The Best of Both Worlds: Adaptation During Natural Tasks Produces Long-Lasting Plasticity in Perceptual Ocular Dominance

Abstract

In human vision, one eye is usually stronger than the other. This is called ocular dominance. Extremely imbalanced ocular dominance can be found among certain patient groups, for example, in patients with amblyopia. Here, we introduce a novel method to rebalance ocular dominance. We developed an altered-reality system that subjects used to interact with the natural world, the appearance of which was changed through a real-time image process. Several daily adaptation sessions lasting 3 hr each reduced sensory ocular dominance in adults who were not diagnosed with amblyopia and improved vision in patients with amblyopia. Surprising additional strengthening was found over the subsequent 2 months, when subjects experienced natural vision only. Our method effectively trains subjects to use both eyes in the wide variety of everyday tasks. The transfer of this training to everyday vision likely produced the continuing growth in effects during the months after the training. These findings are promising for the application of this method in future clinical research on amblyopia.

Keywords

ocular dominance plasticity adaptation patchwork binocular rivalry

Get full access to this article

View all access options for this article.

References

Bach

(1996). The Freiburg Visual Acuity test—automatic measurement of visual acuity. Optometry and Vision Science, 73, 49–53.

Bai

Dong

Bao

(2017). Monocular deprivation of Fourier phase information boosts the deprived eye’s dominance during interocular competition but not interocular phase combination. Neuroscience, 352, 122–130.

Bao

Engel

S. A.

(2012). Distinct mechanism for long-term contrast adaptation. Proceedings of the National Academy of Sciences, USA, 109, 5898–5903.

Bao

Fast

Mesik

Engel

(2013). Distinct mechanisms control contrast adaptation over different timescales. Journal of Vision, 13(10), Article 14. doi:10.1167/13.10.14

Blake

(1989). A neural theory of binocular rivalry. Psychological Review, 96, 145–167.

Brainard

D. H.

(1997). The Psychophysics Toolbox. Spatial Vision, 10, 433–436.

Carbon

C. C.

Ditye

(2011). Sustained effects of adaptation on the perception of familiar faces. Journal of Experimental Psychology: Human Perception and Performance, 37, 615–625.

Cohen

(1992). A power primer. Psychological Bulletin, 112, 155–159.

Greifzu

Pielecka-Fortuna

Kalogeraki

Krempler

Favaro

P. D.

Schluter

O. M.

Siegrid

(2014). Environmental enrichment extends ocular dominance plasticity into adulthood and protects from stroke-induced impairments of plasticity. Proceedings of the National Academy of Sciences, USA, 111, 1150–1155.

10.

H. Y.

Ray

Dennis

Quinlan

E. M.

(2007). Experience-dependent recovery of vision following chronic deprivation amblyopia. Nature Neuroscience, 10, 1134–1136.

11.

Hess

R. F.

Mansouri

Thompson

(2010). A new binocular approach to the treatment of amblyopia in adults well beyond the critical period of visual development. Restorative Neurology and Neuroscience, 28, 793–802.

12.

Hess

R. F.

Thompson

(2015). Amblyopia and the binocular approach to its therapy. Vision Research, 114, 4–16.

13.

Holmes

J. M.

Lazar

E. L.

Melia

B. M.

Astle

W. F.

Dagi

L. R.

Donahue

S. P.

, . . . Pediatric Eye Disease Investigator Group. (2011). Effect of age on response to amblyopia treatment in children. Archives of Ophthalmology, 129, 1451–1457.

14.

Hubel

D. H.

Wiesel

T. N.

(1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. The Journal of Physiology, 206, 419–436.

15.

Jones

P. D.

Holding

D. H.

(1975). Extremely long-term persistence of the McCollough effect. Journal of Experimental Psychology: Human Perception and Performance, 1, 323–327.

16.

Karni

Sagi

(1993). The time course of learning a visual skill. Nature, 365, 250–252.

17.

Klink

P. C.

Brascamp

J. W.

Blake

van Wezel

R. J.

(2010). Experience-driven plasticity in binocular vision. Current Biology, 20, 1464–1469.

18.

Kovacs

Papathomas

T. V.

Yang

Feher

(1996). When the brain changes its mind: Interocular grouping during binocular rivalry. Proceedings of the National Academy of Sciences, USA, 93, 15508–15511.

19.

Levi

D. M.

R. W.

(2009). Perceptual learning as a potential treatment for amblyopia: A mini-review. Vision Research, 49, 2535–2549.

20.

Levi

D. M.

Polat

(1996). Neural plasticity in adults with amblyopia. Proceedings of the National Academy of Sciences, USA, 93, 6830–6834.

21.

Thompson

Deng

Chan

L. Y.

Hess

R. F.

(2013). Dichoptic training enables the adult amblyopic brain to learn. Current Biology, 23, R308–R309.

22.

R. W.

Ngo

Nguyen

Levi

D. M.

(2011). Video-game play induces plasticity in the visual system of adults with amblyopia. PLOS Biology, 9(8), Article e1001135. doi:10.1371/journal.pbio.1001135

23.

S. L.

Reynaud

Hess

R. F.

Wang

Y.-Z.

Jost

R. M.

Morale

S. E.

, . . . Birch

(2015). Dichoptic movie viewing treats childhood amblyopia. Journal of the American Association for Pediatric Ophthalmology and Strabismus, 19, 401–405.

24.

Lunghi

Burr

D. C.

Morrone

(2011). Brief periods of monocular deprivation disrupt ocular balance in human adult visual cortex. Current Biology, 21, R538–R539.

25.

Lunghi

Burr

D. C.

Morrone

M. C.

(2013). Long-term effects of monocular deprivation revealed with binocular rivalry gratings modulated in luminance and in color. Journal of Vision, 13(6), Article 1. doi:10.1167/13.6.1

26.

Lunghi

Emir

U. E.

Morrone

M. C.

Bridge

(2015). Short-term monocular deprivation alters GABA in the adult human visual cortex. Current Biology, 25, 1496–1501.

27.

Lunghi

Sale

(2015). A cycling lane for brain rewiring. Current Biology, 25, R1122–R1123.

28.

Maya Vetencourt

J. F.

Sale

Viegi

Baroncelli

De Pasquale

O’Leary

O. F.

, . . . Maffei

(2008). The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science, 320, 385–388.

29.

Mei

Dong

Bao

(2015). Spontaneous recovery of effects of contrast adaptation without awareness. Frontiers in Psychology, 6, Article 1464. doi:10.3389/fpsyg.2015.01464

30.

Ooi

T. L.

Y. R.

Natale

D. M.

Z. J.

(2013). A push-pull treatment for strengthening the ‘lazy eye’ in amblyopia. Current Biology, 23, R309–R310.

31.

Polat

Ma-Naim

Belkin

Sagi

(2004). Improving vision in adult amblyopia by perceptual learning. Proceedings of the National Academy of Sciences, USA, 101, 6692–6697.

32.

Sagi

(2011). Perceptual learning in vision research. Vision Research, 51, 1552–1566.

33.

Sale

Maya Vetencourt

J. F.

Medini

Cenni

M. C.

Baroncelli

De Pasquale

Maffei

(2007). Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nature Neuroscience, 10, 679–681.

34.

Spiegel

D. P.

Hess

R. F.

Byblow

W. D.

Deng

Thompson

(2013). Transcranial direct current stimulation enhances recovery of stereopsis in adults with amblyopia. Neurotherapeutics, 10, 831–839.

35.

Thompson

Mansouri

Koski

Hess

R. F.

(2008). Brain plasticity in the adult: Modulation of function in amblyopia with rTMS. Current Biology, 18, 1067–1071.

36.

Tibber

M. S.

Anderson

E. J.

Bobin

Antonova

Seabright

Wright

. . .Dakin

S. C.

(2013). Visual surround suppression in schizophrenia. Frontiers in Psychology, 4, Article 88. doi:10.3389/fpsyg.2013.00088

37.

Vedamurthy

Nahum

Huang

S. J.

Zheng

Bayliss

Bavelier

Levi

D. M.

(2015). A dichoptic custom-made action video game as a treatment for adult amblyopia. Vision Research, 114, 173–187.

38.

Wiesel

T. N.

Hubel

D. H.

(1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology, 26, 1003–1017.

39.

J. P.

Z. J.

Ooi

T. L.

(2010). Effectively reducing sensory eye dominance with a push-pull perceptual learning protocol. Current Biology, 20, 1864–1868.

40.

Yoon

J. H.

Maddock

R. J.

Rokem

Silver

M. A.

Minzenberg

M. J.

Ragland

J. D.

Carter

C. S.

(2010). GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression. The Journal of Neuroscience, 30, 3777–3781.

41.

Zhang

Bao

Kwon

Engel

S. A.

(2009). Effects of orientation-specific visual deprivation induced with altered reality. Current Biology, 19, 1956–1960.

42.

Zhou

Thompson

Hess

R. F.

(2013). A new form of rapid binocular plasticity in adult with amblyopia. Scientific Reports, 3, Article 2638. doi:10.1038/srep02638

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

1.52 MB