Literature DB >> 30733219

Binocular Eye Movements Are Adapted to the Natural Environment.

Agostino Gibaldi1, Martin S Banks2.   

Abstract

Humans and many animals make frequent saccades requiring coordinated movements of the eyes. When landing on the new fixation point, the eyes must converge accurately or double images will be perceived. We asked whether the visual system uses statistical regularities in the natural environment to aid eye alignment at the end of saccades. We measured the distribution of naturally occurring disparities in different parts of the visual field. The central tendency of the distributions was crossed (nearer than fixation) in the lower field and uncrossed (farther) in the upper field in male and female participants. It was uncrossed in the left and right fields. We also measured horizontal vergence after completion of vertical, horizontal, and oblique saccades. When the eyes first landed near the eccentric target, vergence was quite consistent with the natural-disparity distribution. For example, when making an upward saccade, the eyes diverged to be aligned with the most probable uncrossed disparity in that part of the visual field. Likewise, when making a downward saccade, the eyes converged to enable alignment with crossed disparity in that part of the field. Our results show that rapid binocular eye movements are adapted to the statistics of the 3D environment, minimizing the need for large corrective vergence movements at the end of saccades. The results are relevant to the debate about whether eye movements are derived from separate saccadic and vergence neural commands that control both eyes or from separate monocular commands that control the eyes independently.SIGNIFICANCE STATEMENT We show that the human visual system incorporates statistical regularities in the visual environment to enable efficient binocular eye movements. We define the oculomotor horopter: the surface of 3D positions to which the eyes initially move when stimulated by eccentric targets. The observed movements maximize the probability of accurate fixation as the eyes move from one position to another. This is the first study to show quantitatively that binocular eye movements conform to 3D scene statistics, thereby enabling efficient processing. The results provide greater insight into the neural mechanisms underlying the planning and execution of saccadic eye movements.
Copyright © 2019 the authors.

Entities:  

Keywords:  binocular vision; eye movements; horopter; statistics of natural disparity

Mesh:

Year:  2019        PMID: 30733219      PMCID: PMC6462454          DOI: 10.1523/JNEUROSCI.2591-18.2018

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  48 in total

1.  Dynamics of horizontal vergence movements: interaction with horizontal and vertical saccades and relation with monocular preferences.

Authors:  A F van Leeuwen; H Collewijn; C J Erkelens
Journal:  Vision Res       Date:  1998-12       Impact factor: 1.886

2.  An area for vergence eye movement in primate frontal cortex.

Authors:  P D Gamlin; K Yoon
Journal:  Nature       Date:  2000-10-26       Impact factor: 49.962

3.  Are corresponding points fixed?

Authors:  J M Hillis; M S Banks
Journal:  Vision Res       Date:  2001-09       Impact factor: 1.886

4.  Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding.

Authors:  A Takemura; Y Inoue; K Kawano; C Quaia; F A Miles
Journal:  J Neurophysiol       Date:  2001-05       Impact factor: 2.714

5.  The backward inclination of a surface defined by empirical corresponding points.

Authors:  P M Grove; H Kaneko; H Ono
Journal:  Perception       Date:  2001       Impact factor: 1.490

6.  Neural mechanisms for the control of vergence eye movements.

Authors:  Paul D R Gamlin
Journal:  Ann N Y Acad Sci       Date:  2002-04       Impact factor: 5.691

7.  Stereopsis, cyclovergence and the backwards tilt of the vertical horopter.

Authors:  J Siderov; R S Harwerth; H E Bedell
Journal:  Vision Res       Date:  1999-04       Impact factor: 1.886

8.  The Eyelink Toolbox: eye tracking with MATLAB and the Psychophysics Toolbox.

Authors:  Frans W Cornelissen; Enno M Peters; John Palmer
Journal:  Behav Res Methods Instrum Comput       Date:  2002-11

9.  Slow saccades in spinocerebellar degeneration.

Authors:  D S Zee; L M Optican; J D Cook; D A Robinson; W K Engel
Journal:  Arch Neurol       Date:  1976-04

10.  Comparison of the time courses of concomitant and nonconcomitant vertical phoria adaptation.

Authors:  Erich W Graf; James S Maxwell; Clifton M Schor
Journal:  Vision Res       Date:  2003-03       Impact factor: 1.886

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  12 in total

1.  A Geometric Theory Integrating Human Binocular Vision With Eye Movement.

Authors:  Jacek Turski
Journal:  Front Neurosci       Date:  2020-12-07       Impact factor: 4.677

2.  Crossed-uncrossed projections from primate retina are adapted to disparities of natural scenes.

Authors:  Agostino Gibaldi; Noah C Benson; Martin S Banks
Journal:  Proc Natl Acad Sci U S A       Date:  2021-02-16       Impact factor: 11.205

3.  Mice Discriminate Stereoscopic Surfaces Without Fixating in Depth.

Authors:  Jason M Samonds; Veronica Choi; Nicholas J Priebe
Journal:  J Neurosci       Date:  2019-08-28       Impact factor: 6.167

4.  Neural control of rapid binocular eye movements: Saccade-vergence burst neurons.

Authors:  Julie Quinet; Kevin Schultz; Paul J May; Paul D Gamlin
Journal:  Proc Natl Acad Sci U S A       Date:  2020-11-02       Impact factor: 11.205

5.  Optimal Stereoacuity Reveals More Than Critical Time in Patients With Intermittent Exotropia.

Authors:  Haoran Wu; Xiaoning Li; Yao Tang; Qinglin Xu; Xuhong Zhang; Lu Zhou; Weizhong Lan; Bin Zhang; Zhikuan Yang
Journal:  Front Neurosci       Date:  2020-02-18       Impact factor: 4.677

6.  Near-optimal combination of disparity across a log-polar scaled visual field.

Authors:  Guido Maiello; Manuela Chessa; Peter J Bex; Fabio Solari
Journal:  PLoS Comput Biol       Date:  2020-04-10       Impact factor: 4.475

7.  Natural scene statistics predict how humans pool information across space in surface tilt estimation.

Authors:  Seha Kim; Johannes Burge
Journal:  PLoS Comput Biol       Date:  2020-06-24       Impact factor: 4.475

8.  The blur horopter: Retinal conjugate surface in binocular viewing.

Authors:  Agostino Gibaldi; Vivek Labhishetty; Larry N Thibos; Martin S Banks
Journal:  J Vis       Date:  2021-03-01       Impact factor: 2.240

9.  Binocular vision and the control of foot placement during walking in natural terrain.

Authors:  Kathryn Bonnen; Jonathan S Matthis; Agostino Gibaldi; Martin S Banks; Dennis M Levi; Mary Hayhoe
Journal:  Sci Rep       Date:  2021-10-22       Impact factor: 4.379

10.  A dichoptic feedback-based oculomotor training method to manipulate interocular alignment.

Authors:  Andrea Caoli; Silvio P Sabatini; Agostino Gibaldi; Guido Maiello; Anna Kosovicheva; Peter Bex
Journal:  Sci Rep       Date:  2020-09-24       Impact factor: 4.379

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