Saccades to future ball location reveal memory-based prediction in a virtual-reality interception task

Journal of Vision

Volumn 13, Issue 1, 2013, Pages

  Diaz, Gabriel ^a   Cooper, Joseph ^a   Rothkopf, Constantin ^b   Hayhoe, Mary ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b FRANKFURT INSTITUTE FOR ADVANCED STUDIES   (Germany)

Author keywords

Anticipation; Eye movements; Prediction; Pursuit eye movements; Saccade

Indexed keywords

ARTICLE; COMPARATIVE STUDY; COMPUTER INTERFACE; COMPUTER SIMULATION; FEMALE; HUMAN; LEARNING; MALE; MEMORY; MOVEMENT PERCEPTION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; SACCADIC EYE MOVEMENT; SMOOTH PURSUIT EYE MOVEMENT;

COMPUTER SIMULATION; FEMALE; HUMANS; LEARNING; MALE; MEMORY; MOTION PERCEPTION; PSYCHOMOTOR PERFORMANCE; PURSUIT, SMOOTH; SACCADES; USER-COMPUTER INTERFACE;

EID: 84878355774     PISSN: None     EISSN: 15347362     Source Type: Journal    
DOI: 10.1167/13.1.21     Document Type: Article

References (62)

1. Assad, J.,&Maunsell, J. (1995). Neuronal correlates of inferred motion in primate posterior parietal cortex. Nature, 373(9), 518-521.
2. Barborica, A.,&Ferrera, V. P. (2003). Estimating invisible target speed from neuronal activity in monkey frontal eye field. Nature Neuroscience, 6(1), 66-74, doi:10.1038/nn990.
3. Barnes, G. R.,&Collins, C. J. S. (2008). Evidence for a link between the extra-retinal component of random- onset pursuit and the anticipatory pursuit of predictable object motion. Journal of Neurophysiology, 100(2), 1135-1146, doi:10.1152/jn.00060. 2008.
4. Barnes, G. R., Collins, C. J. S.,&Arnold, L. R. (2005). Predicting the duration of ocular pursuit in humans. Experimental Brain Research, 160(1), 10- 21, doi:10.1007/s00221-004-1981-3.
5. Battaglia, P. W., Schrater, P. R.,&Kersten, D. J. (2005). Auxiliary object knowledge influences visually-guided interception behavior. APGV '05 Proceedings of the 2nd Symposium on Applied Perception in Graphics and Visualization, 95, 145- 152. doi:10.1145/1080402.1080430.
6. Becker, W.,&Fuchs, A. (1985). Prediction in the oculomotor system: Smooth pursuit during transient disappearance of a visual target. Experimental Brain Research, 57, 562-575.
7. Bennett, S. J.,&Barnes, G. R. (2003). Human ocular pursuit during the transient disappearance of a visual target. Journal of Neurophysiology, 90(4), 2504-2520, doi:10.1152/jn.01145.2002.
8. Bennett, S. J.,&Barnes, G. R. (2004). Predictive smooth ocular pursuit during the transient disappearance of a visual target. Journal of Neurophysiology, 92(1), 578-590, doi:10.1152/jn.01188.2003.
9. Bennett, S. J.,&Barnes, G. R. (2006). Combined smooth and saccadic ocular pursuit during the transient occlusion of a moving visual object. Experimental Brain Research, 168(3), 313-321, doi:10.1007/s00221-005-0101-3.
10. Bennett, S. J., Orban de Xivry, J. J., Barnes, G. R.,&Lefèvre, P. (2007). Target acceleration can be extracted and represented within the predictive drive to ocular pursuit. Journal of Neurophysiology, 98(3), 1405-1414, doi:10.1152/jn.00132.2007.
11. Blakemore, S. J., Frith, C. D.,&Wolpert, D. M. (2001). The cerebellum is involved in predicting the sensory consequences of action. Neuroreport, 12(9), 1879-1884.
12. Brouwer, A., Brenner, E.,&Smeets, J. B. J. (2002). Perception of acceleration with short presentation times: Can acceleration be used in interception. Perception&Psychophysics, 64(7), 1160-1168.
13. de Hemptinne, C., Lefèvre, P.,&Missal, M. (2008). Neuronal bases of directional expectation and anticipatory pursuit. The Journal of Neuroscience, 28(17), 4298-4310, doi:10.1523/JNEUROSCI. 5678-07.2008.
14. Duchowski, A., Medlin, E., Cournia, N., Murphy, H., Gramopadhye, A., Nair, S. et al. (2002). 3-D eye movement analysis. Behavior Research Methods, Instruments,&Computers: A Journal of the Psychonomic Society, Inc, 34(4), 573-591.
15. Duhamel, J., Colby, C. L.,&Goldberg, M. E. (1991). The updating of the representation of visual space in parietal cortex by intended eye movements. Science, 255(1990), 1989-1991.
16. Enns, J. T.,&Lleras, A. (2008). What's next? New evidence for prediction in human vision. Trends in Cognitive Sciences, 12(9), 327-333, doi:10.1016/j. tics.2008.06.001.
17. Fautrelle, L., Pichat, C., Ricolfi, F., Peyrin, C.,&Bonnetblanc, F. (2011). Catching falling objects: The role of the cerebellum in processing sensorymotor errors that may influence updating of feedforward commands. An fMRI study. Neuroscience, 190, 135-144, doi:10.1016/j.neuroscience. 2011.06.034.
18. Ferrera, V. P.,&Barborica, A. (2010). Internally generated error signals in monkey frontal eye field during an inferred motion task. Journal of Neuroscience, 30(35), 11 612-11 623, doi:10.1523/ JNEUROSCI.2977-10.2010.
19. Findlay, J. (1981). Spatial and temporal factors in the predictive generation of saccadic eye movements. Vision Research, 21, 347-351.
20. Flanders, M.,&Cordo, P. J. (1989). Kinesthetic and visual control of a bimanual task: specification of direction and amplitude. The Journal of Neuroscience, 9(2), 447-453.
21. Fukushima, J., Akao, T., Kurkin, S., Kaneko, C.,&Fukushima, K. (2006). The vestibular-related frontal cortex and its role in smooth-pursuit eye movements and vestibular-pursuit interactions. Journal of Vestibular Research, 16, 1-22.
22. Georgopoulos, A. P., Kalaska, J. F.,&Massey, J. T. (1981). Spatial trajectories and reaction times of aimed movements: Effects of practice, uncertainty, and change in target location. Journal of Neurophysiology, 46(4), 725-743.
23. Gregory, R. L. (1980). Perceptions as hypotheses. Philosophical Transactions of the Royal Society of London, 290(1038), 181-197.
24. Hayhoe, M. M., McKinney, T., Chajka, K.,&Pelz, J. B. (2012). Predictive eye movements in natural vision. Experimental Brain Research, 217(1), 125- 36, doi:10.1007/s00221-011-2979-2.
25. Hayhoe, M., Mennie, N., Sullivan, B.,&Gorgos, K. (2005, Fall). The role of internal models and prediction in catching balls. In Technical Report FS-05-05 (C. Castelfranchi, C. Balkenius, M. Butz,&A. Ortony). Proceedings of AAAI. Symposium conducted at the meeting of AAI, Menlo Park, CA, USA.
26. Huerta, M. F., Krubitzer, L. A.,&Kass, J. H. (1987). Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. Journal of Computational Neurology, 265(3), 332-361.
27. Itti, L.,&Koch, C. (2001). Computational modelling of visual sttention. Nature Reviews Neuroscience, 2(February), 1-11.
28. Kowler, E. (1989). Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit. Vision Research, 29(9), 1049-1057.
29. Kowler, E.,&Martins, A. (1984). The effect of expectations on slow oculomotor control-IV. Anticipatory smooth eye movements depend on prior target motions. Vision Research, 24(3), 197- 210.
30. 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. Vision Research, 24(3), 197- 210.
31. Körding, K. P.,&Wolpert, D. M. (2004). Bayesian integration in sensorimotor learning. Nature, 427(6971), 244-247, doi:10.1038/nature02169.
32. Land, M. F.,&Furneaux, S. (1997). The knowledge base of the oculomotor system. Philosophical Transactions of the Royal Society of London, 352(1358), 1231-1239, doi:10.1098/rstb.1997.0105.
33. Land, M. F.,&McLeod, P. (2000). From eye movements to actions: How batsmen hit the ball. Nature Neuroscience, 3(12), 1340-1345, doi:10. 1038/81887.
34. Lopez-Moliner, J.,&Keil, M. S. (2012). People favour imperfect catching by assuming a stable world. PLOS One, 7(4), doi:10.1371/Citation.
35. Madelain, L.,&Krauzlis, R. J. (2003). Effects of learning on smooth pursuit during transient disappearance of a visual target. Journal of Neurophysiology, 90(2), 972-982, doi:10.1152/jn. 00869.2002.
36. Melcher, D.,&Colby, C. L. (2008). Trans-saccadic perception. Trends in Cognitive Sciences, 12(12), 466-473, doi:10.1016/j.tics.2008.09.003.
37. Merriam, E. P., Genovese, C. R.,&Colby, C. L. (2007). Remapping in human visual cortex. Journal of Neurophysiology, 97(2), 1738-1755, doi:10.1152/ jn.00189.2006.
38. Miall, R. C., Weir, D. J., Wolpert, D. M.,&Stein, J. F. (1993). Is the cerebellum a smith predictor. Journal of Motor Behavior, 25(3), 203-216, doi:10.1080/ 00222895.1993.9942050.
39. Milner, A.,&Goodale, M. (2008). Two visual systems re-viewed. Neuropsychologia, 46(3), 774-785, doi: 10.1016/j.neuropsychologia.2007.10.005.
40. Mrotek, L. A.,&Soechting, J. F. (2007). Predicting curvilinear target motion through an occlusion. Experimental Brain Research, 178(1), 99-114, doi: 10.1007/s00221-006-0717-y.
41. Mulliken, G. H.,&Andersen, R. A. (2009). Forward models and state estimation in posterior parietal cortex. In M. S. Gazzaniga (Ed.), The cognitive neurosciences IV (pp. 599-611). Cambridge, MA: MIT Press.
42. Nyffeler, T., Rivaud-Pechoux, S., Wattiez, N.,&Gaymard, B. (2008). Involvement of the supplementary eye field in oculomotor predictive behavior. Journal of Cognitive Neuroscience, 20(9), 1583- 1594, doi:10.1162/jocn.2008.20073.
43. Orban de Xivry, J.-J., Bennett, S. J., Lefèvre, P.,&Barnes, G. R. (2006). Evidence for synergy between saccades and smooth pursuit during transient target disappearance. Journal of Neurophysiology, 95(1), 418-427, doi:10.1152/jn.00596.2005.
44. Orban de Xivry, J. J., Missal, M.,&Lefèvre, P. (2008). A dynamic representation of target motion drives predictive smooth pursuit during target blanking. Journal of Vision, 8(15):6, 1-13, http://www.journalofvision.org/content/8/15/6, doi:10.1167/8. 15.6. [PubMed] [Article]
45. Pierrot-Deseilligny, C., Müri, R. M., Nyffeler, T.,&Milea, D. (2005). The role of the human dorsolateral prefrontal cortex in ocular motor behavior. Annals of the New York Academy of Sciences, 1039, 239-251, doi:10.1196/annals.1325.023.
46. Saunders, J. A,&Knill, D. C. (2003). Humans use continuous visual feedback from the hand to control fast reaching movements. Experimental Brain Research, 152(3), 341-352, doi:10.1007/ s00221-003-1525-2.
47. Shadmehr, R., Smith, M.,&Krakauer, J. (2010). Error correction, sensory prediction, and adaptation in motor control. Annual Review of Neuroscience, 33, 89-108, doi:10.1146/annurev-neuro-060909- 153135.
48. Shelhamer, M.,&Joiner, W. M. (2003). Saccades exhibit abrupt transition between reactive and predictive; predictive saccade sequences have longterm correlations. Journal of Neurophysiology, 90(4), 2763-2769, doi:10.1152/jn.00478.2003.
49. Shichinohe, N., Akao, T., Kurkin, S., Fukushima, J., Kaneko, C. R. S.,&Fukushima, K. (2009). Memory and decision making in the frontal cortex during visual motion processing for smooth pursuit eye movements. Neuron, 62(5), 717-732, doi:10. 1016/j.neuron.2009.05.010.
50. Simó , L. S., Krisky, C. M.,&Sweeney, J. A. (2005). Functional neuroanatomy of anticipatory behavior: Dissociation between sensory-driven and memory- driven systems. Cerebral Cortex, 15(12), 1982- 1991, doi:10.1093/cercor/bhi073.
51. Spering, M., Schütz, A. C., Braun, D. I.,&Gegenfurtner, K. R. (2011). Keep your eyes on the ball: Smooth pursuit eye movements enhance prediction of visual motion. Journal of Neurophysiology, 105(4), 1756-1767, doi:10.1152/jn.00344.2010.
52. Tabata, H., Miura, K.,&Kawano, K. (2007). Preparation for smooth pursuit eye movement based on expectation in humans. Systems and Computers in Japan, 38(6), 1-9, doi:10.1002/scj. 20677.
53. Tassinari, H., Hudson, T. E.,&Landy, M. S. (2006). Combining priors and noisy visual cues in a rapid pointing task. The Journal of Neuroscience, 26(40), 10 154-10 163, doi:10.1523/JNEUROSCI.2779-06. 2006.
54. Tseng, Y.-W., Diedrichsen, J., Krakauer, J. W., Shadmehr, R.,&Bastian, A. J. (2007). Sensory prediction errors drive cerebellum-dependent adaptation of reaching. Journal of Neurophysiology, 98(1), 54-62, doi:10.1152/jn.00266.2007.
55. Von Helmholtz, H. (1962). Helmholtz's treatise on physiological optics, James P. C. Southall (Ed.). New York: Dover Publishing.
56. Warren, W. (2006). The dynamics of perception and action. Psychological Review, 113(2), 358-389, doi: 10.1037/0033-295X.113.2.358.
57. Warren, W. H., Kim, E. E.,&Husney, R. (1987). The way the ball bounces: Visual and auditory percep- tion of elasticity and control of the bounce pass. Perception, 16, 309-336.
58. Wolpert, D. M., Miall, R. C.,&Kawato, M. (1998). Internal models in the cerebellum. Trends in Cognitive Sciences, 2(9), 338-347.
59. Xiao, Q., Barborica, A.,&Ferrera, V. P. (2007). Modulation of visual responses in macaque frontal eye field during covert tracking of invisible targets. Cerebral Cortex, 17(4), 918-928, doi:10.1093/ cercor/bhl002.
60. Zago, M., McIntyre, J., Senot, P.,&Lacquaniti, F. (2009). Visuo-motor coordination and internal models for object interception. Experimental Brain Research, 192(4), 571-604, doi:10.1007/s00221- 008-1691-3.
61. Zhang, L., Tong, M. H., Marks, T. K.,&Cottrell, G. W. (2008). SUN: A Bayesian framework for saliency using natural statistics. Journal of Vision, 8(7):32, 1-20, http://www.journalofvision.org/content/8/7/32, doi:10.1167/8.7.32. [PubMed] [Article]
62. Zhao, Q.,&Koch, C. (2011). Learning a saliency map using fixated locations in natural scenes. Journal of Vision, 11(3):9, 1-15, http://www.journalofvision.org/content/11/3/9, doi:10.1167/11.3.9. [PubMed] [Article]