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Gaze–grasp coordination in obstacle avoidance: differences between binocular and monocular viewing

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Abstract

Most adults can skillfully avoid potential obstacles when acting in everyday cluttered scenes. We examined how gaze and hand movements are normally coordinated for obstacle avoidance and whether these are altered when binocular depth information is unavailable. Visual fixations and hand movement kinematics were simultaneously recorded, while 13 right-handed subjects reached-to-precision grasp a cylindrical household object presented alone or with a potential obstacle (wine glass) located to its left (thumb’s grasp side), right or just behind it (both closer to the finger’s grasp side) using binocular or monocular vision. Gaze and hand movement strategies differed significantly by view and obstacle location. With binocular vision, initial fixations were near the target’s centre of mass (COM) around the time of hand movement onset, but usually shifted to end just above the thumb’s grasp site at initial object contact, this mainly being made by the thumb, consistent with selecting this digit for guiding the grasp. This strategy was associated with faster binocular hand movements and improved end-point grip precision across all trials than with monocular viewing, during which subjects usually continued to fixate the target closer to its COM despite a similar prevalence of thumb-first contacts. While subjects looked directly at the obstacle at each location on a minority of trials and their overall fixations on the target were somewhat biased towards the grasp side nearest to it, these gaze behaviours were particularly marked on monocular vision-obstacle behind trials which also commonly ended in finger-first contact. Subjects avoided colliding with the wine glass under both views when on the right (finger side) of the workspace by producing slower and straighter reaches, with this and the behind obstacle location also resulting in ‘safer’ (i.e. narrower) peak grip apertures and longer deceleration times than when the goal object was alone or the obstacle was on its thumb side. But monocular reach paths were more variable and deceleration times were selectively prolonged on finger-side and behind obstacle trials, with this latter condition further resulting in selectively increased grip closure times and corrections. Binocular vision thus provided added advantages for collision avoidance, known to require intact dorsal cortical stream processing mechanisms, particularly when the target of the grasp and potential obstacle to it were fairly closely separated in depth. Different accounts of the altered monocular gaze behaviour converged on the conclusion that additional perceptual and/or attentional resources are likely engaged compared to when continuous binocular depth information is available. Implications for people lacking binocular stereopsis are briefly considered.

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References

  • Anderson J, Bingham GP (2010) A solution to the online guidance problem for targeted reaches: proportional rate control using relative disparity τ. Exp Brain Res 205:291–306

    Article  PubMed  Google Scholar 

  • Bauer A, Dietz K, Hart W, Schiefer U (2001) The relevance of stereopsis for motorists: a pilot study. Graefe’s Arch Clin Exp Ophthalmol 239:400–406

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

    Article  PubMed  Google Scholar 

  • Brouwer A-M, Franz VH, Gegenfurtner KR (2009) Differences in fixations between grasping and viewing objects. J Vis 9:1–24

    Google Scholar 

  • Buckley JG, Panesar GK, MacLellan MJ, Pacey IE, Barrett BT (2010) Changes to control of adaptive gait in individuals with long-standing reduced stereoacuity. Invest Ophthalmol Vis Sci 51:2487–2495

    Article  PubMed  Google Scholar 

  • Cavina-Pratesi C, Hesse C (2013) Why do the eyes prefer the index finger? Simultaneous recording of eye and hand movements during precision grasping. J Vis 13:1–15

    Article  Google Scholar 

  • Cottereau BR, McKee SP, Ales JM, Norcia AM (2011) Disparity-tuned population responses from human visual cortex. J Neurosci 31:954–965

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Culham JC, Brandt SA, Cavanagh P, Kanwisher NG, Dale AM, Tootell RBH (1998) Cortical fMRI activation produced by attentive tracking of moving targets. J Neurophysiol 80:2657–2670

    CAS  PubMed  Google Scholar 

  • Danckert J, Goodale MA (2001) Superior performance for visually guided pointing in the lower visual field. Exp Brain Res 137:303–308

    Article  CAS  PubMed  Google Scholar 

  • de Grave DDJ, Hesse C, Brouwer A-M, Franz VH (2008) Fixation locations when grasping partly occluded objects. J Vision 8:1–11

    Article  Google Scholar 

  • Desanghere L, Marotta JJ (2011) “Graspability” of objects affects gaze patterns during perception and action tasks. Exp Brain Res 212:177–187

    Article  PubMed  Google Scholar 

  • Fehd HM, Seiffert AE (2010) Looking at the center of the targets helps multiple object tracking. J Vis 10:1–13

    Article  PubMed  Google Scholar 

  • Flanagan JR, Terao Y, Johansson RS (2008) Gaze behavior when reaching to remembered targets. J Neurophysiol 100:1533–1543

    Article  PubMed  Google Scholar 

  • Gallivan JP, Cavina-Pratesi C, Culham JC (2009) Is that within reach? fMRI reveals that human superior parieto-occipital cortex encodes objects reachable by the hand. J Neurosci 29:4381–4391

    Article  CAS  PubMed  Google Scholar 

  • Gnanaseelan R, Gonzalez D, Niechwiej-Szwedo E (2014) Binocular advantage for prehension movements performed in visually enriched environments requiring visual search. Front Hum Neurosci. doi:10.3389/fnhum.2014.00959

    PubMed Central  PubMed  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 

  • Greenwald HS, Knill DC, Saunders JA (2005) Integrating visual cues for motor control: a matter of time. Vis Res 45:1975–1989

    Article  PubMed  Google Scholar 

  • Haggard P, Wing AM (1997) On the hand transport component of prehensile movements. J Motor Behav 29:282–287

    Article  CAS  Google Scholar 

  • Jackson SR, Jackson GM, Rosicky J (1995) Are non-relevant objects represented in working memory? The effect of non-target objects on reach and grasp kinematics. Exp Brain Res 102:519–530

    Article  CAS  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 Cogn 4:113–142

    Article  Google Scholar 

  • Johansson RS, Westling G, Bäckström A, Flanagan JR (2001) Eye-hand coordination in object manipulation. J Neurosci 21:6917–6932

    CAS  PubMed  Google Scholar 

  • Keefe BD, Watt SJ (2009) The role of binocular vision in grasping: a small stimulus-set distorts results. Exp Brain Res 194:435–444

    Article  PubMed  Google Scholar 

  • Knill DC (2005) Reaching for visual cues to depth: the brain combines depth cues differently for motor control and perception. J Vis 5:103–115

    Article  PubMed  Google Scholar 

  • Kritikos A, Bennett KMB, Dunai J, Castiello U (2000) Interference from distractors in reach-to-grasp movements. Q J Exp Psychol 53A:131–151

    Article  Google Scholar 

  • Land MF, Mennie N, Rusted J (1997) The roles of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328

    Article  Google Scholar 

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

    Article  CAS  PubMed  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 

  • Makris S, Grant S, Hadar AA, Yarrow K (2013) Binocular vision enhances a rapidly evolving affordance priming effect: behavioural and TMS evidence. Brain Cogn 83:279–287

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • McIntosh RD, McClements KI, Dijkerman HC, Birchall D, Milner AD (2004) Preserved obstacle avoidance during reaching in patients with left visual neglect. Neuropyschologica 42:1107–1117

    Article  CAS  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 

  • Melmoth DR, Grant S (2012) Getting a grip: different actions and visual guidance of the thumb and finger in precision grasping. Exp Brain Res 222:265–276

    Article  PubMed  Google Scholar 

  • Melmoth DR, Storoni M, Todd G, Finlay AL, Grant S (2007) Dissociation between vergence and binocular disparity cues in the control of prehension. Exp Brain Res 183:283–298

    Article  PubMed  Google Scholar 

  • Melmoth DR, Finlay AL, Morgan MJ, Grant S (2009) Grasping deficits and adaptations in adults with stereo vision losses. Invest Ophthalmol Vis Sci 50:3711–3720

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Mon-Williams M, McIntosh RD (2000) A test between two hypotheses and a possible third way for the control of prehension. Exp Brain Res 134:268–273

    Article  CAS  PubMed  Google Scholar 

  • Mon-Williams M, Tresilian JR, Coppard VL, Carson RG (2001) The effect of obstacle position on reach-to-grasp movements. Exp Brain Res 137:497–501

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pardhan S, Zuidhoek S (2013) Dual cognitive task affects reaching and grasping behavior in subjects with macular disorders. Invest Ophthalmol Vis Sci 54:3281–3288

    Article  PubMed  Google Scholar 

  • Pardhan S, Gonzalez-Alvarez C, Subramanian A (2011) How does the presence and duration of central visual impairment affect reaching and grasping movements? Ophthalmic Physiol Opt 31:233–239

    Article  PubMed  Google Scholar 

  • Previc FH (1990) Functional specialization in the lower and upper visual fields in humans: its ecological origins and neurophysiological implications. Behav Brain Res 13:519–575

    Google Scholar 

  • Prime SL, Marotta JJ (2013) Gaze strategies during visually-guided versus memory-guided grasping. Exp Brain Res 225:291–305

    Article  PubMed  Google Scholar 

  • Pylyshyn Z, Storm R (1988) Tracking multiple independent targets: evidence for a parallel tracking mechanism. Spat Vis 3:179–197

    Article  CAS  PubMed  Google Scholar 

  • Quinlan DJ, Culham JC (2007) fMRI reveals a preference for near viewing in the human parieto-occipital cortex. Neuroimage 36:167–187

    Article  CAS  PubMed  Google Scholar 

  • Rice NJ, McIntosh RD, Schindler I, Mon-Williams M, Demonet JF, Milner AD (2006) Intact automatic avoidance of obstacles in patients with visual form agnosia. Exp Brain Res 174:176–188

    Article  PubMed  Google Scholar 

  • Rosenbaum DA, Meulenbrook RJ, Vaughan J, Jansen C (2001) Posture-based motion planning: applications to grasping. Psychol Rev 108:709–734

    Article  CAS  PubMed  Google Scholar 

  • Schlicht EJ, Schrater PR (2007) Effects of visual uncertainty on grasping movements. Exp Brain Res 182:47–57

    Article  PubMed  Google Scholar 

  • Schindler I, Rice NJ, McIntosh RD, Rossetti Y, Vighetto A, Milner AD (2004) Automatic avoidance of obstacles is a dorsal stream function: evidence from optic ataxia. Nat Neurosci 7:779–784

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Singhal A, Culham JC, Chinellato E, Goodale MA (2007) Dual-task interference is greater in delayed grasping than in visually guided grasping. J Vis 7:1–12

    Article  PubMed  Google Scholar 

  • Srivastava S, Orban GA, De Mazière PA, Janssen P (2009) A distinct representation of three-dimensional shape in macaque anterior intraparietal area: fast, metric and coarse. J Neurosci 29:10613–10626

    Article  CAS  PubMed  Google Scholar 

  • Tipper SP, Howard LA, Jackson SR (1997) Selective reaching to grasp: evidence for distractor interference effects. Vis Cogn 4:1–38

    Article  Google Scholar 

  • Tombu M, Seiffert A (2008) Attentional costs in multiple-object tracking. Cognition 108:1–25

    Article  PubMed Central  PubMed  Google Scholar 

  • Tresilian JR (1998) Attention in action or obstruction of movement? A kinematic analysis of avoidance behavior in prehension. Exp Brain Res 120:352–368

    Article  CAS  PubMed  Google Scholar 

  • Verhagen L, Dijkerman HC, Grol MJ, Toni I (2008) Perceptuo-motor interactions during prehension movements. J Neurosci 28:4726–4735

    Article  CAS  PubMed  Google Scholar 

  • Verhagen L, Dijkerman HC, Medendorp WP, Toni I (2012) Cortical dynamics of sensorimotor integration during grasp planning. J Neurosci 32:4508–4519

    Article  CAS  PubMed  Google Scholar 

  • Verheij R, Brenner E, Smeets JBJ (2012) Grasping kinematics from the perspective of individual digits: a modelling study. PLoS ONE 7(3):e33150. doi:10.1371/journal.pone.0033150

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Verheij R, Brenner E, Smeets JBJ (2014a) The influence of target object shape on maximum grip aperture in human grasping movements. Exp Brain Res 232:3569–3578

    Article  PubMed  Google Scholar 

  • Verheij R, Brenner E, Smeets JBJ (2014b) Why does an obstacle just below the digits’ paths not influence a grasping movement while an obstacle to the side of their paths does? Exp Brain Res 232:103–112

    Article  PubMed  Google Scholar 

  • Volcic R, Domini F (2014) The visibility of contact points influences grasping movements. Exp Brain Res 232:2997–3005

    Article  PubMed  Google Scholar 

  • Voudouris D, Smeets JBJ, Brenner E (2012a) Do humans prefer to see their grasping points? J Motor Behav 44:295–304

    Article  CAS  Google Scholar 

  • Voudouris D, Smeets JBJ, Brenner E (2012b) Do obstacles affect the selection of grasping points? Hum Mov Sci 31:1090–1102

    Article  CAS  PubMed  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 (2002) Binocular information in the control of prehensile movements in multiple-object scenes. Spat Vis 15:141–155

    Article  PubMed  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

    Article  Google Scholar 

  • Yantis S (1992) Multielement visual tracking: attention and perceptual organization. Cogn Psychol 24:295–340

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Thanks to TrackSys (Nottingham, UK) and Michael Morgan for loans of gaze recording equipment, and to Ken Cocker, Asim Hyder, Dean Melmoth, Keval Sejpar and Colin Vallance for help with the experiments. This study was supported by Grants 066282 and 093280/Z/10/Z from the Wellcome Trust.

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Grant, S. Gaze–grasp coordination in obstacle avoidance: differences between binocular and monocular viewing. Exp Brain Res 233, 3489–3505 (2015). https://doi.org/10.1007/s00221-015-4421-7

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