The cerebellum and visual perceptual learning: Evidence from a motion extrapolation task

Cortex

Volumn 58, Issue , 2014, Pages 52-71

  Deluca, Cristina ^a   Golzar, Ashkan ^a,b   Santandrea, Elisa ^a   Lo Gerfo, Emanuele ^a   Eštočinová, Jana ^a   Moretto, Giuseppe ^c   Fiaschi, Antonio ^a,d   Panzeri, Marta ^e   Mariotti, Caterina ^e   Tinazzi, Michele ^a,d   Chelazzi, Leonardo ^a,d  

^a UNIVERSITY OF VERONA   (Italy)

^b MCGILL UNIVERSITY   (Canada)

^c BORGO TRENTO HOSPITAL   (Italy)

^d National Institute of Neuroscience   (Italy)

^e DEPARTMENT OF NEUROSURGERY   (Italy)

Author keywords

Cerebellum; Motion extrapolation; Perceptual adaptation; Perceptual learning

Indexed keywords

ADAPTATION; ADULT; ARTICLE; CEREBELLUM; CEREBELLUM INJURY; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DOUBLE DISSOCIATION; FEMALE; HUMAN; LEARNING; LEARNING CURVE; MALE; MENTAL TASK; MOTION; MOTOR CONTROL; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); PSYCHOMOTOR DISORDER; VISUAL PERCEPTUAL LEARNING; AGED; BRAIN MAPPING; MIDDLE AGED; MOVEMENT PERCEPTION; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; VISION; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADULT; AGED; BRAIN MAPPING; CEREBELLUM; FEMALE; HUMANS; LEARNING; MALE; MIDDLE AGED; MOTION PERCEPTION; NEUROPSYCHOLOGICAL TESTS; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84904619843     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2014.04.017     Document Type: Article

References (113)

1. Ahissar M., Nahum M., Nelken I., Hochstein S. Reverse hierarchies and sensory learning. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 2009, 364:285-299.
2. Albus J.S. A theory of cerebellar function. Mathematical Biosciences 1971, 10:25-61.
3. Anstis S. Footsteps and inchworms: illusions show that contrast affects apparent speed. Perception 2001, 30:785-794.
4. Balster J.H., Ramnani N. Cerebellar plasticity and the automation of first-order rules. Journal of Neuroscience 2011, 31:2305-2312.
5. Bastian A.J. Understanding sensorimotor adaptation and learning for rehabilitation. Current Opinion in Neurology 2008, 21:628-633.
6. Bastian A.J. Moving, sensing and learning with cerebellar damage. Current Opinion in Neurobiology 2011, 21:596-601.
7. Beck D.M., Kastner S. Top-down and bottom-up mechanisms in biasing competition in the human brain. Vision Research 2009, 49:1154-1165.
8. Bellebaum C., Daum I. Cerebellar involvement in executive control. Cerebellum 2007, 6:184-192.
9. Bellebaum C., Daum I. Mechanisms of cerebellar involvement in associative learning. Cortex 2011, 47:128-136.
10. Ben-Yehudah G., Guediche S., Fiez J.A. Cerebellar contributions to verbal working memory: beyond cognitive theory. Cerebellum 2007, 6:193-201.
11. Bhanpuri N.H., Okamura A.M., Bastian A.J. Active force perception depends on cerebellar function. Journal of Neurophysiology 2012, 107:1612-1620.
12. Bisley J.W., Goldberg M.E. Attention, intention, and priority in the parietal lobe. Annual Review of Neuroscience 2010, 33:1-21.
13. Blazquez P.M., Hirata Y., Highstein S.M. The vestibulo-ocular reflex as a model system for motor learning: what is the role of the cerebellum?. Cerebellum 2004, 3:188-192.
14. Bostan A.C., Dum R.P., Strick P.L. Cerebellar networks with the cerebral cortex and basal ganglia. Trends in Cognitive Sciences 2013, 17:241-254.
15. Brainard D.H. The psychophysics toolbox. Spatial Vision 1997, 10:433-436.
16. Bueti D., Lasaponara S., Cercignani M., Macaluso E. Learning about time: plastic changes and interindividual brain differences. Neuron 2012, 75:725-737.
17. Byers A., Serences J.T. Exploring the relationship between perceptual learning and top-down attentional control. Vision Research 2012, 74:30-39.
18. Carey M.R. Synaptic mechanisms of sensorimotor learning in the cerebellum. Current Opinion in Neurobiology 2011, 21:609-615.
19. Censor N., Sagi D., Cohen L.G. Common mechanisms of human perceptual and motor learning. Nature Reviews. Neuroscience 2012, 13:658-664.
20. Cerminara N.L., Apps R., Marple-Horvat D.E. An internal model of a moving visual target in the lateral cerebellum. Journal of Physiology 2009, 587(2):429-442.
21. Choi H., Watanabe T. Perceptual learning solely induced by feedback. Vision Research 2012, 61:77-82.
22. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews. Neurosciences 2002, 3:201-215.
23. Corbetta M., Shulman G.L. Spatial neglect and attention networks. Annual Review of Neuroscience 2011, 34:569-599.
24. Courchesne E., Allen G. Prediction and preparation, fundamental functions of the cerebellum. Learning & Memory. 1997, 4:1-35.
25. De Bruyn B., Orban G.A. Human velocity and direction discrimination measured with random dot patterns. Vision Research 1988, 28:1323-1335.
26. Deubel H., Wolf W., Hauske G. Adaptive gain control of saccadic eye movements. Human Neurobiology 1986, 5:245-253.
27. Dimitrov M., Grafman J., Kosseff P., Wachs J., Alway D., Higgins J., et al. Preserved cognitive processes in cerebellar degeneration. Behavioural Brain Research 1996, 79:131-135.
28. Dimitrova A., Weber J., Redies C., Kindsvater K., Maschke M., Kolb F.P., et al. MRI atlas of the human cerebellar nuclei. NeuroImage 2002, 17:240-255.
29. Dosher B.A., Lu Z.L. Hebbian reweighting on stable representations in perceptual learning. Learning & Perception 2009, 1:37-58.
30. Dow R.S., Moruzzi G. The physiology and pathology of the cerebellum 1958, University of Minnesota Press, Minneapolis.
31. Doyon J. Skill learning. International Review of Neurobiology 1997, 41:273-294.
32. Drepper J., Timmann D., Kolb F.P., Diener H.C. Non-motor associative learning in patients with isolated degenerative cerebellar disease. Brain 1999, 122:87-97.
33. Durisko C., Fiez J.A. Functional activation of the cerebellum during working memory and simple speech task. Cortex 2010, 46:896-906.
34. E K.H., Chen S.H.A., Ho M.H.R., Desmond J.E. A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Human Brain Mapping 2014, 35:593-615.
35. Fahle M. Perceptual learning and sensomotor flexibility: cortical plasticity under attentional control?. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 2009, 364:313-319.
36. Frens M.A., van Opstal A.J. Transfer of short-term adaptation in human saccadic eye movements. Experimental Brain Research 1994, 100:293-306.
37. Gao Z., van Beugen B.J., De Zeeuw C.I. Distributed synergistic plasticity and cerebellar learning. Nature Reviews. Neuroscience 2012, 13:619-635.
38. Gilbert C.D., Li W., Piech V. Perceptual learning and adult cortical plasticity. Journal of Physiology 2009, 587:2743-2751.
39. Glickstein M. What does the cerebellum really do?. Current Biology 2007, 17:R824-R827.
40. Glickstein M., Doron K. Cerebellum: connections and functions. Cerebellum 2008, 7:589-594.
41. Gold J.I., Shadlen M.N. The neural basis of decision making. Annual Review of Neuroscience 2007, 30:535-574.
42. Golla H., Tziridis K., Haarmeier T., Catz N., Barash S., Thier P. Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. European Journal of Neuroscience 2008, 27:132-144.
43. Händel B., Thier P., Haarmeier T. Visual motion perception deficits due to cerebellar lesions are paralleled by specific changes in cerebro-cortical activity. Journal of Neuroscience 2009, 29:15126-15133.
44. Hopp J.J., Fuchs A.F. The characteristics and neuronal substrate of saccadic eye movement plasticity. Progress in Neurobiology 2004, 72:27-53.
45. Ignashchenkova A., Dash S., Dicke P.W., Haarmeier T., Glickstein M., Thier P. Normal spatial attention but impaired saccades and visual motion perception after lesions of the monkey cerebellum. Journal of Neurophysiology 2009, 102:3156-3168.
46. Imamizu H., Miyauchi S., Tamada T., Sasaki Y., Takino R., Pütz B., et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 2000, 403:192-195.
47. Ioffe M.E., Chernikova L.A., Ustinova K.I. Role of cerebellum in learning postural tasks. Cerebellum 2007, 6:87-94.
48. Ito M. Cerebellar circuitry as a neuronal machine. Progress in Neurobiology 2006, 78:272-303.
49. Ito M. Control of mental activities by internal models in the cerebellum. Nature Reviews. Neuroscience 2008, 9:304-313.
50. Ivry R.B., Spencer R.M. The neural representation of time. Current Opinion in Neurobiology 2004, 14:225-232.
51. Karni A., Bertini G. Learning perceptual skills: behavioral probes into adult cortical plasticity. Current Opinion in Neurobiology 1997, 7:530-535.
52. Krakauer J.W., Shadmehr R. Consolidation of motor memory. Trends in Neurosciences 2006, 29:58-64.
53. Lamont M.G., Weber J.T. The role of calcium in synaptic plasticity and motor learning in the cerebellar cortex. Neuroscience & Biobehavioral Reviews 2012, 36:1153-1162.
54. Language cognition and the cerebellum: grappling with the enigma [Special issue]. Alan Beaton & Peter Marïen (Guest Eds.). (2010). Cortex, 46, 811-946.
55. Law C.T., Gold J.I. Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area. Nature Neuroscience 2008, 11:505-513.
56. Leiner H.C., Leiner A.L., Dow R.S. Reappraising the cerebellum: what does the hindbrain contribute to the forebrain?. Behavioral Neuroscience 1989, 103:998-1008.
57. Leiner H.C., Leiner A.L., Dow R.S. The human cerebro-cerebellar system: its computing, cognitive, and language skills. Behavioral Brain Research 1991, 44:113-128.
58. Levitt H. Transformed up-down methods in psychoacoustics. Journal of the Acoustical Society of America 1971, 49:467+.
59. Lu Z.L., Hua T., Huang C.B., Zhou Y., Dosher B.A. Visual perceptual learning. Neurobiology of Learning and Memory 2011, 95:145-151.
60. Makin A.D., Poliakoff E., Chen J., Stewart A.J. The effect of previously viewed velocities on motion extrapolation. Vision Research 2008, 48:1884-1893.
61. Manto M., Bower J.M., Conforto A.B., Delgado-García J.M., da Guarda S.N., Gerwig M., et al. Consensus paper: roles of the cerebellum in motor control-the diversity of ideas on cerebellar involvement in movement. Cerebellum 2012, 11:457-487.
62. Marr D. A theory of cerebellar cortex. Journal of Physiology 1969, 202:437-470.
63. Marvel C.L., Desmond J.E. The contributions of cerebro-cerebellar circuitry to executive verbal working memory. Cortex 2010, 46:880-895.
64. McKee S.P., Nakayama K. The detection of motion in the peripheral visual field. Vision Research 1984, 24:25-32.
65. McLaughlin S.C. Parametric adjustment in saccadic eye movements. Perception & Psychophysics 1967, 2:359-362.
66. Mednick S.C., Arman A.C., Boynton G.M. The time course and specificity of perceptual deterioration. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:3881-3885.
67. Mednick S.C., Nakayama K., Cantero J.L., Atienza M., Levin A.A., Pathak N., et al. The restorative effect of naps on perceptual deterioration. Nature Neuroscience 2002, 5:677-681.
68. Mesulam M.M. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 1999, 354:1325-1346.
69. Miall R.C., Weir D.J., Wolpert D.M., Stein J.F. Is the cerebellum a smith predictor?. Journal of Motor Behavior 1993, 25:203-216.
70. Molinari M., Chiricozzi F.R., Clausi S., Tedesco A.M., De Lisa M., Leggio M.G. Cerebellum and detection of sequences, from perception to cognition. Cerebellum 2008, 7:611-615.
71. Murdoch B.E. The cerebellum and language: historical perspective and review. Cortex 2010, 46:858-868.
72. Noudoost B., Chang M.H., Steinmetz N.A., Moore T. Top-down control of visual attention. Current Opinion in Neurobiology 2010, 20:183-190.
73. O'Reilly J.X., Mesulam M.M., Nobre A.C. The cerebellum predicts the timing of perceptual events. Journal of Neuroscience 2008, 28:2252-2260.
74. Paulin M.G. The role of the cerebellum in motor control and perception. Brain Behavior and Evolution. 1993, 41:39-50.
75. Pelli D.G. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spatial Vision 1997, 10:437-442.
76. Prsa M., Thier P. The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning. European Journal of Neuroscience 2011, 33:2114-2128.
77. Rabe K., Livne O., Gizewski E.R., Aurich V., Beck A., Timmann D., et al. Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. Journal of Neurophysiology 2009, 101:1961-1971.
78. Ramnani N. The primate cortico-cerebellar system: anatomy and function. Nature Reviews. Neurosciences 2006, 7:511-522.
79. Raymond J.L., Lisberger S.G., Mauk M.D. The cerebellum: a neuronal learning machine?. Science 1996, 272:1126-1131.
80. Roelfsema P.R., van Ooyen A., Watanabe T. Perceptual learning rules based on reinforcers and attention. Trends in Cognitive Sciences 2010, 14:64-71.
81. Rorden C., Brett M. Stereotaxic display of brain lesions. Behavioural Neurology 2000, 12:191-200.
82. Roth M.J., Synofzik M., Lindner A. The cerebellum optimizes perceptual predictions about external sensory events. Current Biology 2013, 23:930-935.
83. Rothwell J. The cerebellum. Control of human voluntary movement 1994, Chapman & Hall. 2nd ed.
84. Salmi J., Pallesen K.J., Neuvonen T., Brattico E., Korvenoja A., Salonen O., et al. Cognitive and motor loops of the human cerebro-cerebellar system. Journal of Cognitive Neuroscience 2010, 22:2663-2676.
85. Sasaki Y., Nanez J.E., Watanabe T. Advances in visual perceptual learning and plasticity. Nature Reviews. Neurosciences 2010, 11:53-60.
86. Schiltz C., Bodart J.M., Dubois S., Dejardin S., Michel C., Roucoux A., et al. Neuronal mechanisms of perceptual learning: changes in human brain activity with training in orientation discrimination. NeuroImage 1999, 9:46-62.
87. Schmahmann J.D. An emerging concept: the cerebellar contribution to higher function. Archives of Neurology 1991, 48:1178-1187.
88. Schmahmann J.D. Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends in Cognitive Sciences 1998, 2:362-371.
89. Schmamann J.D. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychology Review 2010, 20:236-260.
90. Schmahmann J.D., MacMore J., Vangel M. Cerebellar stroke without motor deficit: clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience 2009, 162:852-861.
91. Schmitz-Hübsch T., du Montcel S.T., Baliko L., Berciano J., Boesch S., Depondt C., et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology 2006, 66:1717-1720.
92. Seitz A.R., Kim R., Shams L. Sound facilitates visual learning. Current Biology 2006, 16:1422-1427.
93. Serences J.T., Yantis S. Selective visual attention and perceptual coherence. Trends in Cognitive Sciences 2006, 10:38-45.
94. Smith A.C., Frank L.M., Wirth S., Yanike M., Hu D., Kubota Y., et al. Dynamic analysis of learning in behavioral experiments. Journal of Neuroscience 2004, 24:447-461.
95. Smith M.A., Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. Journal of Neurophysiology 2005, 93:2809-2821.
96. Sokolov A.N., Ehrenstein W.H., Pavlova M.A., Cavonius C.R. Motion extrapolation and velocity transposition. Perception 1997, 26:875-889.
97. Stoodley C.J. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum 2012, 11:352-365.
98. Stoodley C.J., Schmahmann J.D. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 2010, 46:831-844.
99. Stoodley C.J., Valera E.M., Schmahmann J.D. Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. NeuroImage 2012, 59:1560-1570.
100. Strata P., Scelfo B., Sacchetti B. Involvement of cerebellum in emotional behavior. Physiological Research 2011, 60:S39-S48.
101. Strick P.L., Dum R.P., Fiez J.A. Cerebellum and nonmotor function. Annual Review of Neuroscience 2009, 32:413-434.
102. Sultan F., Augath M., Hamodeh S., Murayama Y., Oeltermann A., Rauch A., et al. Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks. Nature Communications 2012, 3:924.
103. Synofzik M., Lindner A., Thier P. The cerebellum updates predictions about the visual consequences of one's behavior. Current Biology 2008, 18:814-818.
104. Thach W.T. A role for the cerebellum in learning movement coordination. Neurobiology of Learning and Memory 1998, 70:177-188.
105. Timmann D., Daum I. Cerebellar contributions to cognitive functions: a progress report after two decades of research. Cerebellum 2007, 6:159-162.
106. Timmann D., Daum I. How consistent are cognitive impairments in patients with cerebellar disorders?. Behavioural Neurology 2010, 23:81-100.
107. Timmann D., Drepper J., Frings M., Maschke M., Richter S., Gerwig M., et al. The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex 2010, 46:845-857.
108. Tseng Y.W., Diedrichsen J., Krakauer J.W., Shadmehr R., Bastian A.J. Sensory prediction errors drive cerebellum-dependent adaptation of reaching. Journal of Neurophysiology 2007, 98:54-62.
109. Vaina L.M., Belliveau J.W., des Roziers E.B., Zeffiro T.A. Neural systems underlying learning and representation of global motion. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:12657-12662.
110. Watamaniuk S.N. The predictive power of trajectory motion. Vision Research 2005, 45:2993-3003.
111. Watamaniuk S.N.J., McKee S.P. 'Seeing' motion behind occluders. Nature 1995, 377:729-730.
112. Werner S., Bock O., Gizewski E.R., Schoch B., Timmann D. Visuomotor adaptive improvement and aftereffects are impaired differentially following cerebellar lesions in SCA and PICA territory. Experimental Brain Research 2010, 201:429-439.
113. Werner S., Bock O., Timmann D. The effect of cerebellar cortical degeneration on adaptive plasticity and movement control. Experimental Brain Research 2009, 193:189-196.