Saccade adaptation as a model of flexible and general motor learning

Experimental Eye Research

Volumn 114, Issue , 2013, Pages 6-15

  Herman, James P ^a   Blangero, Annabelle ^a   Madelain, Laurent ^b,c   Khan, Afsheen ^a   Harwood, Mark R ^a  

^a CITY COLLEGE OF NEW YORK   (United States)

^b UNIV LILLE   (France)

^c CNRS   (France)

Author keywords

Motor learning; Saccade adaptation; Saccadic eye movements

Indexed keywords

ADAPTATION; ARM MOVEMENT; ARTICLE; HUMAN; INJURY; LEARNING; PRIORITY JOURNAL; REINFORCEMENT; RETINA; SACCADIC EYE MOVEMENT; VISUAL FEEDBACK;

MOTOR LEARNING; SACCADE ADAPTATION; SACCADIC EYE MOVEMENTS;

ADAPTATION, OCULAR; FEEDBACK, SENSORY; HUMANS; LEARNING; PSYCHOMOTOR PERFORMANCE; SACCADES;

EID: 84881241632     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.04.001     Document Type: Article

References (106)

1. Abel L.A., Schmidt D., Dell'Osso L.F., Daroff R.B. Saccadic system plasticity in humans. Ann. Neurol. 1978, 4:313-318.
2. Alahyane N., Pélisson D. Eye position specificity of saccadic adaptation. Invest. Ophthalmol. Vis. Sci. 2004, 45:123-130.
3. Alahyane N., Pélisson D. Long-lasting modifications of saccadic eye movements following adaptation induced in the double-step target paradigm. Learn. Mem. 2005, 12:433-443.
4. Albano J.E., King W.M. Rapid adaptation of saccadic amplitude in humans and monkeys. Invest. Ophthalmol. Vis. Sci. 1989, 30:1883-1893.
5. Bahcall D.O., Kowler E. The control of saccadic adaptation: implications for the scanning of natural visual scenes. Vis. Res. 2000, 40:2779-2796.
6. Beaton K., Wong A., Shelhamer M. Context-specific Adaptation of Sensorimotor Responses 2010, Society for Neuroscience, San Diego.
7. Berniker M., Körding K. Estimating the sources of motor errors for adaptation and generalization. Nat. Neurosci. 2008, 11:1454-1461.
8. Bridgeman B., Hendry D., Stark L. Failure to detect displacement of the visual world during saccadic eye movements. Vis. Res. 1975, 15:719-722.
9. Bryan C.P. The Papyrus Ebers 1930, Geoffrey Bles, London.
10. Castet E., Jeanjean S., Montagnini A., Laugier D., Masson G.S. Dynamics of attentional deployment during saccadic programming. J.Vis. 2006, 6:196-212.
11. Castet E., Masson G.S. Motion perception during saccadic eye movements. Nat. Neurosci. 2000, 3:177-183.
12. Cavanagh P., Hunt A.R., Afraz A., Rolfs M. Visual stability based on remapping of attention pointers. Trends Cogn. Sci. 2010, 14:147-153.
13. Chaturvedi V., van Gisbergen J.A. Specificity of saccadic adaptation in three-dimensional space. Vis. Res. 1997, 37:1367-1382.
14. Chen-Harris H., Joiner W.M., Ethier V., Zee D.S., Shadmehr R. Adaptive control of saccades via internal feedback. J.Neurosci. 2008, 28:2804-2813.
15. Collins T. Extraretinal signal metrics in multiple-saccade sequences. J.Vis. 2010, 10(14).
16. Collins T., Wallman J. The relative importance of retinal error and prediction in saccadic adaptation. J.Neurophysiol. 2012, 107:3342-3348.
17. Collins T., Rolfs M., Deubel H., Cavanagh P. Post-saccadic location judgments reveal remapping of saccade targets to non-foveal locations. J.Vis. 2009, 9:1-9.
18. Collins T., Vergilino-Perez D., Beauvillain C., Doré-Mazars K. Saccadic adaptation depends on object selection: evidence from between- and within-object saccadic eye movements. Brain Res. 2007, 1152:95-105.
19. Criscimagna-Hemminger S.E., Bastian A.J., Shadmehr R. Size of error affects cerebellar contributions to motor learning. J.Neurophysiol. 2010, 103:2275-2284.
20. Dam G., Kording K., Wei K. Credit assignment during movement reinforcement learning. PLoS ONE 2013, 8(2):e55352. 10.1371/journal.pone.0055352.
21. Deubel H. Adaptivity of gain and direction in oblique saccades. Eye Movements: Form Physiology to Cognition 1987, 181-190. Elsevier Science Publishers B.V, Amsterdam. J.K. O'Regan, A. Levy-Schoen (Eds.).
22. Deubel H. Adaptive control of saccade metrics. Presbyopia Research: from Molecular Biology to Visual Adaptation 1991, 93-100. Springer, New York. G. Obrecht, L. Stark (Eds.).
23. Deubel H. Is saccadic adaptation context-specific?. Eye Movement Research: Mechanisms, Processes and Applications 1995, Elsevier Science. J.M. Findlay, R.W. Kentridge, R. Walker (Eds.).
24. Deubel H. Separate adaptive mechanisms for the control of reactive and volitional saccadic eye movements. Vis. Res. 1995, 35:3529-3540.
25. Deubel H. 2 separate mechanisms for the adaptive control of reactive, volitional, and memory-guided saccadic eye movements. Attention and Performance XVII: Cognitive Regulation of Performance: Interaction of Theory and Application 1999, 814. A Bradford Book. D. Gopher, A. Koriat (Eds.).
26. Deubel H. Localization of targets across saccades: role of landmark objects. Vis. Cogn. 2004, 11:173-202.
27. Deubel H., Wolf W., Hauske G. Adaptive gain control of saccadic eye movements. Hum. Neurobiol. 1986, 5:245-253.
28. Deubel H., Schneider W.X. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vis. Res. 1996, 36:1827-1837.
29. Deubel H., Schneider W.X., Bridgeman B. Postsaccadic target blanking prevents saccadic suppression of image displacement. Vis. Res. 1996, 36:985-996.
30. Deubel H., Koch C., Bridgeman B. Landmarks facilitate visual space constancy across saccades and during fixation. Vis. Res. 2010, 50:249-259.
31. Ditterich J., Eggert T., Straube A. Does visual background information influence saccade adaptation. Current Oculomotor Research: Physiological and Psychological Aspects 1999, 71-80. Springer, New York. W. Becker, H. Deubel, T. Mergner (Eds.).
32. Ditterich J., Eggert T., Straube A. The role of the attention focus in the visual information processing underlying saccadic adaptation. Vis. Res. 2000, 40:1125-1134.
33. Erkelens C.J., Hulleman J. Selective adaptation of internally triggered saccades made to visual targets. Exp. Brain Res. 1993, 93:157-164.
34. Ethier V., Zee D.S., Shadmehr R. Spontaneous recovery of motor memory during saccade adaptation. J.Neurophysiol. 2008, 99:2577-2583.
35. Ethier V., Zee D.S., Shadmehr R. Changes in control of saccades during gain adaptation. J.Neurosci. 2009, 28:13929-13937.
36. Fitzgibbon E.J., Goldberg M.E., Segraves M.A. Short Term Saccadic Adaptation in the Monkey 1986, Oxford, Eng, Pergamon.
37. Frens M.A., Van Opstal A.J. Monkey superior colliculus activity during short-term saccadic adaptation. Brain Res. Bull. 1997, 43:473-483.
38. Fuchs A.F., Reiner D., Pong M. Transfer of gain changes from targeting to other types of saccade in the monkey: constraints on possible sites of saccadic gain adaptation. J.Neurophysiol. 1996, 76:2522-2535.
39. Fujita M., Amagai A., Minakawa F., Aoki M. Selective and delay adaptation of human saccades. Brain Res. Cogn. Brain Res. 2002, 13:41-52.
40. Gaveau V., Alahyane N., Salemme R., Desmurget M. Self-generated saccades do not modify the gain of adapted reactive saccades. Exp. Brain Res. 2005, 162:526-531.
41. Harris C.M. Does saccadic undershoot minimize saccadic flight-time? A Monte-Carlo study. Vis. Res. 1995, 35:691-701.
42. Hatada Y., Rossetti Y., Miall R.C. Long-lasting aftereffect of a single prism adaptation: shifts in vision and proprioception are independent. Exp. Brain Res. 2006, 173:415-424.
43. Havermann K., Lappe M. The influence of the consistency of postsaccadic visual errors on saccadic adaptation. J.Neurophysiol. 2010, 103:3302-3310.
44. Henson D.B. Corrective saccades: effects of altering visual feedback. Vis. Res. 1978, 18:63-67.
45. Herman J.P., Harwood M.R., Wallman J. Saccade adaptation specific to visual context. J.Neurophysiol. 2009, 101:1713-1721.
46. Herman J.P., Cloud C.P., Wallman J. End-point variability is not noise in saccade adaptation. PLoS ONE 2013, 8(3):e59731. 10.1371/journal.pone.0059731.
47. Hoffman J.E., Subramaniam B. The role of visual attention in saccadic eye movements. Percept Psychophys. 1995, 57:787-795.
48. Hopp J.J., Fuchs A.F. Investigating the site of human saccadic adaptation with express and targeting saccades. Exp. Brain Res. 2002, 144:538-548.
49. Hopp J.J., Fuchs A.F. The characteristics and neuronal substrate of saccadic eye movement plasticity. Prog. Neurobiol. 2004, 72:27-53.
50. Huang V.S., Shadmehr R. Persistence of motor memories reflects statistics of the learning event. J.Neurophysiol. 2009, 102:931-940.
51. Joiner W.M., Smith M.A. Long-term retention explained by a model of short-term learning in the adaptive control of reaching. J.Neurophysiol. 2008, 100:2948-2955.
52. Kagerer F.A., Contreras-Vidal J.L., Stelmach G.E. Adaptation to gradual as compared with sudden visuo-motor distortions. Exp. Brain Res. 1997, 115:557-561.
53. Klassen J., Tong C., Flanagan J.R. Learning and recall of incremental kinematic and dynamic sensorimotor transformations. Exp. Brain Res. 2005, 164:250-259.
54. Kowler E., Anderson E., Dosher B., Blaser E. The role of attention in the programming of saccades. Vis. Res. 1995, 35:1897-1916.
55. Kommerell G., Olivier D., Theopold H. Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. Invest. Ophthalmol. 1976, 15:657-660.
56. Körding K.P., Tenenbaum J.B., Shadmehr R. The dynamics of memory as a consequence of optimal adaptation to a changing body. Nat. Neurosci. 2007, 10:779-786.
57. Kroller J., De Graaf J.B., Prablanc C., Pélisson D. Effects of short-term adaptation of saccadic gaze amplitude on hand-pointing movements. Exp. Brain Res. 1999, 124:351-362.
58. Lauwereyns J., Watanabe K., Coe B., Hikosaka O. Aneural correlate of response bias in monkey caudate nucleus. Nature 2002, 418:413-417.
59. Lewis R.F., Zee D.S., Hayman M.R., Tamargo R.J. Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles. Exp. Brain Res. 2001, 141:349-358.
60. Madelain L., Champrenaut L., Chauvin A. Control of sensorimotor variability by consequences. J.Neurophysiol. 2007, 98:2255-2265.
61. Madelain L., Harwood M.R., Herman J.P., Wallman J. Saccade adaptation is unhampered by distractors. J.Vis. 2010, 10:1-14.
62. Madelain L., Paeye C., Wallman J. Modification of saccadic gain by reinforcement. J.Neurophysiol. 2011, 106:219-232.
63. Madelain L., Herman J.P., Harwood M.R. Saccade adaptation goes for the goal. J.Vis. 2013, 13(4):9.
64. May M.T. Galen on the Usefulness of the Parts of the Body 1968, Cornell University Press, Ithaca.
65. Mazzoni P., Krakauer J.W. An implicit plan overrides an explicit strategy during visuomotor adaptation. J.Neurosci. 2006, 26:3642-3645.
66. McKelvie P., Friling R., Davey K., Kowal L. Changes as the result of ageing in extraocular muscles: a post-mortem study. Aust. N. Z. J. Ophthalmol. 1999, 27(6):420-425.
67. McFadden S.A., Khan A., Wallman J. Gain adaptation of exogenous shifts of visual attention. Vis. Res. 2002, 42:2709-2726.
68. McLaughlin S.C. Parametric adjustment in saccadic eye movements. Perception Psychophys. 1967, 2:359-362.
69. Michel C., Pisella L., Prablanc C., Rode G., Rossetti Y. Enhancing visuomotor adaptation by reducing error signals: single-step (aware) versus multiple-step (unaware) exposure to wedge prisms. J.Cognitive Neurosci. 2007, 19:341-350.
70. Miller J.E. Aging changes in extraocular muscles. Basic Mechanisms of Ocular Motility and Their Clinical Implications 1975, 47-61. Pergamon Press, Ltd, Oxford.
71. Miller J.M., Anstis T., Templeton W.B. Saccadic plasticity: parametric adaptive control by retinal feedback. J.Exp. Psychology. Hum. Perception Perform. 1981, 7:356-366.
72. Müller-Höcker J., Schneiderbanger K., Stefani F.H., Kadenbach B. Progressive loss of cytochrome c oxidase in the human extraocular muscles in ageing-a cytochemical-immunohistochemical study. Mutat. Res. 1992, 275(3-6):115-124.
73. Munoz D.P., Broughton J.R., Goldring J.E., Armstrong I.T. Age-related performance of human subjects on saccadic eye movement tasks. Exp. Brain Res. 1998, 121:391-400.
74. Noto C.T., Robinson F.R. Visual error is the stimulus for saccade gain adaptation. Brain Res. Cogn. Brain Res. 2001, 12:301-305.
75. Optican L.M., Robinson D.A. Cerebellar-dependent adaptive control of primate saccadic system. J.Neurophysiol. 1980, 44:1058-1076.
76. Paeye C., Madelain L. Reinforcing saccadic amplitude variability. J.Exp. Anal. Behav. 2011, 95:149-162.
77. Panouillères M., Gaveau V., Socasau C., Urquizar C., Pélisson D. Brain processing of visual information during fast eye movements maintains motor performance. PLoS ONE 2013, 8(1).
78. Pélisson D., Alahyane N., Panouillères M., Tilikete C. Sensorimotor adaptation of saccadic eye movements. Neurosci. Biobehavioral Rev. 2010, 34:1103-1120.
79. Porterfield W. An essay concerning the motions of our eyes. Part I. Of their external motions. Edinburgh Med. Essays Observations 1737, 4:124-294.
80. Robinson F.R., Noto C., Watanabe S. Effect of visual background on saccade adaptation in monkeys. Vis. Res. 2000, 40:2359-2367.
81. Robinson F.R., Fuchs A., Noto C. Cerebellar influences on saccade plasticity. Ann. N. Y. Acad. Sci. 2002, 956:155-163.
82. Robinson F.R., Noto C.T., Bevans S.E. Effect of visual error size on saccade adaptation in monkey. J.Neurophysiol. 2003, 90:1235-1244.
83. Scudder C.A., Batourina E.Y., Tunder G.S. Comparison of two methods of producing adaptation of saccade size and implications for the site of plasticity. J.Neurophysiol. 1998, 79:704-715.
84. Semmlow J.L., Gauthier G.M., Vercher J.L. Mechanisms of short-term saccadic adaptation. J.Exp. Psychol. Hum. Percept Perform. 1989, 15:249-258.
85. Shadmehr R., Smith M., Krakauer J.W. Error correction, sensory prediction, and adaptation in motor control. Annu. Rev. Neurosci. 2010, 33:89-108.
86. Shafer J.L., Noto C.T., Fuchs A.F. Temporal characteristics of error signals driving saccadic gain adaptation in the macaque monkey. J.Neurophysiol. 2000, 84:88-95.
87. Shelhamer M., Clendaniel R. Sensory, motor, and combined contexts for context specific adaptation of saccade gain in humans. Neurosci. Lett. 2002, 332:200-204.
88. Shelhamer M., Clendaniel R.A. Context-specific adaptation of saccade gain. Exp. Brain Res. 2002, 146:441-450.
89. Smith E.L. Optical treatment strategies to slow myopia progression: effects of the visual extent of the optical treatment zone. Exp Eye Res. 2013, 114:77-88. 10.1016/j.exer.2012.11.019.
90. Sommer M.A., Wurtz R.H. Brain circuits for internal monitoring of movements. Annu. Rev. Neurosci. 2008, 31:317-338.
91. Srimal R., Diedrichsen J., Ryklin E.B., Curtis C.E. Obligatory adaptation of saccade gains. J.Neurophysiol. 2008, 99:1554-1558.
92. Straube A., Deubel H. Rapid gain adaptation affects the dynamics of saccadic eye movements in humans. Vis. Res. 1995, 35:3451-3458.
93. Straube A., Fuchs A.F., Usher S., Robinson F.R. Characteristics of saccadic gain adaptation in rhesus macaques. J.Neurophysiol. 1997, 77:874-895.
94. Takikawa Y., Kawagoe R., Itoh H., Nakahara H., Hikosaka O. Modulation of saccadic eye movements by predicted reward outcome. Exp. Brain Res. 2002, 142:284-291.
95. Todorov E. Stochastic optimal control and estimation methods adapted to the noise characteristics of the sensorimotor system. Neural Comput. 2005, 17(5):1084-1108.
96. Vergilino-Perez D., Findlay J.M. Between-object and within-object saccade programming in a visual search task. Vis. Res. 2006, 46:2204-2216.
97. Wallman J., Fuchs A.F. Saccadic gain modification: visual error drives motor adaptation. J.Neurophysiol. 1998, 80:2405-2416.
98. Warabi T., Kase M., Kato T. Effect of aging on the accuracy of visually guided saccadic eye movement. Ann. Neurol. 1984, 16:449-454.
99. Watanabe K., Lauwereyns J., Hikosaka O. Effects of motivational conflicts on visually elicited saccades in monkeys. Exp. Brain Res. 2003, 152:361-736.
100. Wei K., Körding K. Relevance of error: what drives motor adaptation?. J.Neurophysiol. 2009, 101:655-664.
101. Wolpert D.M., Kawato M. Multiple paired forward and inverse models for motor control. Neural Netw. 1998, 11:1317-1329.
102. Wong A.L., Shelhamer M. Sensorimotor adaptation error signals are derived from realistic predictions of movement outcomes. J.Neurophysiol. 2011, 105:1130-1140.
103. Wong A.L., Shelhamer M. Saccade adaptation improves in response to a gradually introduced stimulus perturbation. Neurosci. Lett. 2011, 500:207-211.
104. Xu-Wilson M., Zee D.S., Shadmehr R. The intrinsic value of visual information affects saccade velocities. Exp. Brain Res. 2009, 196:475-481.
105. Zee D.S., Optican L.M., Cook J.D., Robinson D.A., Engel W.K. Slow saccades in spinocerebellar degeneration. Arch. Neurol. 1976, 33:243-251.
106. Zimmermann E., Lappe M. Eye position effects in oculomotor plasticity and visual localization. J.Neurosci. 2011, 31:7341-7348.