Abstract
Manual interceptions are known to depend critically on integration of visual feedback information and experience-based predictions of the interceptive event. Within this framework, coupling between gaze and limb movements might also contribute to the interceptive outcome, since eye movements afford acquisition of high-resolution visual information. We investigated this issue by analyzing subjects’ head-fixed oculomotor behavior during manual interceptions. Subjects moved a mouse cursor to intercept computer-generated ballistic trajectories either congruent with Earth’s gravity or perturbed with weightlessness (0g) or hypergravity (2g) effects. In separate sessions, trajectories were either fully visible or occluded before interception to enforce visual prediction. Subjects’ oculomotor behavior was classified in terms of amounts of time they gazed at different visual targets and of overall number of saccades. Then, by way of multivariate analyses, we assessed the following: (1) whether eye movement patterns depended on targets’ laws of motion and occlusions; and (2) whether interceptive performance was related to the oculomotor behavior. First, we found that eye movement patterns depended significantly on targets’ laws of motion and occlusion, suggesting predictive mechanisms. Second, subjects coupled differently oculomotor and interceptive behavior depending on whether targets were visible or occluded. With visible targets, subjects made smaller interceptive errors if they gazed longer at the mouse cursor. Instead, with occluded targets, they achieved better performance by increasing the target’s tracking accuracy and by avoiding gaze shifts near interception, suggesting that precise ocular tracking provided better trajectory predictions for the interceptive response.
Similar content being viewed by others
References
Abrams RA, Meyer DE, Kornblum S (1990) Eye–hand coordination: oculomotor control in rapid aimed limb movements. J Exp Psychol Hum Percept Perform 16:248–267
André-Deshays C, Israël I, Charade O, Berthoz A, Popov K, Lipshits M (1993) Gaze control in microgravity. 1. Saccades, pursuit, eye-head coordination. J Vestib Res 3(3):331–343
Angelaki DE, Shaikh AG, Green AM, Dickman JD (2004) Neurons compute internal models of the physical laws of motion. Nature 430(6999):560–564
Bahill AT, LaRitz T (1984) Why can’t batters keep their eyes on the ball? Am Sci 72:249–253
Bahill AT, Baldwin DG, Venkateswaran J (2006) Predicting a baseball’s path. Am Sci 93:218–225
Barborica A, Ferrera VP (2003) Estimating invisible target speed from neuronal activity in monkey frontal eye field. Nat Neurosci 6(1):66–74
Barnes GR, Collins CJS (2008) Evidence for a link between the extra-retinal component of random-onset pursuit and the anticipatory pursuit of predictable object motion. J Neurophysiol 100(2):1135–1146
Barnes GR, Collins CJS, Arnold LR (2005) Predicting the duration of ocular pursuit in humans. Exp Brain Res 160(1):10–21
Baures R, Benguigui N, Amorim MA, Siegler IA (2007) Intercepting free falling objects: better use Occam’s razor than internalize. Newton’s law. Vis Res 47:2982–2991
Becker W, Fuchs A (1985) Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target. Exp Brain Res 57:562–575
Bennett SJ, Barnes GR (2003) Human ocular pursuit during the transient disappearance of a visual target. J Neurophysiol 90(4):2504–2520
Bennett SJ, Barnes GR (2004) Predictive smooth ocular pursuit during the transient disappearance of a visual target. J Neurophysiol 92(1):578–590
Bennett SJ, Barnes GR (2006a) Combined smooth and saccadic ocular pursuit during the transient occlusion of a moving visual object. Exp Brain Res 168(3):313–321
Bennett SJ, Barnes GR (2006b) Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control. Exp Brain Res 175(1):1–10
Bennett SJ, Benguigui N (2013) Is acceleration used for ocular pursuit and spatial estimation during prediction motion? PLoS One 8(5):e63382
Bennett SJ, Orban de Xivry JJ, Barnes GR, Lefèvre P (2007) Target acceleration can be extracted and represented within the predictive drive to ocular pursuit. J Neurophysiol 98(3):1405–1414
Bennett SJ, Baures R, Hecht H, Benguigui N (2010a) Eye movements influence estimation of time-to-contact in prediction motion. Exp Brain Res 206(4):399–407
Bennett SJ, Orban de Xivry JJ, Lefèvre P, Barnes GR (2010b) Oculomotor prediction of accelerative target motion during occlusion: long-term and short-term effects. Exp Brain Res 204(4):493–504
Binsted G, Chua R, Helsen W, Elliott D (2001) Eye–hand coordination in goal-directed aiming. Hum Mov Sci 20:563–585
Bootsma RJ, Fayt V, Zaal FTJM, Laurent M (1997) On the information-based regulation of movement: what Wann (1996) may want to consider. J Exp Psychol Hum Percept Perform 23:1282–1289
Bosco G, Carrozzo M, Lacquaniti F (2008) Contributions of the human temporoparietal junction and MT/V5+ to the timing of interception revealed by transcranial magnetic stimulation. J Neurosci 28:12071–12084
Bosco G, Delle Monache S, Lacquaniti F (2012) Catching what we can’t see: manual interception of occluded fly-ball trajectories. PloS One 7(11):e49381
Bowman MC, Johansson RS, Johannson RS, Flanagan JR (2009) Eye–hand coordination in a sequential target contact task. Exp Brain Res 195:273–283
Brancazio PJ (1985) Looking into Chapman’s homer: the physics of judging a fly ball. Am J Phys 53:849–855
Brenner E, Smeets JBJ (2009) Sources of variability in interceptive movements. Exp Brain Res 195:117–133
Brenner E, Smeets JBJ (2011) Continuous visual control of interception. Hum Mov Sci 30:475–494
Brenner E, Smeets JBJ, de Lussanet MHE (1998) Hitting moving targets: continuous control of the acceleration of the hand on the basis of the target’s velocity. Exp Brain Res 122:467–474
Brouwer AM, Brenner E, Smeets JBJ (2000) Hitting moving objects: the dependency of hand velocity on the speed of the target. Exp Brain Res 133:242–248
Brouwer A, Brenner E, Smeets JBJ (2002) Perception of acceleration with short presentation times: can acceleration be used in interception? Percept Psychophys 64(7):1160–1168
Buchel C, Josephs O, Rees G, Turner R, Frith CD, Friston KJ (1998) The functional anatomy of attention to visual motion. A functional MRI study. Brain 121:1281–1294
Carnahan H, Marteniuk RG (1991) The temporal organization of hand, eye, and head movements during reaching and pointing. J Mot Behav 23:109–119
Chapman S (1968) Catching a baseball. Am J Phys 36:868–870
Clarke AH (2008) Listing’s plane and the otolith-mediated gravity vector. Prog Brain Res 171:291–294
Clarke AH, Haslwanter T (2007) The orientation of Listing’s plane in microgravity. Vis Res 47(25):3132–3140
Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA, Linenweber MR, Petersen SE, Raichle ME, Van Essen DC, Shulman GL (1998) A common network of functional areas for attention and eye movements. Neuron 21:761–773
de Lussanet MH, Smeets JB, Brenner E (2004) The quantitative use of velocity information in fast interception. Exp Brain Res 157:181–196
de Rugy A, Marinovic W, Wallis G (2012) Neural prediction of complex accelerations for object interception. J Neurophysiol 107:766–771
Dessing JC, Bullock D, Peper CE, Beek PJ (2002) Prospective control of manual interceptive actions: comparative simulations of extant and new model constructs. Neural Netw 15:163–179
Dessing JC, Peper CL, Bullock D, Beek PJ (2005) How position, velocity, and temporal information combine in the prospective control of catching: data and model. J Cogn Neurosci 17:668–686
Dessing JC, Oostwoud Wijdenes L, Peper CE, Beek PJ (2009) Visuomotor transformation for interception: catching while fixating. Exp Brain Res 196:511–527
Diaz G, Cooper J, Rothkopf C, Hayhoe M (2013) Saccades to future ball location reveal memory-based prediction in a virtual-reality interception task. J Vis 13(1):20
Eggert T, Rivas F, Straube A (2005) Predictive strategies in interception tasks: differences between eye and hand movements. Exp Brain Res 160:433–449
Faisal AA, Wolpert DM (2009) Near optimal combination of sensory and motor uncertainty in time during a naturalistic perception–action task. J Neurophysiol 101(4):1901–1912
Ferrera VP, Barborica A (2010) Internally generated error signals in monkey frontal eye field during an inferred motion task. J Neurosci 30(35):11612–11623
Findlay J (1981) Spatial and temporal factors in the predictive generation of saccadic eye movements. Vis Res 21:347–351
Fink PW, Foo PS, Warren WH (2009) Catching fly balls in virtual reality: a critical test of the outfielder problem. J Vis 9:1–8
Gielen CC, Dijkstra TM, Roozen IJ, Welten J (2009) Coordination of gaze and hand movements for tracking and tracing in 3D. Cortex 45(3):340–355
Green AM, Angelaki DE (2010a) Internal models and neural computation in the vestibular system. Exp Brain Res 200(3–4):197–222
Green AM, Angelaki DE (2010b) Multisensory integration: resolving sensory ambiguities to build novel representations. Curr Opin Neurobiol 20(3):353–360
Hardiess G, Hansmann-Roth S, Mallot HA (2013) Gaze movements and spatial working memory in collision avoidance: a traffic intersection task. Front Behav Neurosci 7:62
Hayhoe MM, McKinney T, Chajka K, Pelz JB (2012) Predictive eye movements in natural vision. Exp Brain Res 217(1):125–136
Helsen WF, Elliott D, Starkes JL, Ricker KL (2000) Coupling of eye, finger, elbow, and shoulder movements during manual aiming. J Mot Behav 32:241–248
Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F (2005) Representation of visual gravitational motion in the human vestibular cortex. Science 308:416–419
Indovina I, Maffei V, Pauwels K, Macaluso E, Orban GA, Lacquaniti F (2013) Simulated self-motion in a visual gravity field: sensitivity to vertical and horizontal heading in the human brain. Neuroimage 71:114–124
Johansson RS, Westling G, Backstrom A, Flanagan JR (2001) Eye–hand coordination in object manipulation. J Neurosci 21:6917–6932
Kato K, Higashiyama A (1998) Estimation of height for persons in pictures. Percept Psychophys 60:1318–1328
Kattoulas E, Smyrnis N, Mantas A, Evdokimidis I, Raos V et al (2008) Arm movement metrics influence saccade metrics when looking and pointing towards a memorized target location. Exp Brain Res 189:323–338
Kattoulas E, Smyrnis N, Stefanis NC, Avramopoulos D, Stefanis CN, Evdokimidis I (2011) Predictive smooth eye pursuit in a population of young men: I. Effects of age, IQ, oculomotor and cognitive tasks. Exp Brain Res 215:207–218
Kettner RE, Leung HC, Peterson BW (1996) Predictive smooth pursuit of complex two dimensional trajectories in monkey: component interactions. Exp Brain Res 108:221–235
Kowler E (1989) Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit. Vis Res 29(9):1049–1057
Kowler E, Martins A, Pavel M (1984) The effect of expectations on slow oculomotor control-IV. Anticipatory smooth eye movements depend on prior target motions. Vis Res 24(3):197–210
Land MF, Furneaux S (1997) The knowledge base of the oculomotor system. Philos Trans R Soc B 352:1231–1239
Land MF, McLeod P (2000) From eye movements to actions: how batsmen hit the ball. Nat Neurosci 3:1340–1345
Land M, Mennie N, Rusted J (1999) The roles of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328
Lyon DR, Waag WL (1995) Time course of visual extrapolation accuracy. Acta Psychol 89:239–260
López-Moliner J, Brenner E, Louw S, Smeets JBJ (2010) Catching a gently thrown ball. Exp Brain Res 206:409–417
Madelain L, Krauzlis RJ (2003) Effects of learning on smooth pursuit during transient disappearance of a visual target. J Neurophysiol 90(2):972–982
Maffei V, Macaluso E, Indovina I, Orban G, Lacquaniti F (2010) Processing of targets in smooth or apparent motion along the vertical in the human brain: an fMRI study. J Neurophysiol 103:360–370
Marinovic W, Plooy AM, Tresilian JR (2009) Preparation and inhibition of interceptive actions. Exp Brain Res 197:311–319
McBeath MK, Shaffer DM, Kaiser M (1995) How baseball outfielders determine where to run to catch fly balls. Science 268:569–573
McIntyre J, Zago M, Berthoz A, Lacquaniti F (2001) Does the brain model Newton’s laws? Nat Neurosci 4:693–694
McKinney T, Chajka K, Hayhoe M (2008) Pro-active gaze control in squash. J Vis 8:111
McLeod P, Reed N, Dienes Z (2002) The optic trajectory is not a lot of use if you want to catch the ball. J Exp Psychol Hum Perfect Perform 28:1499–1501
McLeod P, Reed N, Dienes Z (2003) How fielders arrive in time to catch the ball. Nature 426:244–245
McLeod P, Reed N, Dienes Z (2006) The generalized optic acceleration cancellation theory of catching. J Exp Psychol Hum Percept Perform 32:139–148
McLeod P, Reed N, Gilson SJ, Glennerster A (2008) How soccer players head the ball: a test of optic acceleration cancellation theory with virtual reality. Vis Res 48:1479–1487
Merfeld DM, Zupan L, Peterka RJ (1999) Humans use internal models to estimate gravity and linear acceleration. Nature 398(6728):615–618
Michaels CF, Oudejans RD (1992) The optics and actions of catching fly balls: zeroing out optic acceleration. Ecol Psychol 4:199–222
Miller WL, Maffei V, Bosco G, Iosa M, Zago M, Lacquaniti F (2008) Vestibular nuclei and cerebellum put visual gravitational motion in context. J Neurophysiol 99:1969–1982
Mrotek LA (2013) Following and intercepting scribbles: interactions between eye and hand control. Exp Brain Res 227(2):161–174
Mrotek LA, Soechting JF (2007a) Target interception: hand–eye coordination and strategies. J Neurosci 27:7297–7309
Mrotek LA, Soechting JF (2007b) Predicting curvilinear target motion through an occlusion. Exp Brain Res 178:99–114
Neggers SFW, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83:639–651
Neggers SFW, Bekkering H (2001) Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. J Neurophysiol 86:961–970
Nooij SA, Bos JE, Groen EL (2008) Orientation of Listing’s plane after hypergravity in humans. J Vestib Res 18(2–3):97–105
Orban de Xivry JJ, Bennett SJ, Lefèvre P, Barnes GR (2006) Evidence for synergy between saccades and smooth pursuit during transient target disappearance. J Neurophysiol 95(1):418–427
Orban de Xivry JJ, Missal M, Lefèvre P (2008) A dynamic representation of target motion drives predictive smooth pursuit during target blanking. J Vis 8(15):6.1–6.13
Orban de Xivry JJ, Missal M, Lefèvre P (2009) Smooth pursuit performance during target blanking does not influence the triggering of predictive saccades. J Vis 9:7.1–7.16
Pelz J, Hayhoe M, Loeber R (2001) The coordination of eye, head, and hand movements in a natural task. Exp Brain Res 139:266–277
Peper CE, Bootsma RJ, Mestre DR, Bakker FC (1994) Catching balls: how to get the hand to the right place at the right time. J Exp Psychol Hum Percept Perform 20:591–612
Port NL, Lee D, Dassonville P, Georgopoulos AP (1997) Manual interception of moving targets. I. Performance and movement initiation. Exp Brain Res 116:406–420
Postma DBW, den Otter AR, Zaal FTJM (2014) Keeping your eyes continuously on the ball while running for catchable and uncatchable fly balls. PLoS One 9(3):e92392
Regan D, Gray R (2000) Visually guided collision avoidance and collision achievement. Trends Cogn Sci 4:99–107
Ripoll H, Bard C, Paillard J (1986) Stabilization of head and eyes on target as a factor in successful basketball shooting. Hum Mov Sci 5:47–58
Rodrigues ST, Vickers JN, Williams AM (2002) Head, eye and arm coordination in table tennis. J Sports Sci 20:187–200
Rozendaal LA, van Soest AJ (2003) Optical acceleration cancellation: a viable interception strategy? Biol Cybern 89:415–425
Senot P, Zago M, Lacquaniti F, McIntyre J (2005) Anticipating the effects of gravity when intercepting moving objects: differentiating up and down based on nonvisual cues. J Neurophysiol 94:4471–4480
Senot P, Zago M, Le Séac’h A, Zaoui M, Berthoz A, Lacquaniti F, McIntyre J (2012) When up is down in 0g: how gravity sensing affects the timing of interceptive actions. J Neurosci 32:1969–1973
Shaffer DM, McBeath MK (2002) Baseball outfielders maintain a linear optical trajectory when tracking uncatchable fly balls. J Exp Psychol Hum Percept Perform 28:335–348
Shaffer DM, McBeath MK, Roy WL, Krauchunas SM (2003) A linear optical trajectory informs the fielder where to run to the side to catch fly balls. J Exp Psychol Hum Percept Perform 29:1244–1250
Sharp RH, Whiting HTA (1974) Exposure and occluded duration effects in a ball-catching skill. J Mot Behav 6:139–147
Shelhamer M, Joiner WM (2003) Saccades exhibit abrupt transition between reactive and predictive; predictive saccade sequences have long-term correlations. J Neurophysiol 90(4):2763–2769
Soechting JF, Flanders M (2008) Extrapolation of visual motion for manual interception. J Neurophysiol 99:2956–2967
Souto D, Kerzel D (2013) Like a rolling stone: naturalistic visual kinematics facilitate tracking eye movements. J Vis 13(2):9
Spering M, Schütz AC, Braun DI, Gegenfurtner KR (2011) Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion. J Neurophysiol 105:1756–1767
Tabata H, Miura K, Kawano K (2007) Preparation for smooth pursuit eye movement based on expectation in humans. Syst Comput Jpn 38(6):1–9
Van Donkelaar P, Lee RG, Gellman RS (1992) Control strategies in directing the hand to moving targets. Exp Brain Res 91:151–161
Whiting HTA, Gill EB, Stephenson JM (1970) Critical time intervals for taking in flight information in a ball-catching task. Ergonomics 13:265–272
Zago M, Bosco G, Maffei V, Iosa M, Ivanenko YP, Lacquaniti F (2004) Internal models of target motion: expected dynamics overrides measured kinematics in timing manual interceptions. J Neurophysiol 91:1620–1634
Zago M, Bosco G, Maffei V, Iosa M, Ivanenko YP, Lacquaniti F (2005) Fast adaptation of the internal model of gravity for manual interceptions: evidence for event-dependent learning. J Neurophysiol 93:1055–1068
Zago M, McIntyre J, Senot P, Lacquaniti F (2008) Internal models and prediction of visual gravitational motion. Vis Res 48:1532–1538
Zago M, McIntyre J, Senot P, Lacquaniti F (2009) Visuo-motor coordination and internal models for object interception. Exp Brain Res 192:571–604
Zago M, La Scaleia B, Miller WL, Lacquaniti F (2011a) Coherence of structural visual cues and pictorial gravity paves the way for interceptive actions. J Vis 11(10):13, 1–10
Zago M, La Scaleia B, Miller WL, Lacquaniti F (2011b) Observing human movements helps decoding environmental forces. Exp Brain Res 215:53–63
Acknowledgments
This work was supported by the Italian Ministry of University and Research (PRIN Grant) and the Italian Space Agency (CRUSOE and COREA Grants).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Delle Monache, S., Lacquaniti, F. & Bosco, G. Eye movements and manual interception of ballistic trajectories: effects of law of motion perturbations and occlusions. Exp Brain Res 233, 359–374 (2015). https://doi.org/10.1007/s00221-014-4120-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-014-4120-9