis- P1A). By reducing the contrast of the DE’sframe(Fig.P1A, parity test) before and after training. Left) and carefully aligning the images, it is possible for an After more than 10,000 trials of training, observers with ab- abnormal observer to perceive both eyes’ images simulta- normal binocular vision improved their stereo performance neously (Fig. P1A, Right). In the present study we used a ste- substantially and significantly. Indeed, three observers who were reoscope to aid eye alignment and perceptual learning to train stereoblind before training achieved measurable stereopsis stereopsis in five adults who were stereoblind or stereo- through stereo training. The training effect was very limited for anomalous. Recent studies suggest that perceptual learning normal observers with comparable training. may provide an important method for recovery of vision in Before training, all stereoblind observers failed the clinical adults with lazy eye (1). In a few instances, improvement of stereo test (>400 arc seconds); however, after training, they stereopsis appears to be a side benefitofimprovingmonocular displayed stereoacuities of 40–140 arc seconds on this test. Some vision through perceptual learning in juveniles with lazy eye (2). consider the appreciation of depth in random dot stereograms Recently, Nakatsuka et al. (3) reported that adult monkeys with to be the gold standard for stereopsis, because the stereograms mild stereo deficiencies (i.e., that required a larger depth cue contain no monocular information that might be used in depth than normal) improved their stereoacuity—the ability to detect perception. We developed a psychophysical stereo test with the smallest depths—through perceptual learning. However, high-contrast dynamic random-dot stereograms (DRS) that perceptual learning has not been applied directly to the treat- ment of stereoblindness in human observers. The purpose of the present study was to test whether the recovery of stereopsis Author contributions: J.D. and D.M.L. designed research; J.D. performed research; J.D. can be induced through perceptual learning in human observers analyzed data; and J.D. and D.M.L. wrote the paper. who have suffered long-standing stereoblindness, and, if so, The authors declare no conflict of interest. what the nature of the recovered stereopsis is. To induce ste- This article is a PNAS Direct Submission. reopsis, we used a perceptual learning paradigm that combined 1To whom correspondence should be addressed. E-mail: [email protected]. monocular cues—the relative positions of images in one eye— See full research article on page E733 of www.pnas.org. that were correlated perfectly with the binocular disparity cues; Cite this Author Summary as: PNAS 10.1073/pnas.1105183108.

www.pnas.org/cgi/doi/10.1073/pnas.1105183108 PNAS | September 13, 2011 | vol. 108 | no. 37 | 15035–15036 Downloaded by guest on September 26, 2021 eliminate any possible monocular cues. With the exception of tual learning may provide a useful method for treating stereo- one abnormal observer, all observers were able to detect depth in blindness and stereoanomalies and that the recovered our DRS test. A demonstration DRS is available online in stereopsis may improve the quality of life in persons with Supporting Information. We also examined the properties of the stereo deficiencies. recovered stereopsis and found that it has reduced resolution and precision relative to normal, although it is based on per- 1. Levi DM, Li RW (2009) Perceptual learning as a potential treatment for amblyopia: A ceiving depth by detecting binocular disparity. mini-review. Vision Res 49:2535–2549. Stereoblind or stereodeficient individuals who recover ste- 2. Li RW, Provost A, Levi DM (2007) Extended perceptual learning results in substantial reopsis may gain substantial benefitineverydaylife(5).After recovery of positional acuity and visual acuity in juvenile amblyopia. Invest Ophthalmol achieving stereopsis, our observers reported that depth “pop- Vis Sci 48:5046–5051. ped out” in daily life. They feel more confident in daily tasks 3. Nakatsuka C, et al. (2007) Effects of perceptual learning on local stereopsis and neuronal – that are related to depth perception and are able, for the responses of V1 and V2 in prism-reared monkeys. J Neurophysiol 97:2612 2626. fi 4. Wilcox LM, Harris JM, McKee SP (2007) The role of binocular stereopsis in monoptic rst time, to enjoy 3D movies. Here we have documented the depth perception. Vision Res 47:2367–2377. recovery of stereopsis in human adults with abnormal binocular 5. Barry SR (2009) Fixing My Gaze: A Scientist’s Journey into Seeing in Three Dimensions vision through perceptual learning. We conclude that percep- (Basic Books, New York).

15036 | www.pnas.org/cgi/doi/10.1073/pnas.1105183108 Ding and Levi Downloaded by guest on September 26, 2021