Grasping deficits and adaptations in adults with stereo vision losses.

PURPOSE To examine the effects of permanent versus brief reductions in binocular stereo vision on reaching and grasping (prehension) skills. METHODS The first experiment compared prehension proficiency in 20 normal and 20 adults with long-term stereo-deficiency (10 with coarse and 10 with undetectable disparity sensitivities) when using binocular vision or just the dominant or nondominant eye. The second experiment examined effects of temporarily mimicking similar stereoacuity losses in normal adults, by placing defocusing low- or high-plus lenses over one eye, compared with their control (neutral lens) binocular performance. Kinematic and error measures of prehension planning and execution were quantified from movements of the subjects' preferred hand recorded while they reached, precision-grasped, and lifted cylindrical objects (two sizes, four locations) on 40 to 48 trials under each viewing condition. RESULTS Performance was faster and more accurate with normal compared with reduced binocular vision and least accomplished under monocular conditions. Movement durations were extended (up to approximately 100 ms) whenever normal stereo vision was permanently (ANOVA P < 0.05) or briefly (ANOVA P < 0.001) reduced, with a doubling of error rates in executing the grasp (ANOVA P < 0.001). Binocular deficits in reaching occurred during its end phase (prolonged final approach, more velocity corrections, poorer coordination with object contact) and generally increased with the existing loss of disparity sensitivity. Binocular grasping was more uniformly impaired by stereoacuity loss and influenced by its duration. Adults with long-term stereo-deficiency showed increased variability in digit placement at initial object contact, and they adapted by prolonging (by approximately 25%) the time spent subsequently applying their grasp (ANOVA P < 0.001). Brief stereoreductions caused systematic shifts in initial digit placement and two to three times more postcontact adjustments in grip position (ANOVA P < 0.01). CONCLUSIONS High-grade binocular stereo vision is essential for skilled precision grasping. Reduced disparity sensitivity results in inaccurate grasp-point selection and greater reliance on nonvisual (somesthetic) information from object contact to control grip stability.

[1]  C. Wheatstone.  XVIII. Contributions to the physiology of vision. —Part the first. On some remarkable, and hitherto unobserved, phenomena of binocular vision , 1962, Philosophical Transactions of the Royal Society of London.

[2]  Charles Wheatstone.  On some remarkable and hitherto unobserved phenomena of binocular vision. , 1962 .

[3]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[4]  G. K. Noorden,et al.  Binocular vision and ocular motility;: Theory and management of strabismus , 1974 .

[5]  R K Jones,et al.  Why two eyes are better than one: the two views of binocular vision. , 1981, Journal of experimental psychology. Human perception and performance.

[6]  THE RELATIONSHIP BETWEEN CLINICAL STEREOTESTS , 1982, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[7]  A. Wing,et al.  The Contribution of the Thumb to Reaching Movements , 1983, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[8]  Michael J. Morgan,et al.  Vision of solid objects , 1989, Nature.

[9]  B. Rogers,et al.  Disparity curvature and the perception of three-dimensional surfaces , 1989, Nature.

[10]  C. MacKenzie,et al.  The effects of object weight on the kinematics of prehension. , 1991, Journal of motor behavior.

[11]  E. Johnston.  Systematic distortions of shape from stereopsis , 1991, Vision Research.

[12]  Melvyn A. Goodale,et al.  The role of binocular vision in prehension: a kinematic analysis , 1992, Vision Research.

[13]  M. J. Morgan,et al.  Stereoscopic depth perception at high velocities , 1995, Nature.

[14]  F. A. Miles.  Binocular Vision and Stereopsis by Ian P. Howard and Brian J. Rogers, Oxford University Press, 1995. £90.00 (736 pages) ISBN 0 19 508476 4. , 1996, Trends in Neurosciences.

[15]  M. Moseley,et al.  Does stereopsis matter in humans? , 1996, Eye.

[16]  H. Sakata,et al.  The TINS Lecture The parietal association cortex in depth perception and visual control of hand action , 1997, Trends in Neurosciences.

[17]  M. A. Goodale,et al.  The removal of binocular cues disrupts the calibration of grasping in patients with visual form agnosia , 1997, Experimental Brain Research.

[18]  Hc. Dijkertnan.  The perception and prehension of objects oriented in the depth plane. I. Effects of visual form agnosia , 1997 .

[19]  N W Daw,et al.  Critical periods and amblyopia. , 1998, Archives of ophthalmology.

[20]  Mark Nawrot,et al.  Abnormal depth perception from motion parallax in amblyopic observers , 1999, Vision Research.

[21]  Lynne Kiorpes,et al.  Neural mechanisms underlying amblyopia , 1999, Current Opinion in Neurobiology.

[22]  M. Lenoir,et al.  Ecological Relevance of Stereopsis in One-Handed Ball-Catching , 1999, Perceptual and motor skills.

[23]  M. Mon-Williams,et al.  The use of vergence information in the programming of prehension , 1999, Experimental Brain Research.

[24]  M. Mon-Williams,et al.  Vertical gaze angle: absolute height-in-scene information for the programming of prehension , 2001, Experimental Brain Research.

[25]  Simon J Watt,et al.  Binocular cues are important in controlling the grasp but not the reach in natural prehension movements , 2000, Neuropsychologia.

[26]  M. A. Goodale,et al.  The Role of Familiar Size in the Control of Grasping , 2001, Journal of Cognitive Neuroscience.

[27]  J. Shimko.  Binocular Vision and Ocular Motility Theory and Management of Strabismus , 2001, The American orthoptic journal.

[28]  G P Bingham,et al.  Accommodation, occlusion, and disparity matching are used to guide reaching: a comparison of actual versus virtual environments. , 2001, Journal of experimental psychology. Human perception and performance.

[29]  Simon J Watt,et al.  The visual control of reaching and grasping: binocular disparity and motion parallax. , 2003, Journal of experimental psychology. Human perception and performance.

[30]  Alison R. Davis,et al.  Electrophysiological and psychophysical differences between early- and late-onset strabismic amblyopia. , 2003, Investigative Ophthalmology and Visual Science.

[31]  E. Birch,et al.  Validity of the Titmus and Randot circles tasks in children with known binocular vision disorders. , 2003, Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus.

[32]  R. Johansson,et al.  Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip , 2004, Experimental Brain Research.

[33]  M. Mon-Williams,et al.  When two eyes are better than one in prehension: monocular viewing and end-point variance , 2004, Experimental Brain Research.

[34]  D. Knill,et al.  Visuomotor sensitivity to visual information about surface orientation. , 2004, Journal of neurophysiology.

[35]  A. Milner,et al.  The perception and prehension of objects oriented in the depth plane , 1996, Experimental Brain Research.

[36]  Gilles Montagne,et al.  The contribution of stereo vision to one-handed catching , 2004, Experimental Brain Research.

[37]  Paul B Hibbard,et al.  Binocular cues and the control of prehension. , 2004, Spatial vision.

[38]  Simon Grant,et al.  Advantages of binocular vision for the control of reaching and grasping , 2006, Experimental Brain Research.

[39]  J. Lang.  Anomalous retinal correspondence update , 2005, Graefe's Archive for Clinical and Experimental Ophthalmology.

[40]  David C. Knill,et al.  Integrating visual cues for motor control: A matter of time , 2005, Vision Research.

[41]  Simon Grant,et al.  Dissociation between vergence and binocular disparity cues in the control of prehension , 2007, Experimental Brain Research.

[42]  Paul R. Schrater,et al.  Effects of visual uncertainty on grasping movements , 2007, Experimental Brain Research.

[43]  Simon Grant,et al.  Prehension deficits in amblyopia. , 2007, Investigative ophthalmology & visual science.

[44]  A. Parker.  Binocular depth perception and the cerebral cortex , 2007, Nature Reviews Neuroscience.

[45]  Megan L. Frankl,et al.  Concordant eye movement and motion parallax asymmetries in esotropia , 2008, Vision Research.

[46]  Z. Kourtzi,et al.  Multivoxel Pattern Selectivity for Perceptually Relevant Binocular Disparities in the Human Brain , 2008, The Journal of Neuroscience.

[47]  Umberto Castiello,et al.  The Cortical Control of Visually Guided Grasping , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[48]  Ivan Toni,et al.  Perceptuo-Motor Interactions during Prehension Movements , 2008, The Journal of Neuroscience.