Role of plasticity at different sites across the time course of cerebellar motor learning

Journal of Neuroscience

Volumn 34, Issue 21, 2014, Pages 7077-7090

  Yang, Yan ^a   Lisberger, Stephen G ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Climbing fibers; Floccular complex; Long term depression; Smooth pursuit eye movement; Synaptic plasticity; Trial over trial learning

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM; CLIMBING FIBER; CONTROLLED STUDY; HAPLORHINI; LEARNING; MALE; MOTOR LEARNING; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SMOOTH PURSUIT EYE MOVEMENT; SPIKE;

CLIMBING FIBERS; FLOCCULAR COMPLEX; LONG-TERM DEPRESSION; SMOOTH PURSUIT EYE MOVEMENT; SYNAPTIC PLASTICITY; TRIAL-OVER-TRIAL LEARNING;

ACTION POTENTIALS; ANIMALS; CEREBELLUM; LEARNING; MACACA MULATTA; MALE; ORIENTATION; PHOTIC STIMULATION; PURKINJE CELLS; PURSUIT, SMOOTH; TIME FACTORS; WAKEFULNESS;

EID: 84901022733     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0017-14.2014     Document Type: Article

References (59)

1. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25-61. CrossRef
2. Armano S, Rossi P, Taglietti V, D'Angelo E (2000) Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. J Neurosci 20:5208-5216. Medline
3. Belmeguenai A, Hosy E, Bengtsson F, Pedroarena CM, Piochon C, Teuling E, He Q, Ohtsuki G, De Jeu MT, Elgersma Y, De Zeeuw CI, Jörntell H, Hansel C (2010) Intrinsic plasticity complements long-term potentiation in parallel fiber input gain control in cerebellar Purkinje cells. J Neurosci 30:13630-13643. CrossRef Medline
4. Blazquez PM, Hirata Y, Highstein SM (2004) The vestibulo-ocular reflex as a model system for motor learning: what is the role of the cerebellum? Cerebellum 3:188-192. CrossRef Medline
5. Blazquez PM, Hirata Y, Highstein SM (2006) Chronic changes in inputs to dorsal Y neurons accompany VOR motor learning. J Neurophysiol 95: 1812-1825. CrossRef Medline
6. Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581-609. CrossRef Medline
7. Boyden ES, Katoh A, Pyle JL, Chatila TA, Tsien RW, Raymond JL (2006) Selective engagement of plasticity mechanisms for motor memory storage. Neuron 21:823-834. Medline
8. Carey MR (2011) Synaptic mechanisms of sensorimotor learning in the cerebellum. Curr Opin Neurobiol 21:609-615. CrossRef Medline
9. Christian KM, Thompson RF (2003) Neural substrates of eye blink conditioning: acquisition and retention. Learn Mem 10:427-455. CrossRef Medline
10. D'Angelo E, Rossi P, Armano S, Taglietti V (1999) Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fiber-granule cell transmission in rat cerebellum. J Neurophysiol 81:277-287. Medline
11. Ethier V, Zee DS, Shadmehr R (2008) Spontaneous recovery of motor memory during saccade adaptation. J Neurophysiol 99:2577-2583. CrossRef Medline
12. Gao Z, van Beugen BJ, De Zeeuw CI (2012) Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13:619-635. CrossRef Medline
13. Gilbert PF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309-328. CrossRef Medline
14. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4:467-475. Medline
15. Highstein SM (1973) Synaptic linkage in the vestibulo-ocular and cerebellovestibular pathways to the VIth nucleus in the rabbit. Exp Brain Res 17:301-314. Medline
16. Ito M (1972) Neural design of the cerebellar motor control system. Brain Res 40:81-84. CrossRef Medline
17. Jörntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34:797-806. CrossRef Medline
18. Jörntell H, Ekerot CF (2003) Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J Neurosci 23:9620-9631. Medline
19. Jörntell H, Hansel C (2006) Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron 52: 227-238. CrossRef Medline
20. Kahlon M, Lisberger SG (1996) Coordinate system for learning in the smooth pursuit eye movements of monkeys. J Neurosci 16:7270-7283. Medline
21. Kahlon M, Lisberger SG (2000) Changes in the responses of Purkinje cells in the floccular complex of monkeys after motor learning in smooth pursuit eye movements. J Neurophysiol 84:2945-2960. Medline
22. Kalmbach BE, Davis T, Ohyama T, Riusech F, Nores WL, Mauk MD (2010) Cerebellar cortex contributions to the expression and timing of conditioned eyelid responses. J Neurophysiol 103:2039-2049. CrossRef Medline
23. Ke MC, Guo CC, Raymond JL (2009) Elimination of climbing fiber instructive signals during motor learning. Nat Neurosci 12:1171-1179. CrossRef Medline
24. Krauzlis RJ, Lisberger SG (1996) Directional organization of eye movement and visual signals in the floccular lobe of the monkey cerebellum. Exp Brain Res 109:289-302. Medline
25. Lev-Ram V, Wong ST, Storm DR, Tsien RY (2002) A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci U S A 99:8389-8393. CrossRef Medline
26. Lisberger SG (1994) Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. J Neurophysiol 72:974-998. Medline
27. Lisberger SG (2009) Internal models of eye movement in the floccular complex of the monkey cerebellum. Neuroscience 162:763-776. CrossRef Medline
28. Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol 41:733-763. Medline
29. Lisberger SG, Pavelko TA (1986) Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys. J Neurosci 6:346-354. Medline
30. Lisberger SG, Pavelko TA, Broussard DM (1994) Neural basis for motor learning in the vestibulo-ocular reflex of primates: I. Changes in the responses of brain stem neurons that receive monosynaptic inhibition from the flocculus and ventral paraflocculus. J Neurophysiol 72:928-953. Medline
31. Maekawa K, Simpson JI (1973) Climbing fiber responses evoked in vestibulecerebellum of rabbit from visual system. J Neurophysiol 36:649-666. Medline
32. Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437-470.
33. Maruta J, Hensbroek RA, Simpson JI (2007) Intraburst and interburst signaling by climbing fibers. J Neurosci 27:11263-11270. CrossRef Medline
34. Medina JF, Lisberger SG (2008) Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11:1185-1192. CrossRef Medline
35. Medina JF, Lisberger SG (2009) Encoding and decoding of learned smoothpursuit eye movements in the floccular complex of the monkey cerebellum. J Neurophysiol 102:2039-2054. CrossRef Medline
36. Medina JF, Mauk MD (2000) Computer simulation of cerebellar information processing. Nat Neurosci 3:1205-1211. CrossRef Medline
37. Medina JF, Nores WL, Ohyama T, Mauk MD (2000) Mechanisms of cerebellar learning suggested by eyelid conditioning. Curr Opin Neurobiol 10:717-724. CrossRef Medline
38. Medina JF, Carey MR, Lisberger SG (2005) The representation of time for motor learning. Neuron 45:157-167. CrossRef Medline
39. Miles FA, Fuller JH (1975) Visual tracking and the primate flocculus. Science 189:1000-1002. Medline
40. Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 4:273-299. CrossRef Medline
41. Nelson AB, Gittis AH, du Lac S (2005) Decreases in CaMKII activity trigger persistent potentiation of intrinsic excitability in spontaneously firing vestibular nucleus neurons. Neuron 46:623-631. CrossRef Medline
42. Ohyama T, Nores WL, Medina JF, Riusech FA, Mauk MD (2006) Learninginduced plasticity in deep cerebellar nucleus. J Neurosci 26:12656-12663. CrossRef Medline
43. Ramachandran R, Lisberger SG (2005) Normal performance and expression of learning in the vestibulo-ocular reflex (VOR) at high frequencies. J Neurophysiol 93:2028-2038. Medline
44. Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG (2002) Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J Neurophysiol 87:912-924. Medline
45. Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol 159:326-338. Medline
46. Smith MA, Ghazizadeh A, Shadmehr R (2006) Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4:e179. Medline
47. Stone LS, Lisberger SG (1990a) Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple-spikes. J Neurophysiol 63:1241-1261. Medline
48. Stone LS, Lisberger SG (1990b) Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. II. Complex spikes. J Neurophysiol 63:1262-1275. Medline
49. Suzuki DA, Keller EL (1988) The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocityrelated Purkinje cell activity. J Neurophysiol 59:19-40. Medline
50. Takagi M, Zee DS, Tamargo RJ (2000) Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J Neurophysiol 83:2047-2062. Medline
51. Thompson RF (2013) An essential memory trace found. Behav Neurosci 127:669-675. CrossRef Medline
52. van Alphen AM, De Zeeuw CI (2002) Cerebellar LTD facilitates but is not essential for long-term adaptation of the vestibulo-ocular reflex. Eur J Neurosci 16:486-490. CrossRef Medline
53. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoè-Pognetto M, Badura A, Gao Z, Hoebeek FE, van Dorp S, Wisden W, Farrant M, De Zeeuw CI (2009) Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat Neurosci 12:1042-1049. CrossRef Medline
54. Yang Y, Lisberger SG (2010) Learning on multiple timescales in smooth pursuit eye movements. J Neurophysiol 104:2850-2862. CrossRef Medline
55. Yang Y, Lisberger SG (2013) Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning. eLife 2:e01574. CrossRef Medline
56. Yang Y, Lisberger SG (2014) Purkinje-cell plasticity and cerebellar motor learning are graded by complex-spike duration. Advance online publication. doi:10.1038/nature13282. CrossRef
57. Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878-899. Medline
58. Zhang W, Linden DJ (2006) Long-term depression at the mossy fiber-deep cerebellar nucleus synapse. J Neurosci 26:6935-6944. CrossRef Medline
59. Zheng N, Raman IM (2010) Synaptic inhibition, excitation, and plasticity in neurons of the cerebellar nuclei. Cerebellum 9:56-66. CrossRef Medline