Learning-induced structural plasticity in the cerebellum

International Review of Neurobiology

Volumn 117, Issue , 2014, Pages 1-19

  Nishiyama, Hiroshi ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cerebellum; Electron microscopy; Live imaging; Motor learning; Parallel fibers; Purkinje cells; Rewiring; Structural plasticity

Indexed keywords

ACROBATIC MOTOR SKILL; ARTICLE; BASILAR PONTINE NUCLEUS; CEREBELLUM; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CONDITIONING; DORSOLATERAL HUMP; EYELID CLOSURE; EYELID CONDITIONING; FUNCTIONAL PLASTICITY; GOLGI CELL; HUMAN; INFERIOR OLIVE; INTERPOSITUS NUCLEUS; LEARNING; LONG TERM DEPRESSION; LONG TERM MEMORY; LONG TERM POTENTIATION; MOSSY FIBER; MOTOR LEARNING; MOTOR PERFORMANCE; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PARALLEL FIBER; PONTINE NUCLEUS; PRIORITY JOURNAL; PURKINJE CELL; STRUCTURAL PLASTICITY; SYNAPSE; ANIMAL; CYTOLOGY; PHYSIOLOGY;

ANIMALS; CEREBELLUM; HUMANS; LEARNING; NEURONAL PLASTICITY; SYNAPSES;

EID: 84906777754     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-420247-4.00001-4     Document Type: Chapter

References (91)

1. Anderson B.J., Alcantara A.A., Greenough W.T. Motor-skill learning: Changes in synaptic organization of the rat cerebellar cortex. Neurobiology of Learning and Memory 1996, 66(2):221-229.
2. Anderson B.J., Relucio K., Haglund K., Logan C., Knowlton B., Thompson J., et al. Effects of paired and unpaired eye-blink conditioning on Purkinje cell morphology. Learning & Memory 1999, 6(2):128-137.
3. Aziz W., Wang W., Kesaf S., Mohamed A.A., Fukazawa Y., Shigemoto R. Distinct kinetics of synaptic structural plasticity, memory formation, and memory decay in massed and spaced learning. Proceedings of the National Academy of Sciences of the United States of America 2014, 111(1):E194-E202.
4. Bennett E.L., Diamond M.C., Krech D., Rosenzweig M.R. Chemical and anatomical plasticity brain. Science 1964, 146(3644):610-619.
5. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proceedings of the National Academy of Sciences of the United States of America 1990, 87(14):5568-5572.
6. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. Journal of Physiology 1973, 232(2):331-356.
7. Boele H.J., Koekkoek S.K., De Zeeuw C.I., Ruigrok T.J. Axonal sprouting and formation of terminals in the adult cerebellum during associative motor learning. Journal of Neuroscience 2013, 33(45):17897-17907.
8. Carey M.R. Synaptic mechanisms of sensorimotor learning in the cerebellum. Current Opinion in Neurobiology 2011, 21(4):609-615.
9. Carrillo J., Cheng S.Y., Ko K.W., Jones T.A., Nishiyama H. The long-term structural plasticity of cerebellar parallel fiber axons and its modulation by motor learning. Journal of Neuroscience 2013, 33(19):8301-8307.
10. Carulli D., Rhodes K.E., Brown D.J., Bonnert T.P., Pollack S.J., Oliver K., et al. Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. Journal of Comparative Neurology 2006, 494(4):559-577.
11. Chang F.L., Greenough W.T. Lateralized effects of monocular training on dendritic branching in adult split-brain rats. Brain Research 1982, 232(2):283-292.
12. Coesmans M., Weber J.T., De Zeeuw C.I., Hansel C. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 2004, 44(4):691-700.
13. Connor S., Bloomfield J., LeBoutillier J.C., Thompson R.F., Petit T.L., Weeks A.C. Eyeblink conditioning leads to fewer synapses in the rabbit cerebellar cortex. Behavioral Neuroscience 2009, 123(4):856-862.
14. Corvetti L., Rossi F. Degradation of chondroitin sulfate proteoglycans induces sprouting of intact Purkinje axons in the cerebellum of the adult rat. Journal of Neuroscience 2005, 25(31):7150-7158.
15. De Paola V., Holtmaat A., Knott G., Song S., Wilbrecht L., Caroni P., et al. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 2006, 49(6):861-875.
16. Eccles J.C., Ito M., Szentagothai J. The cerebellum as a neuronal machine 1967, Springer, New York, NY.
17. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399(6731):66-70.
18. Federmeier K.D., Kleim J.A., Greenough W.T. Learning-induced multiple synapse formation in rat cerebellar cortex. Neuroscience Letters 2002, 332(3):180-184.
19. Foscarin S., Ponchione D., Pajaj E., Leto K., Gawlak M., Wilczynski G.M., et al. Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses. PLoS One 2011, 6(1):e16666.
20. Gao Z., van Beugen B.J., De Zeeuw C.I. Distributed synergistic plasticity and cerebellar learning. Nature Reviews. Neuroscience 2012, 13(9):619-635.
21. Garcia K.S., Steele P.M., Mauk M.D. Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. Journal of Neuroscience 1999, 19(24):10940-10947.
22. Geinisman Y., Berry R.W., Disterhoft J.F., Power J.M., Van der Zee E.A. Associative learning elicits the formation of multiple-synapse boutons. Journal of Neuroscience 2001, 21(15):5568-5573.
23. Gogolla N., Caroni P., Luthi A., Herry C. Perineuronal nets protect fear memories from erasure. Science 2009, 325(5945):1258-1261.
24. Greenough W.T., Larson J.R., Withers G.S. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behavioral and Neural Biology 1985, 44(2):301-314.
25. Grutzendler J., Kasthuri N., Gan W.B. Long-term dendritic spine stability in the adult cortex. Nature 2002, 420(6917):812-816.
26. Halverson H.E., Freeman J.H. Medial auditory thalamic input to the lateral pontine nuclei is necessary for auditory eyeblink conditioning. Neurobiology of Learning and Memory 2010, 93(1):92-98.
27. Hansel C., Linden D.J., D'Angelo E. Beyond parallel fiber LTD: The diversity of synaptic and non-synaptic plasticity in the cerebellum. Nature Neuroscience 2001, 4(5):467-475.
28. Heiney S.A., Kim J., Augustine G.J., Medina J.F. Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. Journal of Neuroscience 2014, 34(6):2321-2330.
29. Hesslow G., Svensson P., Ivarsson M. Learned movements elicited by direct stimulation of cerebellar mossy fiber afferents. Neuron 1999, 24(1):179-185.
30. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., et al. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45(2):279-291.
31. Holtmaat A., Wilbrecht L., Knott G.W., Welker E., Svoboda K. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 2006, 441(7096):979-983.
32. Ito M. The cerebellum and neural control 1984, Raven Press, New York, NY.
33. Ito M. Cerebellar long-term depression: Characterization, signal transduction, and functional roles. Physiological Reviews 2001, 81(3):1143-1195.
34. Ito M., Kano M. Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neuroscience Letters 1982, 33(3):253-258.
35. Ito M., Sakurai M., Tongroach P. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. Journal of Physiology 1982, 324:113-134.
36. Jones T.A., Chu C.J., Grande L.A., Gregory A.D. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. Journal of Neuroscience 1999, 19(22):10153-10163.
37. Jones T.A., Klintsova A.Y., Kilman V.L., Sirevaag A.M., Greenough W.T. Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiology of Learning and Memory 1997, 68(1):13-20.
38. Jorntell H., Hansel C. Synaptic memories upside down: Bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron 2006, 52(2):227-238.
39. Kandler K., Herbert H. Auditory projections from the cochlear nucleus to pontine and mesencephalic reticular nuclei in the rat. Brain Research 1991, 562(2):230-242.
40. Kleim J.A., Freeman J.H., Bruneau R., Nolan B.C., Cooper N.R., Zook A., et al. Synapse formation is associated with memory storage in the cerebellum. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(20):13228-13231.
41. Kleim J.A., Swain R.A., Armstrong K.A., Napper R.M., Jones T.A., Greenough W.T. Selective synaptic plasticity within the cerebellar cortex following complex motor skill learning. Neurobiology of Learning and Memory 1998, 69(3):274-289.
42. Knott G.W., Quairiaux C., Genoud C., Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 2002, 34(2):265-273.
43. Lee W.C., Huang H., Feng G., Sanes J.R., Brown E.N., So P.T., et al. Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biology 2006, 4(2):e29.
44. Lee K.J., Jung J.G., Arii T., Imoto K., Rhyu I.J. Morphological changes in dendritic spines of Purkinje cells associated with motor learning. Neurobiology of Learning and Memory 2007, 88(4):445-450.
45. Lee K.J., Park I.S., Kim H., Greenough W.T., Pak D.T., Rhyu I.J. Motor skill training induces coordinated strengthening and weakening between neighboring synapses. Journal of Neuroscience 2013, 33(23):9794-9799.
46. Lendvai B., Stern E.A., Chen B., Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 2000, 404(6780):876-881.
47. Lev-Ram V., Wong S.T., Storm D.R., Tsien R.Y. A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(12):8389-8393.
48. Linden D.J. The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(24):14066-14071.
49. Linden D.J., Dickinson M.H., Smeyne M., Connor J.A. A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons. Neuron 1991, 7(1):81-89.
50. Majewska A.K., Newton J.R., Sur M. Remodeling of synaptic structure in sensory cortical areas in vivo. Journal of Neuroscience 2006, 26(11):3021-3029.
51. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429(6993):761-766.
52. Mauk M.D. Roles of cerebellar cortex and nuclei in motor learning: Contradictions or clues?. Neuron 1997, 18(3):343-346.
53. Mauk M.D., Garcia K.S., Medina J.F., Steele P.M. Does cerebellar LTD mediate motor learning? Toward a resolution without a smoking gun. Neuron 1998, 20(3):359-362.
54. Mauk M.D., Steinmetz J.E., Thompson R.F. Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proceedings of the National Academy of Sciences of the United States of America 1986, 83(14):5349-5353.
55. McCormick D.A., Thompson R.F. Cerebellum: Essential involvement in the classically conditioned eyelid response. Science 1984, 223(4633):296-299.
56. Medina J.F., Mauk M.D. Simulations of cerebellar motor learning: Computational analysis of plasticity at the mossy fiber to deep nucleus synapse. Journal of Neuroscience 1999, 19(16):7140-7151.
57. Miyata S., Akagi A., Hayashi N., Watanabe K., Oohira A. Activity-dependent regulation of a chondroitin sulfate proteoglycan 6B4 phosphacan/RPTPbeta in the hypothalamic supraoptic nucleus. Brain Research 2004, 1017(1-2):163-171.
58. Morita S., Oohira A., Miyata S. Activity-dependent remodeling of chondroitin sulfate proteoglycans extracellular matrix in the hypothalamo-neurohypophysial system. Neuroscience 2010, 166(4):1068-1082.
59. Nagerl U.V., Eberhorn N., Cambridge S.B., Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 2004, 44(5):759-767.
60. Nishiyama N., Colonna J., Shen E., Carrillo J., Nishiyama H. Long-term in vivo time-lapse imaging of synapse development and plasticity in the cerebellum. Journal of Neurophysiology 2014, 111(1):208-216.
61. Nishiyama H., Fukaya M., Watanabe M., Linden D.J. Axonal motility and its modulation by activity are branch-type specific in the intact adult cerebellum. Neuron 2007, 56(3):472-487.
62. Ohyama T., Nores W.L., Medina J.F., Riusech F.A., Mauk M.D. Learning-induced plasticity in deep cerebellar nucleus. Journal of Neuroscience 2006, 26(49):12656-12663.
63. Ohyama T., Nores W.L., Murphy M., Mauk M.D. What the cerebellum computes. Trends in Neurosciences 2003, 26(4):222-227.
64. Okamoto K., Nagai T., Miyawaki A., Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nature Neuroscience 2004, 7(10):1104-1112.
65. Ostroff L.E., Fiala J.C., Allwardt B., Harris K.M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 2002, 35(3):535-545.
66. Palay S., Chan-Palay V. Cerebellar cortex: Cytology and organization 1974, Springer, New York, NY.
67. Perrett S.P., Mauk M.D. Extinction of conditioned eyelid responses requires the anterior lobe of cerebellar cortex. Journal of Neuroscience 1995, 15(3 Pt. 1):2074-2080.
68. Pichitpornchai C., Rawson J.A., Rees S. Morphology of parallel fibres in the cerebellar cortex of the rat: An experimental light and electron microscopic study with biocytin. Journal of Comparative Neurology 1994, 342(2):206-220.
69. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298(5596):1248-1251.
70. Popov V.I., Bocharova L.S. Hibernation-induced structural changes in synaptic contacts between mossy fibres and hippocampal pyramidal neurons. Neuroscience 1992, 48(1):53-62.
71. Popov V.I., Bocharova L.S., Bragin A.G. Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 1992, 48(1):45-51.
72. Pugh J.R., Raman I.M. Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 2006, 51(1):113-123.
73. Raymond J.L., Lisberger S.G., Mauk M.D. The cerebellum: A neuronal learning machine?. Science 1996, 272(5265):1126-1131.
74. Ruediger S., Vittori C., Bednarek E., Genoud C., Strata P., Sacchetti B., et al. Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 2011, 473(7348):514-518.
75. Sale A., Maya Vetencourt J.F., Medini P., Cenni M.C., Baroncelli L., De Pasquale R., et al. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nature Neuroscience 2007, 10(6):679-681.
76. Schonewille M., Gao Z., Boele H.J., Veloz M.F., Amerika W.E., Simek A.A., et al. Reevaluating the role of LTD in cerebellar motor learning. Neuron 2011, 70(1):43-50.
77. Steinmetz J.E., Lavond D.G., Thompson R.F. Classical conditioning in rabbits using pontine nucleus stimulation as a conditioned stimulus and inferior olive stimulation as an unconditioned stimulus. Synapse 1989, 3(3):225-233.
78. Stettler D.D., Yamahachi H., Li W., Denk W., Gilbert C.D. Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 2006, 49(6):877-887.
79. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420(6917):788-794.
80. Tracy J.A., Thompson J.K., Krupa D.J., Thompson R.F. Evidence of plasticity in the pontocerebellar conditioned stimulus pathway during classical conditioning of the eyeblink response in the rabbit. Behavioral Neuroscience 1998, 112(2):267-285.
81. Wang Y.T., Linden D.J. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 2000, 25(3):635-647.
82. Wang W., Nakadate K., Masugi-Tokita M., Shutoh F., Aziz W., Tarusawa E., et al. Distinct cerebellar engrams in short-term and long-term motor learning. Proceedings of the National Academy of Sciences of the United States of America 2014, 111(1):E188-E193.
83. Weeks A.C., Connor S., Hinchcliff R., LeBoutillier J.C., Thompson R.F., Petit T.L. Eye-blink conditioning is associated with changes in synaptic ultrastructure in the rabbit interpositus nuclei. Learning & Memory 2007, 14(6):385-389.
84. Welsh J.P., Yamaguchi H., Zeng X.H., Kojo M., Nakada Y., Takagi A., et al. Normal motor learning during pharmacological prevention of Purkinje cell long-term depression. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(47):17166-17171.
85. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. Journal of Neuroscience 1990, 10(12):4035-4039.
86. Xu T., Yu X., Perlik A.J., Tobin W.F., Zweig J.A., Tennant K., et al. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 2009, 462(7275):915-919.
87. Yang G., Pan F., Gan W.B. Stably maintained dendritic spines are associated with lifelong memories. Nature 2009, 462(7275):920-924.
88. Zhang W., Linden D.J. Long-term depression at the mossy fiber-deep cerebellar nucleus synapse. Journal of Neuroscience 2006, 26(26):6935-6944.
89. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44(5):749-757.
90. Zuo Y., Lin A., Chang P., Gan W.B. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 2005, 46(2):181-189.
91. Zuo Y., Yang G., Kwon E., Gan W.B. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 2005, 436(7048):261-265.