The cerebellum: A neuronal learning machine?

Science

Volumn 272, Issue 5265, 1996, Pages 1126-1131

  Raymond, Jennifer L ^a   Lisberger, Stephen G ^a   Mauk, Michael D ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEHAVIOR; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CONDITIONING; EYELID; LEARNING; MOTOR PERFORMANCE; NERVE CELL; NERVE CELL PLASTICITY; PRIORITY JOURNAL; VESTIBULOOCULAR REFLEX;

EID: 0029942861     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5265.1126     Document Type: Article

References (91)

1. J. S. Albus, Math. Biosci. 10, 25 (1971); D. Marr, J. Physiol. (London) 202, 437 (1969); G. S. Brindley, Int. Brain Res. Organ. Bull. 3, 30 (1964).
2. J. S. Albus, Math. Biosci. 10, 25 (1971); D. Marr, J. Physiol. (London) 202, 437 (1969); G. S. Brindley, Int. Brain Res. Organ. Bull. 3, 30 (1964).
3. J. S. Albus, Math. Biosci. 10, 25 (1971); D. Marr, J. Physiol. (London) 202, 437 (1969); G. S. Brindley, Int. Brain Res. Organ. Bull. 3, 30 (1964).
4. M. Ito, Brain Res. 40, 80 (1972).
5. S. duLac, J. L. Raymond, T. J. Sejnowski, S. G. Lisberger, Annu. Rev. Neurosci. 18, 409 (1995).
6. R. F. Thompson and D. J. Krupa, ibid. 17, 519 (1994).
7. W. T. Thach, H. P. Goodkin, J. G. Keating, ibid. 15, 403 (1992).
8. For details, see J. C. Eccles, M. Ito, J. Szentagothai, The Cerebellum as a Neuronal Machine (Springer-Verlag, Berlin, 1967); M. Ito, The Cerebellum and Neural Control (Raven, New York, 1984).
9. For details, see J. C. Eccles, M. Ito, J. Szentagothai, The Cerebellum as a Neuronal Machine (Springer-Verlag, Berlin, 1967); M. Ito, The Cerebellum and Neural Control (Raven, New York, 1984).
10. R. Llinas and J. P. Welsh, Curr. Opin. Neurobiol. 3, 956 (1993); R. B. Ivry and J. V. Saldo, ibid. 2, 212 (1992); S. W. Keele and R. B. Ivry, Ann. N.Y. Acad. Sci. 608, 179 (1990); R. B. Ivry, S. W. Keele, J. V. Baldo, Exp. Brain Res. 73, 167 (1988).
11. R. Llinas and J. P. Welsh, Curr. Opin. Neurobiol. 3, 956 (1993); R. B. Ivry and J. V. Saldo, ibid. 2, 212 (1992); S. W. Keele and R. B. Ivry, Ann. N.Y. Acad. Sci. 608, 179 (1990); R. B. Ivry, S. W. Keele, J. V. Baldo, Exp. Brain Res. 73, 167 (1988).
12. R. Llinas and J. P. Welsh, Curr. Opin. Neurobiol. 3, 956 (1993); R. B. Ivry and J. V. Saldo, ibid. 2, 212 (1992); S. W. Keele and R. B. Ivry, Ann. N.Y. Acad. Sci. 608, 179 (1990); R. B. Ivry, S. W. Keele, J. V. Baldo, Exp. Brain Res. 73, 167 (1988).
13. R. Llinas and J. P. Welsh, Curr. Opin. Neurobiol. 3, 956 (1993); R. B. Ivry and J. V. Saldo, ibid. 2, 212 (1992); S. W. Keele and R. B. Ivry, Ann. N.Y. Acad. Sci. 608, 179 (1990); R. B. Ivry, S. W. Keele, J. V. Baldo, Exp. Brain Res. 73, 167 (1988).
14. R. F. Thompson, Science 233, 941 (1986).
15. S. G. Lisberger, F. A. Miles, D. S. Zee, J. Neurophysiol 52, 1140 (1984).
16. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
17. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
18. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
19. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
20. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
21. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
22. D. A. Robinson, ibid. 39, 954 (1976); N. H. Barmack and V. E. Pettorosi, ibid. 53, 481 (1985); S. Nagao, Exp. Brain Res. 53, 152 (1983); I. Daum et al., Behav. Neurosci. 107, 748 (1993); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 60, 87 (1985); ibid., p. 99; C. H. Yeo and M. J. Hardiman, ibid. 88, 623 (1992).
23. J. P. Welsh and J. A. Harvey, J. Neurosci. 9, 299 (1989); D. A. McCormick and R. F. Thompson, Science 223, 296 (1984).
24. J. P. Welsh and J. A. Harvey, J. Neurosci. 9, 299 (1989); D. A. McCormick and R. F. Thompson, Science 223, 296 (1984).
25. D. A. McCormick and R. F. Thompson, J. Neurosci. 4, 2811 (1984).
26. D. A. McCormick et al., Bull. Psychon. Soc. 18, 103 (1981).
27. S. P. Perrett, B. P. Ruiz, M. D. Mauk, ibid. 13, 1708 (1993).
28. S. P. Perrett and M. D. Mauk, ibid. 15, 2074 (1995).
29. K. S. Garcia and M. D. Mauk, Soc. Neurosci. Abstr. 21, 1222 (1995).
30. The anterior lobe is one region of the cerebellar cortex involved in eyelid conditioning; however, other regions of the cerebellar cortex may also be involved.
31. In monkeys, learning is abolished by lesions that include the floccular complex as well as some of the dorsal paraflocculus (9). In rabbits, learning is abolished by lesions of the flocculus, which constitutes most of the floccular complex in this species [S. Nagao, Exp. Brain Res. 53, 36 (1983)]. The primate floccular complex includes substantial amounts of tissue from the flocculus and the ventral paraflocculus, and it remains a matter of contention whether one or both of these structures constitute the relevant part of the floccular complex for motor learning in the VOR [N. M. Gerrits and J. Voogd, Exp. Brain Res. Suppl. 17, 26 (1989); M. Ito, Nature 363, 24 (1993); S. G. Lisberger and T. J. Sejnowski, ibid., p. 25]. Electrical recordings cited in (37) give additional support for the idea that the floccular complex is important for motor learning in the VOR.
32. In monkeys, learning is abolished by lesions that include the floccular complex as well as some of the dorsal paraflocculus (9). In rabbits, learning is abolished by lesions of the flocculus, which constitutes most of the floccular complex in this species [S. Nagao, Exp. Brain Res. 53, 36 (1983)]. The primate floccular complex includes substantial amounts of tissue from the flocculus and the ventral paraflocculus, and it remains a matter of contention whether one or both of these structures constitute the relevant part of the floccular complex for motor learning in the VOR [N. M. Gerrits and J. Voogd, Exp. Brain Res. Suppl. 17, 26 (1989); M. Ito, Nature 363, 24 (1993); S. G. Lisberger and T. J. Sejnowski, ibid., p. 25]. Electrical recordings cited in (37) give additional support for the idea that the floccular complex is important for motor learning in the VOR.
33. In monkeys, learning is abolished by lesions that include the floccular complex as well as some of the dorsal paraflocculus (9). In rabbits, learning is abolished by lesions of the flocculus, which constitutes most of the floccular complex in this species [S. Nagao, Exp. Brain Res. 53, 36 (1983)]. The primate floccular complex includes substantial amounts of tissue from the flocculus and the ventral paraflocculus, and it remains a matter of contention whether one or both of these structures constitute the relevant part of the floccular complex for motor learning in the VOR [N. M. Gerrits and J. Voogd, Exp. Brain Res. Suppl. 17, 26 (1989); M. Ito, Nature 363, 24 (1993); S. G. Lisberger and T. J. Sejnowski, ibid., p. 25]. Electrical recordings cited in (37) give additional support for the idea that the floccular complex is important for motor learning in the VOR.
34. In monkeys, learning is abolished by lesions that include the floccular complex as well as some of the dorsal paraflocculus (9). In rabbits, learning is abolished by lesions of the flocculus, which constitutes most of the floccular complex in this species [S. Nagao, Exp. Brain Res. 53, 36 (1983)]. The primate floccular complex includes substantial amounts of tissue from the flocculus and the ventral paraflocculus, and it remains a matter of contention whether one or both of these structures constitute the relevant part of the floccular complex for motor learning in the VOR [N. M. Gerrits and J. Voogd, Exp. Brain Res. Suppl. 17, 26 (1989); M. Ito, Nature 363, 24 (1993); S. G. Lisberger and T. J. Sejnowski, ibid., p. 25]. Electrical recordings cited in (37) give additional support for the idea that the floccular complex is important for motor learning in the VOR.
35. The FTNs in the vestibular nuclei receive monosynaptic inputs from Purkinje cells and therefore function as deep cerebellar nuclei, even though they are not localized in the cerebellum proper [S. G. Lisberger and T. A. Pavelko, Science 242, 771 (1988)].
36. M. D. Mauk, J. E. Steinmetz, R. F. Thompson, Proc. Natl. Acad. Sci. U.S.A. 83, 5349 (1986); J. E. Steinmetz, D. G. Lavond, R. F. Thompson, Synapse 3, 225 (1989).
37. M. D. Mauk, J. E. Steinmetz, R. F. Thompson, Proc. Natl. Acad. Sci. U.S.A. 83, 5349 (1986); J. E. Steinmetz, D. G. Lavond, R. F. Thompson, Synapse 3, 225 (1989).
38. N. E. Berthier and J. W. Moore, Exp. Brain Res. 63, 341 (1986).
39. L. L. Sears and J. E. Steinmetz, Brain Res. 545, 114 (1991).
40. L. S. Stone and S. G. Lisberger, J. Neurophysiol. 63, 1241 (1990).
41. _, ibid., p. 1262; K. Alley, R. Baker, J. I. Simpson, Brain Res. 98, 582 (1975); W. Graf. J. I. Simpson, C. S. Leonard, J. Neurophysiol. 60, 2091 (1988); V. J. Wilson, M. Maeda, J. I. Franck, H. Shimazu, ibid. 39, 301 (1976).
42. _, ibid., p. 1262; K. Alley, R. Baker, J. I. Simpson, Brain Res. 98, 582 (1975); W. Graf. J. I. Simpson, C. S. Leonard, J. Neurophysiol. 60, 2091 (1988); V. J. Wilson, M. Maeda, J. I. Franck, H. Shimazu, ibid. 39, 301 (1976).
43. _, ibid., p. 1262; K. Alley, R. Baker, J. I. Simpson, Brain Res. 98, 582 (1975); W. Graf. J. I. Simpson, C. S. Leonard, J. Neurophysiol. 60, 2091 (1988); V. J. Wilson, M. Maeda, J. I. Franck, H. Shimazu, ibid. 39, 301 (1976).
44. _, ibid., p. 1262; K. Alley, R. Baker, J. I. Simpson, Brain Res. 98, 582 (1975); W. Graf. J. I. Simpson, C. S. Leonard, J. Neurophysiol. 60, 2091 (1988); V. J. Wilson, M. Maeda, J. I. Franck, H. Shimazu, ibid. 39, 301 (1976).
45. S. G. Lisberger and A. F. Fuchs, J. Neurophysiol. 41, 733 (1978); F. A. Miles, J. H. Fuller, D. J. Braitman, B. M. Dow, ibid. 43, 1437 (1980).
46. S. G. Lisberger and A. F. Fuchs, J. Neurophysiol. 41, 733 (1978); F. A. Miles, J. H. Fuller, D. J. Braitman, B. M. Dow, ibid. 43, 1437 (1980).
47. S. G. Lisberger and T. J. Sejnowski, Nature 360, 159 (1992); S. G. Lisberger, J. Neurophysiol. 72, 974 (1994).
48. S. G. Lisberger and T. J. Sejnowski, Nature 360, 159 (1992); S. G. Lisberger, J. Neurophysiol. 72, 974 (1994).
49. See, for example, A. Lundberg Exp. Brain Res. 12, 317 (1971); Y. I. Arshavsky et al., Brain Res. 43, 276 (1972); Y. I. Arshavsky et al., ibid. 151, 493 (1978).
50. See, for example, A. Lundberg Exp. Brain Res. 12, 317 (1971); Y. I. Arshavsky et al., Brain Res. 43, 276 (1972); Y. I. Arshavsky et al., ibid. 151, 493 (1978).
51. See, for example, A. Lundberg Exp. Brain Res. 12, 317 (1971); Y. I. Arshavsky et al., Brain Res. 43, 276 (1972); Y. I. Arshavsky et al., ibid. 151, 493 (1978).
52. D. J. Krupa, J. K. Thompson, R. F. Thompson, Science 260, 989 (1993).
53. J. P. Welsh and J. A. Harvey, J. Physiol. (London) 444, 459 (1991).
54. R. E. Clark, A. A. Zhang, D. G. Lavond, Behav. Neurosci. 106, 879 (1992); G. A. Clark, D. A. McCormick, D. G. Lavond, R. F. Thompson, Brain Res. 291, 125 (1984).
55. R. E. Clark, A. A. Zhang, D. G. Lavond, Behav. Neurosci. 106, 879 (1992); G. A. Clark, D. A. McCormick, D. G. Lavond, R. F. Thompson, Brain Res. 291, 125 (1984).
56. The proximity of FTNs to other VRNs makes it impossible to do this experiment with standard methods for either reversible or permanent ablation of neural tissue. The profound effect of lesions in the vestibular nucleus can be seen in T. Uemura and B. Cohen, Acta Oto-Laryngol. Suppl. 315, 1 (1973).
57. R. E. Clark and D. G. Lavond, Behav. Neurosci. 107, 264 (1993); P. F. Chapman, J. E. Steinmetz, L. L. Sears, R. F. Thompson, Brain Res. 537, 149 (1990).
58. R. E. Clark and D. G. Lavond, Behav. Neurosci. 107, 264 (1993); P. F. Chapman, J. E. Steinmetz, L. L. Sears, R. F. Thompson, Brain Res. 537, 149 (1990).
59. See (29). In contrast, reversible inactivation of the AIN with muscimol blocked acquisition of conditioning (28). However, this result may reflect the effects of residual activity in the presynaptic terminals in the nucleus; for further discussion, see (15).
60. A. E. Luebke and D. A. Robinson, Exp. Brain Res. 98, 379 (1994).
61. A. M. Pastor, R. R. DeLaCruz, R. Baker, J. Neurophysiol. 72, 1383 (1994).
62. A. M. Partsalis, Y. Zhang, S. M. Highstein, ibid., 73, 632.
63. M. Dufosse, M. Ito, P. J. Jastreboff, Y. Miyashita, Brain Res. 150, 611 (1978); F. A. Miles, D. J. Braitman, B. M. Dow, J. Neurophysiol. 43, 1477 (1980); E. Watanabe, Brain Res. 297, 169 (1984); S. G. Lisberger, T. A. Pavelko, D. M. Broussard, J. Neurophysiol. 72, 928 (1994); S. G. Lisberger, T. A. Pavelko, H. M. Bronte-Stewart, L. S. Stone, ibid., p. 954.
64. M. Dufosse, M. Ito, P. J. Jastreboff, Y. Miyashita, Brain Res. 150, 611 (1978); F. A. Miles, D. J. Braitman, B. M. Dow, J. Neurophysiol. 43, 1477 (1980); E. Watanabe, Brain Res. 297, 169 (1984); S. G. Lisberger, T. A. Pavelko, D. M. Broussard, J. Neurophysiol. 72, 928 (1994); S. G. Lisberger, T. A. Pavelko, H. M. Bronte-Stewart, L. S. Stone, ibid., p. 954.
65. M. Dufosse, M. Ito, P. J. Jastreboff, Y. Miyashita, Brain Res. 150, 611 (1978); F. A. Miles, D. J. Braitman, B. M. Dow, J. Neurophysiol. 43, 1477 (1980); E. Watanabe, Brain Res. 297, 169 (1984); S. G. Lisberger, T. A. Pavelko, D. M. Broussard, J. Neurophysiol. 72, 928 (1994); S. G. Lisberger, T. A. Pavelko, H. M. Bronte-Stewart, L. S. Stone, ibid., p. 954.
66. M. Dufosse, M. Ito, P. J. Jastreboff, Y. Miyashita, Brain Res. 150, 611 (1978); F. A. Miles, D. J. Braitman, B. M. Dow, J. Neurophysiol. 43, 1477 (1980); E. Watanabe, Brain Res. 297, 169 (1984); S. G. Lisberger, T. A. Pavelko, D. M. Broussard, J. Neurophysiol. 72, 928 (1994); S. G. Lisberger, T. A. Pavelko, H. M. Bronte-Stewart, L. S. Stone, ibid., p. 954.
67. M. Dufosse, M. Ito, P. J. Jastreboff, Y. Miyashita, Brain Res. 150, 611 (1978); F. A. Miles, D. J. Braitman, B. M. Dow, J. Neurophysiol. 43, 1477 (1980); E. Watanabe, Brain Res. 297, 169 (1984); S. G. Lisberger, T. A. Pavelko, D. M. Broussard, J. Neurophysiol. 72, 928 (1994); S. G. Lisberger, T. A. Pavelko, H. M. Bronte-Stewart, L. S. Stone, ibid., p. 954.
68. J. E. Desmond and J. W. Moore, Exp. Brain Res. 65, 59 (1986); R. F. Thompson et al., Physiol. Psychol. 8, 262 (1980); T. W. Berger, B. Alger, R. F. Thompson, Science 192, 483 (1976).
69. J. E. Desmond and J. W. Moore, Exp. Brain Res. 65, 59 (1986); R. F. Thompson et al., Physiol. Psychol. 8, 262 (1980); T. W. Berger, B. Alger, R. F. Thompson, Science 192, 483 (1976).
70. J. E. Desmond and J. W. Moore, Exp. Brain Res. 65, 59 (1986); R. F. Thompson et al., Physiol. Psychol. 8, 262 (1980); T. W. Berger, B. Alger, R. F. Thompson, Science 192, 483 (1976).
71. M. D. Mauk and B. P. Ruiz, Behav. Neurosci. 106, 666 (1992).
72. J. L. Raymond and S. G. Lisberger, Soc. Neurosci Abstr. 20, 1194 (1994).
73. The VOR is measured as the eye movement response to a head turn in darkness to study the eye movements driven by vestibular stimulation in isolation from visually driven eye movements, which may contribute to the responses measured during head turns in the light.
74. Learned timing is expressed somewhat differently in the conditioned eyelid response and the VOR. When the tone CS and air-puff US are paired with a long interval, the learned eyelid response has no early component, whereas when the vestibular and image motion stimuli are paired with a long interval, the learned VOR response has both early and late components. When the tone CS and air-puff US are paired with a short interval, the learned eyelid response has no late component, whereas when the vestibular and image motion stimuli are paired with a short interval, the learned VOR response has both early and late components. These apparent differences may not reflect fundamental differences in the principles of operation of the two systems Rather, they may reflect a difference in the resting discharge of neurons in the two circuits and the consequent difference in the threshold for the CS and the vestibular stimulus to elicit a behavioral response, or they may reflect small differences in the training protocols that have been used to induce learning in the two systems (for example, for pairing at a short interval, the vestibular stimulus continues after the end of the image motion stimulus, but the tone CS does not continue after the air-puff US).
75. M. Ito, Annu. Rev. Neurosci. 12, 85 (1989); D. J. Linden, M. H. Dickinson, M. Smeyne, J. A. Connor, Neuron 7, 81 (1991).
76. M. Ito, Annu. Rev. Neurosci. 12, 85 (1989); D. J. Linden, M. H. Dickinson, M. Smeyne, J. A. Connor, Neuron 7, 81 (1991).
77. F. A. Miles and S. G. Lisberger, Annu. Rev. Neurosci. 4, 273 (1981).
78. The simple-spike output of the cerebellum does not appear to contain information appropriate to guide learning under all conditions in which learning occurs, for example, when adapting with high-frequency sinusoidal stimuli [J. L. Raymond and S. G. Lisberger, Soc. Neurosci. Abstr. 21, 139 (1995)].
79. F. Tempia, N. Dieringer, P. Strata, Exp. Brain Res. 86, 568 (1991); N. H. Barmack and J. I. Simpson, J. Neurophysiol. 43, 182 (1980).
80. F. Tempia, N. Dieringer, P. Strata, Exp. Brain Res. 86, 568 (1991); N. H. Barmack and J. I. Simpson, J. Neurophysiol. 43, 182 (1980).
81. D. A. McCormick, J. E. Steinmetz, R. F. Thompson, Brain Res. 359, 120 (1985); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 63, 81 (1986).
82. D. A. McCormick, J. E. Steinmetz, R. F. Thompson, Brain Res. 359, 120 (1985); C. H. Yeo, M. J. Hardiman, M. Glickstein, Exp. Brain Res. 63, 81 (1986).
83. D. V. Buonomano and M. D. Mauk, Neural Comput. 6, 38 (1994); H. L. Galiana, in Adaptive Mechanisms in Gaze Control, A. Berthoz and G. Melvill Jones, Eds. (Elsevier, Amsterdam, 1985), pp. 327-344; B. W. Peterson, J. F. Baker, J. C. Houk, in Activity-Driven CNS Changes in Learning and Development, Ann. N.Y. Acad. Sci. 627, 319 (1991).
84. D. V. Buonomano and M. D. Mauk, Neural Comput. 6, 38 (1994); H. L. Galiana, in Adaptive Mechanisms in Gaze Control, A. Berthoz and G. Melvill Jones, Eds. (Elsevier, Amsterdam, 1985), pp. 327-344; B. W. Peterson, J. F. Baker, J. C. Houk, in Activity-Driven CNS Changes in Learning and Development, Ann. N.Y. Acad. Sci. 627, 319 (1991).
85. D. V. Buonomano and M. D. Mauk, Neural Comput. 6, 38 (1994); H. L. Galiana, in Adaptive Mechanisms in Gaze Control, A. Berthoz and G. Melvill Jones, Eds. (Elsevier, Amsterdam, 1985), pp. 327-344; B. W. Peterson, J. F. Baker, J. C. Houk, in Activity-Driven CNS Changes in Learning and Development, Ann. N.Y. Acad. Sci. 627, 319 (1991).
86. L. M. Optican and D. A. Robinson, J. Neurophysiol. 44, 1058 (1980), L. M. Optican and F. A. Miles, ibid. 54, 940 (1985); N. H. Donegan, R. W. Lowery, R. F. Thompson, Soc. Neurosci. Abstr. 9, 331 (1983); N. F. Popov, in Higher Nervous Activity, D. S. Fursikov, M. O. Gurevisch, A. N. Zalmanzon, Eds. (Com. Acad. Press, Moscow, 1929), vol. 1, pp. 140-148, A. I. Karamian, V. V. Fanardijian, A. A. Kosareva, in Neurobiology of Cerebellar Evolution and Development, First International Symposium, R. Llinas, Ed. (American Medical Association, Chicago, 1969), pp. 639-673.
87. L. M. Optican and D. A. Robinson, J. Neurophysiol. 44, 1058 (1980), L. M. Optican and F. A. Miles, ibid. 54, 940 (1985); N. H. Donegan, R. W. Lowery, R. F. Thompson, Soc. Neurosci. Abstr. 9, 331 (1983); N. F. Popov, in Higher Nervous Activity, D. S. Fursikov, M. O. Gurevisch, A. N. Zalmanzon, Eds. (Com. Acad. Press, Moscow, 1929), vol. 1, pp. 140-148, A. I. Karamian, V. V. Fanardijian, A. A. Kosareva, in Neurobiology of Cerebellar Evolution and Development, First International Symposium, R. Llinas, Ed. (American Medical Association, Chicago, 1969), pp. 639-673.
88. L. M. Optican and D. A. Robinson, J. Neurophysiol. 44, 1058 (1980), L. M. Optican and F. A. Miles, ibid. 54, 940 (1985); N. H. Donegan, R. W. Lowery, R. F. Thompson, Soc. Neurosci. Abstr. 9, 331 (1983); N. F. Popov, in Higher Nervous Activity, D. S. Fursikov, M. O. Gurevisch, A. N. Zalmanzon, Eds. (Com. Acad. Press, Moscow, 1929), vol. 1, pp. 140-148, A. I. Karamian, V. V. Fanardijian, A. A. Kosareva, in Neurobiology of Cerebellar Evolution and Development, First International Symposium, R. Llinas, Ed. (American Medical Association, Chicago, 1969), pp. 639-673.
89. L. M. Optican and D. A. Robinson, J. Neurophysiol. 44, 1058 (1980), L. M. Optican and F. A. Miles, ibid. 54, 940 (1985); N. H. Donegan, R. W. Lowery, R. F. Thompson, Soc. Neurosci. Abstr. 9, 331 (1983); N. F. Popov, in Higher Nervous Activity, D. S. Fursikov, M. O. Gurevisch, A. N. Zalmanzon, Eds. (Com. Acad. Press, Moscow, 1929), vol. 1, pp. 140-148, A. I. Karamian, V. V. Fanardijian, A. A. Kosareva, in Neurobiology of Cerebellar Evolution and Development, First International Symposium, R. Llinas, Ed. (American Medical Association, Chicago, 1969), pp. 639-673.
90. L. M. Optican and D. A. Robinson, J. Neurophysiol. 44, 1058 (1980), L. M. Optican and F. A. Miles, ibid. 54, 940 (1985); N. H. Donegan, R. W. Lowery, R. F. Thompson, Soc. Neurosci. Abstr. 9, 331 (1983); N. F. Popov, in Higher Nervous Activity, D. S. Fursikov, M. O. Gurevisch, A. N. Zalmanzon, Eds. (Com. Acad. Press, Moscow, 1929), vol. 1, pp. 140-148, A. I. Karamian, V. V. Fanardijian, A. A. Kosareva, in Neurobiology of Cerebellar Evolution and Development, First International Symposium, R. Llinas, Ed. (American Medical Association, Chicago, 1969), pp. 639-673.
91. We thank the members of the Lisberger and Mauk laboratories and D. Buonomano for helpful comments on earlier versions of this paper. Supported by NIH grants EY03878 (S.G.L.), EY10198 (S.G.L.), and MH46904 (M.D.M.); Office of Naval Research contract N00014-94-1-0269 (S.G.L.); a NASA Research Associate Fellowship (J.L.R.); two McKnight Scholars Awards (M.D.M., S.G.L.); and a McKnight Development Award (S.G.L.).