Reevaluation of the role of parallel fiber synapses in delay eyeblink conditioning in mice using Cbln1 as a tool

Frontiers in Neural Circuits

Volumn 7, Issue NOV, 2013, Pages

  Emi, Kyoichi ^a,b   Kakegawa, Wataru ^a,b   Miura, Eriko ^a,b   Ito Ishida, Aya ^a,b   Kohda, Kazuhisa ^a,b   Yuzaki, Michisuke ^a,b  

^a KEIO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cerebellum; Long term depression; Motor learning; Mouse; Purkinje cell

Indexed keywords

RECOMBINANT CEREBELLIN PRECURSOR PROTEIN 1; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; CBLN1 PROTEIN, MOUSE; NERVE PROTEIN; PROTEIN PRECURSOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CBLN1 GENE; CELL BASED GENE THERAPY; CELL STRUCTURE; CONDITIONED REFLEX; CONTROLLED STUDY; DELAY EYEBLINK CONDITIONING; EYELID REFLEX; EYELID REFLEX DISORDER; GENE; GENE DISRUPTION; GENE FUNCTION; GENE IDENTIFICATION; IN VIVO STUDY; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PURKINJE CELL; REFLEX DISORDER; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; CEREBELLUM; CONDITIONING; DRUG EFFECT; GENETICS; KNOCKOUT MOUSE; LEARNING; MEMORY; MOTOR LEARNING; PHYSIOLOGY; DRUG EFFECTS;

CEREBELLUM; LONG-TERM DEPRESSION; MOTOR LEARNING; MOUSE; PURKINJE CELL;

ANIMALS; ASSOCIATION LEARNING; CEREBELLUM; CONDITIONING, EYELID; MEMORY; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PROTEIN PRECURSORS; PURKINJE CELLS; RECOMBINANT PROTEINS; SYNAPSES;

EID: 84888185226     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00180     Document Type: Article

References (56)

1. Aiba, A., Kano, M., Chen, C., Stanton, M. E., Fox, G. D., Herrup, K., et al. (1994). Deficient cerebellar long-term depression and impaired motor learning in mGluRl mutant mice. Cell 79, 377-388. doi: 10.1016/0092-8674(94)90205-4
2. Attwell, P. J., Cooke, S. F., and Yeo, C. H. (2002). Cerebellar function in consolidation of a motor memory. Neuron 34, 1011-1020. doi: 10.1016/S0896-6273(02) 00719-5
3. Blazquez, P.M., Hirata, Y., and Highstein, S.M. (2004). Thevestibulo-ocular reflexas a model system for motor learning: what is the role of the cerebellum? Cerebellum 3,188-192. doi: 10.1080/14734220410018120
4. Boele, H. J., Koekkoek, S. K., and De Zeeuw, C. I. (2010). Cerebellar and extrac- erebellar involvement in mouse eyeblink conditioning: the ACDC model. Front. Cell. Neurosci. 3:19. doi: 10.3389/neuro.03.019.2009
5. Boyden, E.S., Katoh, A., and Raymond, J.L. (2004). Cerebellum-dependentlearning: the role of multiple plasticitymechanisms. Annu. Rev. Neurosci. 27, 581-609. doi: 10.1146/annurev.neuro.27.070203.144238
6. Bracha, V., Zbarska, S., Parker, K., Carrel, A., Zenitsky, G., and Bloedel, J. R. (2009). The cerebellum and eye-blink conditioning: learning versus network performance hypotheses. Neuroscience 162, 787-796. doi: 10.1016/j.neuroscience.2008. 12.042
7. Brown, K. L., Agelan, A., and Woodruff-Pak, D. S. (2010). Unimpaired trace classical eyeblink conditioning in Purkinje cell degeneration (pcd) mutant mice. Neurobiol Learn. Mem. 93, 303-311. doi: 10.1016/j.nlm.2009.11.004
8. Chen, L., Bao, S., Lockard, J. M., Kim, J. K., and Thompson, R. F. (1996). Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J. Neurosci. 16, 2829-2838.
9. Christian, K. M., and Thompson, R. F. (2003). Neural substrates of eye- blink conditioning: acquisition and retention. Learn. Mem. 10, 427-455. doi: 10.1101/lm.59603
10. Clark, R. E., Zhang, A. A., and Lavond, D. G. (1997). The importance of cerebellar cortex and facial nucleus in acquisition and retention of eyeblink/NM conditioning: evidence for critical unilateral regulation of the conditioned response. Neurobiol Learn. Mem. 67, 96-111. doi: 10.1006/nlme.1996.3740
11. De Zeeuw, C. I., Hansel, C., Bian, F., Koekkoek, S. K., Van Alphen, A. M., Linden, D. J., et al. (1998). Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20, 495-508. doi: 10.1016/S0896-6273(00)80990-3
12. Emi, K., Kohda, K., Kakegawa, W., Narumi, S., and Yuzaki, M. (2011). A new rapid protocol for eyeblink conditioning to assess cerebellar motor learning. Neurochem. Res. 36, 1314-1322. doi: 10.1007/s11064-010-0392-z
13. Fujiwara, A., Kakizawa, S., and Iino, M. (2007). Induction of cerebellar long-term depression requires activation of calcineurin in Purkinje cells. Neuropharmacology 52,1663-1670. doi: 10.1016/j.neuropharm.2007.03.011
14. Garcia, K. S., and Mauk, M. D. (1998). Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37, 471-480. doi: 10.1016/S0028-3908(98)00055-0
15. Hesslow, G., Jirenhed, D. A., Rasmussen, A., and Johansson, F. (2013). Classical conditioning of motor responses: what is the learning mechanism? NeuralNetw. 47, 81-87. doi: 10.1016/j.neunet.2013.03.013
16. Hesslow, G., and Yeo, C. H. (2002). The functional anatomy of skeletal conditioning in A Neuroscientist's Guide to Classical Conditioning, ed. J. W. Moore (New York: Springer-Verlag), 86-146.
17. Hirai, H., Pang, Z., Bao, D., Miyazaki, T., Li, L., Miura, E., et al. (2005). Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nat. Neurosci. 8, 1534-1541. doi: 10.1038/nn1576
18. Ito-Ishida, A., Miura, E., Emi, K., Matsuda, K., Iijima, T., Kondo, T., et al. (2008). Cbln1 regulates rapid formation and maintenance of excitatory synapses in mature cerebellar Purkinje cells in vitro and in vivo. J. Neurosci. 28, 5920-5930. doi: 10.1523/JNEUR0SCI.1030-08.2008
19. Kakegawa, W., Miyazaki, T., Emi, K., Matsuda, K., Kohda, K., Motohashi, J., et al. Differential regulation of synaptic plasticity and cerebellar motor learning by the C-terminal PDZ-binding motif of GluRdelta2. J. Neurosci. 28, 1460-1468. doi: 10.1523/JNEUR0SCI.2553-07.2008
20. Kakegawa, W., Miyazaki, T., Kohda, K., Matsuda, K., Emi, K., Motohashi, J., et al. The N-terminal domain of GluD2 (GluRdelta2) recruits presynaptic terminals and regulates synaptogenesis in the cerebellum in vivo. J. Neurosci. 29, 5738-5748. doi: 10.1523/JNEUR0SCI.6013-08.2009
21. Kakegawa, W., and Yuzaki, M. (2005). A mechanism underlying AMPA receptor trafficking during cerebellar long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 102, 17846-17851. doi: 10.1073/pnas.0508910102
22. Kalmbach, B. E., Davis, T., Ohyama, T., Riusech, F., Nores, W. L., and Mauk, M. D. (2010). Cerebellar cortex contributions to the expression and timing of conditioned eyelid responses. J. Neurophysiol. 103, 2039-2049. doi: 10.1152/jn.00033.2010
23. Kishimoto, Y., Kawahara, S., Fujimichi, R., Mori, H., Mishina, M., and Kirino, Y. (2001a). Impairment of eyeblink conditioning in GluRdelta2-mutant mice depends on the temporal overlap between conditioned and unconditioned stimuli. Eur. J. Neurosci. 14, 1515-1521. doi: 10.1046/j.0953-816x.2001.01772.x
24. Kishimoto, Y., Kawahara, S., Suzuki, M., Mori, H., Mishina, M., and Kirino, Y. (2001b). Classical eyeblink conditioning in glutamate receptor subunit delta 2 mutant mice is impaired in the delay paradigm but not in the trace paradigm. Eur. J. Neurosci. 13,1249-1253. doi: 10.1046/j.0953-816x.2001.01488.x
25. Kleim, J. A., Freeman, J. H., Jr., Bruneau, R., Nolan, B. C., Cooper, N. R., Zook, A., et al. (2002). Synapse formation is associated with memory storage in the cerebellum. Proc. Natl. Acad. Sci. U.S.A. 99, 13228-13231. doi: 10.1073/pnas.202483399
26. Koekkoek, S. K., Hulscher, H. C., Dortland, B. R., Hensbroek, R. A., Elgersma, Y., Ruigrok, T. J., et al. (2003). Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301, 1736-1739. doi: 10.1126/science.1088383
27. Koekkoek, S. K., Yamaguchi, K., Milojkovic, B. A., Dortland, B. R., Ruigrok, T. J., Maex, R., et al. (2005). Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron 47, 339-352. doi: 10.1016/j.neuron.2005.07.005
28. Kohda, K., Kakegawa, W., Matsuda, S., Nakagami, R., Kakiya, N., and Yuzaki, M. (2007). The extreme C-terminus of GluRdelta2 is essential for induction of long-term depression in cerebellar slices. Eur. J. Neurosci. 25, 1357-1362. doi: 10.1111/j.1460-9568.2007.05412.x
29. Lev-Ram, V., Wong, S. T., Storm, D. R., and Tsien, R. Y. (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. doi: 10.1073/pnas.122206399
30. Matsuda, K., Miura, E., Miyazaki, T., Kakegawa, W., Emi, K., Narumi, S., et al. Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science 328, 363-368. doi: 10.1126/science.1185152
31. Matsuda, K., and Yuzaki, M. (2011). Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions. Eur. J. Neurosci. 33,1447-1461. doi: 10.1111/j.1460-9568.2011.07638.x
32. Matsuda, S., Miura, E., Matsuda, K., Kakegawa, W., Kohda, K., Watan- abe, M., etal. (2008). Accumulation of AMPA receptors in autophagosomes in neuronal axons lacking adaptor protein AP-4. Neuron 57, 730-745. doi: 10.1016/j.neuron.2008.02.012
33. Medina, J. F., Garcia, K. S., and Mauk, M. D. (2001). A mechanism for savings in the cerebellum. J. Neurosci. 21, 4081-4089.
34. Medina, J. F., Nores, W. L., and Mauk, M. D. (2002). Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416, 330-333. doi: 10.1038/416330a
35. Miller, M. J., Chen, N. K., Li, L., Tom, B., Weiss, C., Disterhoft, J. F., et al. (2003). fMRI of the conscious rabbit during unilateral classical eyeblink conditioning reveals bilateral cerebellar activation. J. Neurosci. 23, 11753-11758.
36. Miura, E., Iijima, T., Yuzaki, M., and Watanabe, M. (2006). Distinct expression of Cbln family mRNAs in developing and adult mouse brains. Eur. J. Neurosci. 24, 750-760. doi: 10.1111/j.1460-9568.2006.04950.x
37. Miyata, M., Kim, H. T., Hashimoto, K., Lee, T. K., Cho, S. Y., Jiang, H., et al. (2001). Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C beta4 mutant mice. Eur. J. Neurosci. 13, 1945-1954. doi: 10.1046/j.0953-816x.2001.01570.x
38. Nomura, T., Kakegawa, W., Matsuda, S., Kohda, K., Nishiyama, J., Takahashi, T., et al. (2012). Cerebellar long-term depression requires dephosphorylation of TARP in Purkinje cells. Eur. J. Neurosci. 35, 402-410. doi: 10.1111/j.1460- 9568.2011.07963.x
39. Plakke, B., Freeman, J. H., and Poremba, A. (2007). Metabolic mapping of the rat cerebellum during delay and trace eyeblink conditioning. Neurobiol. Learn. Mem. 88, 11-18. doi: 10.1016/j.nlm.2007.03.008
40. Porrill, J., and Dean, P. (2008). Silent synapses, LTP, and the indirect parallel-fibre pathway: computational consequences of optimal cerebellar noise-processing. PLoS Comput. Biol. 4:e1000085. doi: 10.1371/journal.pcbi.1000085
41. Qiao, X., Chen, L., Gao, H., Bao, S., Hefti, F., Thompson, R. F., et al. (1998). Cerebellar brain-derived neurotrophic factor-TrkB defect associated with impairment of eyeblink conditioning in Stargazer mutant mice. J. Neurosci. 18, 6990-6999.
42. Sakamoto, T., and Endo, S. (2010). Amygdala, deep cerebellar nuclei and red nucleus contribute to delay eyeblink conditioning in C57BL /6 mice. Eur. J. Neurosci. 32, 1537-1551. doi: 10.1111/j.1460-9568.2010.07406.x
43. Schonewille, M., Belmeguenai, A., Koekkoek, S. K., Houtman, S. H., Boele, H. J., Van Beugen, B. J., et al. (2010). Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron 67, 618-628. doi: 10.1016/j.neuron.2010.07.009
44. Schonewille, M., Gao, Z., Boele, H. J., Veloz, M. F., Amerika, W. E., Simek, A. A., et al. (2011). Reevaluating the role of LTD in cerebellar motor learning. Neuron 70, 43-50. doi: 10.1016/j.neuron.2011.02.044
45. Shutoh, F., Ohki, M., Kitazawa, H., Itohara, S., and Nagao, S. (2006). Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 139, 767-777. doi: 10.1016/j.neuroscience.2005.12.035
46. Sun, L. W. (2012). Transsynaptic tracing of conditioned eyeblink circuits in the mouse cerebellum. Neuroscience 203, 122-134. doi: 10.1016/j.neuroscience.2011. 12.017
47. Thompson, R. F., and Krupa, D. J. (1994). Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci. 17, 519-549. doi: 10.1146/annurev.ne.17.030194.002511
48. Thompson, R. F., and Steinmetz, J. E. (2009). The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162, 732-755. doi: 10.1016/j.neuroscience.2009.01.041
49. Uemura, T., Lee, S. J., Yasumura, M., Takeuchi, T., Yoshida, T., Ra, M., et al. Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141, 1068-1079. doi: 10.1016/j.cell.2010.04.035
50. van Alphen, A. M., and De Zeeuw, C. I. (2002). Cerebellar LTD facilitates but is not essential for long-term adaptation of the vestibulo-ocular reflex. Eur. J. Neurosci. 16,486-490. doi: 10.1046/j.1460-9568.2002.02094.x
51. Wada, N., Kishimoto, Y., Watanabe, D., Kano, M., Hirano, T., Funabiki, K., et al. (2007). Conditioned eyeblink learning is formed and stored without cerebellar granule cell transmission. Proc. Natl. Acad. Sci. U.S.A. 104, 16690-16695. doi: 10.1073/pnas.0708165104
52. Woodruff-Pak, D. S., Foy, M. R., Akopian, G. G., Lee, K. H., Zach, J., Nguyen, K. P., et al. (2010). Differential effects and rates of normal aging in cerebellum and hippocampus. Proc. Natl. Acad. Sci. U.S.A. 107, 1624-1629. doi: 10.1073/pnas.0914207107
53. Yamasaki, M., Miyazaki, T., Azechi, H., Abe, M., Natsume, R., Hagiwara, T., et al. Glutamate receptor delta2 is essential for input pathway-dependent regulation of synaptic AMPAR contents in cerebellar Purkinje cells. J. Neurosci. 31, 3362-3374. doi: 10.1523/JNEUR0SCI.5601-10.2011
54. Yuzaki, M. (2009). New (but old) molecules regulating synapse integrity and plasticity: Cbln1 and the delta2 glutamate receptor. Neuroscience 162, 633-643. doi: 10.1016/j.neuroscience.2008.12.002
55. Yuzaki, M. (2011). Cbln1 and its family proteins in synapse formation and maintenance. Curr. Opin. Neurobiol. 21,215-220. doi: 10.1016/j.conb.2011.01.010
56. Yuzaki, M. (2012). CerebellarLTDvs. motorlearning-Lessons learnedfromstudying GluD2. Neural Netw. 47, 36-41. doi: 10.1016/j.neunet.2012.07.001