Skip to main content
Log in

Advantages of binocular vision for the control of reaching and grasping

Experimental Brain Research Aims and scope Submit manuscript

Abstract

Theoretical considerations suggest that binocular information should provide advantages, compared to monocular viewing, for the planning and execution of natural reaching and grasping actions, but empirical support for this is quite equivocal. We have examined these predictions on a simple prehension task in which normal subjects reached, grasped and lifted isolated cylindrical household objects (two sizes, four locations) in a well-lit environment, using binocular vision or with one eye occluded. Various kinematic measures reflecting the programming and on-line control of the movements were quantified, in combination with analyses of different types of error occurring in the velocity, spatial path and grip aperture profiles of each trial. There was little consistent effect of viewing condition on the early phase of the reach, up to and including the peak deceleration, but all other aspects of performance were superior under binocular control. Subjects adopted a cautious approach when binocular information was unavailable: they extended the end phase of the reach and pre-shaped their hand with a wider grip aperture further away from the object. Despite these precautions, initial grip application was poorly coordinated with target contact and was inaccurately scaled to the objects’ dimensions, with the subsequent post-contact phase of the grasp significantly more prolonged, error-prone and variable compared to binocular performance. These effects were obtained in two separate experiments in which the participants’ performed the task under randomized or more predictable (blocked) viewing conditions. Our data suggest that binocular vision offers particular advantages for controlling the terminal reach and the grasp. We argue that these benefits derive from binocular disparity processing linked to changes in relative hand–target distance, and that this depth information is independently used to regulate the progress of the approaching hand and to guide the digits to the (pre-selected) contact points on the object, thereby ensuring that the grip is securely applied.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

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

    PubMed  Google Scholar 

  • Bingham GP, Pagano CC (1998) The necessity of a perception-action approach to definite distance perception: monocular distance perception for reaching. J Exp Psychol Hum Percept Perform 24:145–168

    Article  PubMed  CAS  Google Scholar 

  • Bingham GP, Zaal F, Robin D, Shull JA (2000) Distortions in definite distance and shape perception as measured by reaching without and with haptic feedback. J Exp Psychol Hum Percept Perform 26:1436–1460

    Article  PubMed  CAS  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 

  • Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund H-J (1998) Human anterior intraparietal area subserves prehension. A combined lesion and functional MRI activation study. Neurology 50:1253–1259

    PubMed  CAS  Google Scholar 

  • Bootsma RJ, Marteniuk RG, MacKenzie CL, Zaal FTJM (1994) The speed-accuracy trade-off in manual prehension: effects of movement amplitude, object size and object width on kinematic characteristics. Exp Brain Res 98:535–541

    Article  PubMed  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 (2004) Binocular cues and the control of prehension. Spat Vis 17:95–110

    Article  PubMed  Google Scholar 

  • Brenner E, Van Damme WJM (1998) Judging distance from ocular convergence. Vision Res 38:493–498

    Article  PubMed  CAS  Google Scholar 

  • Castiello U, Bonfigliolo C, Bennett KMB (1996) How perceived object dimension influences prehension. Neuroreport 7:825–829

    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, Danckert SL, DeSouza JFX, Gati JS, Menon RS, Goodale MA (2003) Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153:180–189

    Article  PubMed  Google Scholar 

  • Ernst MO, Banks MS (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415: 429–433

    Article  PubMed  CAS  Google Scholar 

  • Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47:381–391

    Article  PubMed  CAS  Google Scholar 

  • Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784

    Article  PubMed  CAS  Google Scholar 

  • Hopkins B, Churchill A, Vogt S, Rönnqvist L (2004) Braking reaching movements: a test of the constant tau-dot strategy under different viewing conditions. J Mot Behav 36:3–12

    Article  PubMed  Google Scholar 

  • Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. NeuroReport 5: 1525–1529

    Article  PubMed  CAS  Google Scholar 

  • Gardner PL, Mon-Williams M (2001) Vertical gaze angle: absolute height-in-scene information for the programming of prehension. Exp Brain Res 136:379–385

    Article  PubMed  CAS  Google Scholar 

  • Glover S (2002) Visual illusions affect planning but not control. Trends Cogn Sci 6:288–292

    Article  PubMed  Google Scholar 

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

    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. Visl Cog 4:113–142

    Article  Google Scholar 

  • Jackson SR, Newport R, Shaw A (2002) Monocular vision leads to a 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 (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 (1984) The timing of natural prehension movements. J Mot Behav 16:235–254

    PubMed  CAS  Google Scholar 

  • Jeannerod M (1988) The neural and behavioural organization of goal-directed movements. Clarendon Press, Oxford

    Google Scholar 

  • Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18: 314–320

    Article  PubMed  CAS  Google Scholar 

  • Jenmalm P, Johansson RS (1997) Visual and somatosensory information about object shape control manipulative fingertip forces. J Neurosci 17:4486–4499

    PubMed  CAS  Google Scholar 

  • Johansson RS, Westling G (1984) Roles of glaborous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 56:550–564

    Article  PubMed  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 

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

    PubMed  Google Scholar 

  • Marotta JJ, Goodale MA (1998) The role of learned pictorial cues in the programming and control of grasping. Exp Brain Res 121:465–470

    Article  PubMed  CAS  Google Scholar 

  • Marotta JJ, Goodale MA (2001) The role of familiar size in the control of grasping. J Cog Neurosci 13:8–17

    Article  CAS  Google Scholar 

  • Marteniuk RG, Leavitt JL, MacKenzie CL, Athenes S (1990) Functional relationships between grasp and transport components in a prehension task. Hum Mov Sci 9:149–176

    Article  Google Scholar 

  • Mazyn LI, Lenoir M, Montagne G, Savelsbergh GJ (2004) The contribution of stereo vision to one-handed catching. Exp Brain Res 157:383–390

    Article  PubMed  Google Scholar 

  • Melmoth DR, Finlay AL, Morgan MJ, Grant S (2005) Deficits in the on-line control of reaching and grasping movements in stereodeficient adults. Spat Vis 18: (abstract)

  • Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, Oxford

    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 

  • Morgan MJ (1989) Vision of solid objects. Nature 339:101–103

    Article  PubMed  CAS  Google Scholar 

  • Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1991a) Selective perturbation of visual input during prehension movements. I. The effects of changing object position. Exp Brain Res 83:502–512

    Article  CAS  Google Scholar 

  • Paulignan Y, Jeannerod M, MacKenzie C, Marteniuk R (1991b) Selective perturbation of visual input during prehension movements II. The effects of changing object size. Exp Brain Res 87:407–420

    Article  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologica 9:97–112

    Article  CAS  Google Scholar 

  • Rogers B, Cagenello R (1989) Disparity curvature and the perception of three-dimensional surfaces. Nature 339:135–137

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rossetti Y, Pisella L, Vighetto A (2003) Optic ataxia revisited: visually guided action versus immediate visuomotor control. Exp Brain Res 153:171–179

    Article  PubMed  Google Scholar 

  • Sakata H, Taira M, Kusunoki M, Murata A, Tanaka Y (1997) The parietal association cortex in depth perception and visual control of hand action. Trends Neurosci 20:350–357

    Article  PubMed  CAS  Google Scholar 

  • Servos P (2000) Distance estimation in the visual and visuomotor systems. Exp Brain Res 130:35–47

    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 

  • Sivak B, MacKenzie CL (1990) Integration of visual information and motor output in reaching and grasping: the contributions of peripheral and central vision. Neuropsychologica 28:1095–1116

    Article  CAS  Google Scholar 

  • Taira M, Mine S, Georgopoulos AP, Murata A, Sakata H (1990) Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res 83:29–36

    Article  PubMed  CAS  Google Scholar 

  • Tresilian JR, Mon-Williams M, Kelly BM (1999) Increasing confidence in vergence as a distance cue. Proc R Soc Lond B 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 

  • Watt SJ, Bradshaw MF, Rushton SK (2000) Field of view affects reaching, not grasping. Exp Brain Res 135:411–416

    Article  PubMed  CAS  Google Scholar 

  • Westling G, Johansson RS (1984) Factors influencing the force control during precision grip. Exp Brain Res 53:277–284

    Article  PubMed  CAS  Google Scholar 

  • Wing AM, Turton A, Fraser C (1986) Grasp size and accuracy of approach in reaching. J Mot Behav 18:245–260

    PubMed  CAS  Google Scholar 

  • Zaal FTJM, Bootsma RJ (1995) The topology of limb deceleration in prehension tasks. J Mot Behav 27:193–207

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by a grant from the Wellcome Trust (no. 066282) to S. Grant. We thank Alistair Fielder, Stephen Jackson, Christopher Kennard and Michael Morgan for their help and advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Simon Grant.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Melmoth, D.R., Grant, S. Advantages of binocular vision for the control of reaching and grasping. Exp Brain Res 171, 371–388 (2006). https://doi.org/10.1007/s00221-005-0273-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0273-x

Keywords

Navigation