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Dissociation between vergence and binocular disparity cues in the control of prehension

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Abstract

Binocular vision provides important advantages for controlling reach-to-grasp movements. We examined the possible source(s) of these advantages by comparing prehension proficiency under four different binocular viewing conditions, created by randomly placing a neutral lens (control), an eight dioptre prism (Base In or Base Out) or a low-power (2.00–3.75 dioptre) Plus lens over the eye opposite the moving limb. The Base In versus Base Out prisms were intended to selectively alter vergence-specified distance (VSD) information, such that the targets appeared beyond or closer than their actual physical position, respectively. The Plus lens was individually tailored to reduce each subject’s disparity sensitivity (to 400–800 arc s), while minimizing effects on distance estimation. In pre-testing, subjects pointed (without visual feedback) to mid-line targets at different distances, and produced the systematic directional errors expected of uncorrected movements programmed under each of the perturbed conditions. For the prehension tasks, subjects reached and precision grasped (with visual feedback available) cylindrical objects (two sizes and three locations), either following a 3 s preview in which to plan their actions or immediately after the object became visible. Viewing condition markedly affected performance, but the planning time allowed did not. Participants made the most errors suggesting premature collision with the object (shortest ‘braking’ times after peak deceleration; fastest velocity and widest grip at initial contact) under Base In prism viewing, consistent with over-reaching movements programmed to transport the hand beyond the actual target due to its ‘further’ VSD. Conversely, they produced the longest terminal reaches and grip closure times, with multiple corrections just before and after object contact, under the Plus lens (reduced disparity) condition. Base Out prism performance was intermediate between these two, with significant increases in additional forward movements during the transport end-phase, indicative of initial under-reaching in response to the target’s ‘nearer’ VSD. Our findings suggest dissociations between the role of vergence and binocular disparity in natural prehension movements, with vergence contributing mainly to reach planning and high-grade disparity cues providing particular advantages for grasp-point selection during grip programming and application.

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References

  • Berthier NE, Clifton RK, Gullapalli V, McCall DD, Robin DJ (1996) Visual information and object size in the control of reaching. J Mot Behav 28:187–197

    Article  PubMed  Google Scholar 

  • Blakemore C, Hague B (1972) Evidence for disparity detecting neurons in the human visual system. J Physiol (Lond) 225:437–455

    CAS  Google Scholar 

  • Bingham GP (2005) Calibration of distance and size does not calibrate shape information: comparison of dynamic monocular and static and dynamic binocular vision. Ecol Psychol 17:55–74

    Article  Google Scholar 

  • Bingham GP, Bradley A, Bailey M, Vinner R (2001) Accommodation, occlusion, and disparity matching are used to guide reaching: a comparison of actual versus virtual environments. J Exp Psychol Hum Percept Perform 27:1314–1334

    Article  PubMed  CAS  Google Scholar 

  • Bishop PO (1989) Vertical disparity, egocentric distance and stereoscopic depth constancy: a new interpretation. Proc R Soc London Biol 237:445–469

    Article  CAS  Google Scholar 

  • Bradshaw MF, Elliot KM (2003) The role of binocular information in the ‘on-line’ control of prehension. Spat Vis 16:295–309

    Article  PubMed  Google Scholar 

  • Bradshaw MF, Parton AD, Glennerster A (2000) The task-dependent use of binocular disparity and motion parallax information. Vision Res 40:3725–3734

    Article  PubMed  CAS  Google Scholar 

  • Bradshaw MF, Elliot KM, Watt SJ, Hibbard PB, Davies IR, Simpson PJ (2004) Binocular cues and the control of prehension. Spat Vis 17:95–110

    Article  PubMed  Google Scholar 

  • Brenner E, van Damme WJM (1999) Perceived distance, shape and size. Vision Res 39:975–986

    Article  PubMed  CAS  Google Scholar 

  • Caminiti R, Ferraina S, Mayer AB (1998) Visuomotor transformations: early cortical mechanisms of reaching. Curr Opin Neurobiol 8:753–761

    Article  PubMed  CAS  Google Scholar 

  • Churchill A, Hopkins B, Rönnqvist L, Vogt S (2000) Vision of the hand and environmental context in human prehension. Exp Brain Res 134:81–89

    Article  PubMed  CAS  Google Scholar 

  • Culham JC, Kanwisher NG (2001) Neuroimaging of cognitive functions in human parietal cortex. Curr Opin Neurobiol 11:157–163

    Article  PubMed  CAS  Google Scholar 

  • Felton TB, Richards W, Smith RA Jr (1972) Disparity processing of spatial frequencies in man. J Physiol (Lond) 225:349–362

    CAS  Google Scholar 

  • Galea MP, Castiello U, Dalwood N (2001) Thumb invariance during prehension movement: effects of object orientation. Neuroreport 12:2185–2187

    Article  PubMed  CAS  Google Scholar 

  • Glover S (2003) Optic ataxia as a deficit specific to the on-line control of actions. Neurosci Behav Rev 27:447–456

    Google Scholar 

  • Goodwin RT, Romano PE (1985) Stereoacuity degradation by experimental and real monocular and binocular amblyopia. Invest Ophthalmol Vis Sci 26:917–923

    PubMed  CAS  Google Scholar 

  • Grant S, Melmoth DR, Morgan MJ, Finlay AL (2007) Prehension deficits in amblyopia. Invest Ophthalmol Vis Sci 48:1139–1148

    Article  PubMed  Google Scholar 

  • Hibbard PB, Bradshaw MF (2003) Reaching for virtual objects: binocular disparity and the control of prehension. Exp Brain Res 148:196–201

    PubMed  Google Scholar 

  • Jackson SR, Jones CA, Newport R, Pritchard C (1997) A kinematic analysis of goal-directed prehension movements executed under binocular, monocular, and memory-guided viewing conditions. Vis Cog 4:113–142

    Article  Google Scholar 

  • Jackson SR, Newport R, Shaw A (2002) Monocular vision leads to dissociation between grip force and grip aperture scaling during reach-to-grasp movements. Curr Biol 12:237–240

    Article  PubMed  CAS  Google Scholar 

  • Jakobson LS, Goodale MA (1989) Trajectories of reaches to prismatically-displaced targets: evidence for ‘automatic’ visuomotor recalibration. Exp Brain Res 78:575–587

    Article  PubMed  CAS  Google Scholar 

  • Jakobson LS, Goodale MA (1991) Factors affecting higher-order movement planning: a kinematic analysis of human prehension. Exp Brain Res 86:199–208

    Article  PubMed  CAS  Google Scholar 

  • Jeannerod M (1986) Mechanisms of visuomotor coordination: a study in normal and brain-damaged subjects. Neuropsychologica 24:41–78

    Article  CAS  Google Scholar 

  • Jones RK, Lee DN (1981) Why two eyes are better than one: the two views of binocular vision. J Exp Psychol Human Percept Perform 7:30–40

    Article  CAS  Google Scholar 

  • Kudoh N, Hattori M, Numata N, Maruyama K (1997) An analysis of spatiotemporal variability during prehension movements: effects of object size and distance. Exp Brain Res 117:457–464

    Article  PubMed  CAS  Google Scholar 

  • Landy MS, Maloney LT, Johnston EB, Young M (1995) Measurement and modeling of depth cue combination: in defense of weak fusion. Vision Res 35:389–412

    Article  PubMed  CAS  Google Scholar 

  • Levy NS, Glick EB (1974) Stereoscopic perception and Snellen acuity. Am J Ophthalmol 78:722–724

    PubMed  CAS  Google Scholar 

  • Loftus A, Servos P, Goodale MA, Mendarozqueta N, Mon-Williams M (2004a) When two eyes are better than one in prehension: monocular viewing and end-point variance. Exp Brain Res 158:317–327

    PubMed  Google Scholar 

  • Loftus A, Murphy S, McKenna I, Mon-Williams M (2004b) Reduced fields of view are neither necessary nor sufficient for distance underestimation but reduce precision and may cause calibration problems. Exp Brain Res 158:328–335

    PubMed  Google Scholar 

  • Maunsell JHR, Van Essen DC (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. II Binocular interactions and sensitivity to binocular disparity. J Neurophysiol 49:1148–1167

    PubMed  CAS  Google Scholar 

  • Melmoth DR, Grant S (2005) Vision of the thumb as the guide to prehension. Perception 34:Supplement 243

    Google Scholar 

  • Melmoth DR, Grant S (2006) Advantages of binocular vision for the control of reaching and grasping. Exp Brain Res 171:371–388

    Article  PubMed  Google Scholar 

  • Meulenbroek RGJ, Rosenbaum DA, Jansen C, Vaughan J, Vogt S (2001) Multijoint grasping movements. Simulated and observed effects of object location, object size, and initial aperture. Exp Brain Res 138:219–234

    Article  PubMed  CAS  Google Scholar 

  • Mon-Williams M, Dijkerman HC (1999) The use of vergence information in the programming of prehension. Exp Brain Res 128:578–582

    Article  PubMed  CAS  Google Scholar 

  • Mon-Williams M, Tresilian JR (1999) The size-distance paradox is a cognitive phenomenon. Exp Brain Res 126:578–582

    Article  PubMed  CAS  Google Scholar 

  • Mon-Williams M, Tresilian JR, Roberts A (2000) Vergence provides veridical depth perception from horizontal retinal image disparities. Exp Brain Res 133:407–413

    Article  PubMed  CAS  Google Scholar 

  • Paulignan Y, Frak VG, Toni I, Jeannerod M (1997) Influence of object position and size on human prehension movements. Exp Brain Res 114:226–234

    Article  PubMed  CAS  Google Scholar 

  • Poggio GF, Talbot WH (1981) Mechanisms of static and dynamic stereopsis in foveal cortex of the rhesus monkey. J Physiol (Lond) 315:469–492

    CAS  Google Scholar 

  • Poggio GF, Gonzalez F, Krause F (1988) Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity. J Neurosci 8:4531–4550

    PubMed  CAS  Google Scholar 

  • Rabbetts RB (1998) Bennett & Rabbetts’ clinical visual optics, 3rd edn. Butterworth Heinemann, London

    Google Scholar 

  • Rogers B, Bradshaw MF (1993) Vertical disparities, differential perspective and binocular stereopsis. Nature 361:253–255

    Article  PubMed  CAS  Google Scholar 

  • Sakata H, Taira M, Kusunoki M, Murata A, Tsutsui K, Tanaka Y, Shein WN, Miyashita Y (1999) Neural representation of three-dimensional features of manipulation objects with stereopsis. Exp Brain Res 128:160–169

    Article  PubMed  CAS  Google Scholar 

  • Saling M, Mescheriakov S, Molokanova E, Stelmach GE, Berger M (1996) Grip reorganization during wrist transport: the influence of an altered aperture. Exp Brain Res 108:493–500

    Article  PubMed  CAS  Google Scholar 

  • Schor CM, Wood IC, Ogawa J (1984) Spatial tuning of static and dynamic local stereopsis. Vision Res 24:573–578

    Article  PubMed  CAS  Google Scholar 

  • Servos P, Goodale MA (1994) Binocular vision and the on-line control of human prehension. Exp Brain Res 98:119–127

    Article  PubMed  CAS  Google Scholar 

  • Servos P, Goodale MA, Jakobson LS (1992) The role of binocular vision in prehension: a kinematic analysis. Vision Res 32:1513–1521

    Article  PubMed  CAS  Google Scholar 

  • Smeets JBJ, Brenner E (1999) A new view on grasping. Motor Control 3:237–271

    PubMed  CAS  Google Scholar 

  • Tresilian JR, Mon-Williams M, Kelly BM (1999) Increasing confidence in vergence as a distance cue. Proc R Soc Lond Biol Sci 266:39–44

    Article  CAS  Google Scholar 

  • Watt SJ, Bradshaw MF (2000) Binocular cues are important in controlling the grasp but not the reach in natural prehension movements. Neuropsychologica 38:1473–1481

    Article  CAS  Google Scholar 

  • Watt SJ, Bradshaw MF (2003) The visual control of reaching and grasping: binocular disparity and motion parallax. J Exp Psychol Hum Percept Perform 29:404–415

    Article  PubMed  Google Scholar 

  • Wing AM, Fraser C (1983) The contribution of the thumb to reaching movements. Q J Exp Psychol 35A:297–309

    Google Scholar 

  • Wood ICJ (1983) Stereopsis with spatially-degraded images. Ophthal Physiol Opt 3:337–340

    Article  CAS  Google Scholar 

  • Yang Y, Blake R (1991) Spatial frequency tuning of human stereopsis. Vision Res 31:1177–1183

    Article  PubMed  CAS  Google Scholar 

  • Zeki SM (1974) Cells responding to changing image size and disparity in the cortex of the rhesus monkey. J Physiol (Lond) 236:549–573

    CAS  Google Scholar 

Download references

Acknowledgements

Funded by The Wellcome Trust (Grant 066282). We thank Prof. Michael Morgan for comments on the work.

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  1. Mithu Storoni

    Present address: Department of Ophthalmology, Norfolk and Norwich University Hospital, Colney Lane, Norwich, NR4 7UY, UK

Authors and Affiliations

  1. Department of Optometry and Visual Science, The Henry Wellcome Laboratories for Visual Sciences, City University, Northampton Square, London, EC1V 0HB, UK

    Dean R. Melmoth, Mithu Storoni, Georgina Todd, Alison L. Finlay & Simon Grant

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Correspondence to Simon Grant.

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Melmoth, D.R., Storoni, M., Todd, G. et al. Dissociation between vergence and binocular disparity cues in the control of prehension. Exp Brain Res 183, 283–298 (2007). https://doi.org/10.1007/s00221-007-1041-x

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