Impairment of eyeblink conditioning in GluRδ2-mutant mice depends on the temporal overlap between conditioned and unconditioned stimuli

European Journal of Neuroscience

Volumn 14, Issue 9, 2001, Pages 1515-1521

  Kishimoto, Yasushi ^a,d   Kawahara, Shigenori ^a,c   Fujimichi, Ryoko ^a   Mori, Hisashi ^b   Mishina, Masayoshi ^b,c   Kirino, Yutaka ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d KANAZAWA UNIVERSITY   (Japan)

Author keywords

Associative learning; Cerebellar LTD; Motor learning; Purkinje cell

Indexed keywords

GLUTAMATE RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONDITIONING; CONTROLLED STUDY; DISEASE SEVERITY; EYELID REFLEX; GENE MUTATION; LEARNING DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; STIMULUS RESPONSE; WILD TYPE;

ANIMALS; CEREBELLUM; CONDITIONING, EYELID; ELECTROMYOGRAPHY; GENOTYPE; GLUTAMIC ACID; LEARNING; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; REACTION TIME; RECEPTORS, GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 0035783468     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.0953-816X.2001.01772.x     Document Type: Article

References (44)

1. Aiba, A., Kano, M., Chen, C., Stanton, M.E., Fox, G.D., Herrup, K., Zwingman, T.A. & Tonegawa, S. (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell, 79, 377-388.
2. Aizenman, C.D. & Linden, D.J. (2000) Rapid, synaptically driven increase in the intrinsic excitability of cerebellar deep nuclear neurons. Nature Neurosci., 3, 109-111.
3. Aizenman, C.D., Manis, P.B. & Linden, D.J. (1998) Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron, 21, 827-835.
4. Araki, K., Meguro, H., Kushiya, E., Takayama, C., Inoue, Y. & Mishina, M. (1993) Selective expression of the glutamate receptor channel δ2 subunit in cerebellar Purkinje cells. Biochem. Biophys. Res. Commun., 197, 1267-1276.
5. 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.
6. Berger, T.W., Alger, B. & Thompson, R.F. (1976) Neuronal substrate of classical conditioning in the hippocampus. Science, 192, 483-485.
7. Chen, C. & Thompson, R.F. (1995) Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slice. Learn. Mem., 2, 185-198.
8. Clark, R.E. & Squire, L.R. (1998) Classical conditioning and brain systems: The role of awareness. Science, 280, 77-81.
9. Ekerot, C.F. & Kano, M. (1989) Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neurosci. Res., 6, 264-268.
10. Espinosa, I.E. & Gerstein, G.L. (1988) Cortical auditory neuron interactions during presentation of 3-tone sequences: Effective connectivity. Brain Res., 450, 39-50.
11. Getting, P.A. (1989) Emerging principles governing the operation of neural networks. Annu. Rev. Neurosci., 12, 185-204.
12. Gilbert, C.D. & Wiesel, T.N. (1992) Receptive field dynamics in adult primary visual cortex. Nature, 356, 150-152.
13. Hansel, C., Linden, D.J. & D'Angelo, E.D. (2001) Beyond parallel fiber LTD: The diversity of synaptic and non-synaptic plasticity in the cerebellum. Nature Neurosci., 4, 467-475.
14. Hironaka, K., Umemori, H., Tezuka, T., Mishina, M. & Yamamoto, T. (2000) The Protein-tyrosine phosphatase PTPMEG interacts with glutamate receptor δ2 and ε subunits. J. Biol. Chem., 275, 16167-16173.
15. Hoehler, F.K. & Thompson, R.F. (1980) Effect of the interstimulus (CS-UCS) interval on hippocampal unit activity during classical conditioning of the nictitating membrane response of the rabbit (Oryctolagus cuniculus). J. Comp. Physiol. Psychol., 94, 201-215.
16. Ito, M. (1989) Long-term depression. Annu. Rev. Neurosci., 12, 85-102.
17. Ito, M. (2000) Mechanisms of motor learning in the cerebellum. Brain. Res., 886, 237-245.
18. Kano, M., Rexhausen, U., Dreessen, J. & Konnerth, A. (1992) Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature, 356, 601-604.
19. Kashiwabuchi, N., Ikeda, K., Araki, K., Hirano, T., Shibuki, K., Takayama, C., Inoue, Y., Kutsuwada, T., Yagi, T., Kang, Y., Aizawa, S. & Mishina, M. (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell, 81, 245-252.
20. Kishimoto, Y., Hirono, M., Sugiyama, T., Kawahara, S., Nakao, K., Kishio, M., Katsuki, M., Yoshioka, T. & Kirino, Y. (2001a) Impaired delay but normal trace eyeblink conditioning in PLCβ4 mutant mice. Neuroreport, 12, 2919-2922.
21. Kishimoto, Y., Kawahara, S., Mori, S., Mishina, M. & Kirino, Y. (2001b) Long trace interval eyeblink conditioning is impaired in mutant mice lacking NMDA receptor subunit ε1. Eur. J. Neurosci., 13, 1221-1227.
22. Kishimoto, Y., Kawahara, S., Suzuki, M., Mori, H., Mishina, M. & Kirino, Y. (2001c) Classical eyeblink conditioning in glutamate receptor subunit δ2 mutant mice is impaired in the delay paradigm but not in the trace paradigm. Eur. J. Neurosci., 13, 1249-1253.
23. Kohda, K., Wang, Y. & Yuzaki, M. (2000) Mutation of a glutamate receptor motif reveals its role in gating and δ2 receptor channel properties. Nature Neurosci., 3, 315-322.
24. Kurihara, H., Hashimoto, K., Kano, M., Takayama, C., Sakimura, K., Mishina, M., Inoue, Y. & Watanabe, M. (1997) Impaired parallel fiber-Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor δ2 subunit. J. Neurosci., 17, 9613-9623.
25. Landsend, A.S., Amiry-Moghaddam, M., Matsubara, A., Bergersen, L., Usami, S., Wenthold, R.J. & Ottersen, O.P. (1997) Differential localization of delta glutamate receptors in the rat cerebellum: Coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber-spine synapses. J. Neurosci., 17, 834-842.
26. Manns, J.R., Clark, R.E. & Squire, L.R. (2000) Awareness predicts the magnitude of single-cue trace eyeblink conditioning. Hippocampus, 10, 181-186.
27. Mauk, M.D. & Donegan, N.H. (1997) A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn. Mem., 4, 130-158.
28. McCormick, D.A. & Thompson, R.F. (1984) Cerebellum: Essential involvement in the classically conditioned eyelid response. Science, 223, 296-299.
29. Meyrand, P., Simmers, J. & Moulins, M. (1991) Construction of a pattern-generating circuit with neurons of different networks. Nature, 351, 60-63.
30. Morishita, W. & Sastry, B.R. (1996) Postsynaptic mechanisms underlying long-term depression of GABAergic transmission in neurons of the deep cerebellar nuclei. J. Neurophysiol., 76, 59-68.
31. Moyer, J.R. Jr, Deyo, R.A. & Disterhoft, J.F. (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosci., 104, 243-252.
32. Racine, R.J., Wilson, D.A., Gingell, R. & Sunderland, D. (1986) Long-term potentiation in the interpositus and vestibular nuclei in the rat. Exp. Brain Res., 63, 158-162.
33. Schneiderman, N. & Gormezano, I. (1964) Conditioning of the nictitating membrane of the rabbit as a function of CS-US interval. J. Comp. Physiol. Psychol., 57, 188-195.
34. Shibuki, K., Gomi, H., Chen, L., Bao, S., Kim, J.J., Wakatsuki, H., Fujisaki, T., Fujimoto, K., Katoh, A., Ikeda, T., Chen, C., Thompson, R.F. & Itohara, S. (1996) Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron, 16, 587-599.
35. Smith, M.C. & Gormezano, I. (1969) Classical conditioning of the rabbit's nictitating membrane response at backward, simultaneous, and forward CS-US intervals. J. Comp. Physiol. Psychol., 69, 226-231.
36. Solomon, P.R., Solomon, S.D., Vander Schaaf, E. & Perry, H.E. (1983) Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science, 220, 329-331.
37. Solomon, P.R., Vander Schaaf, E.R., Thompson, R.F. & Weisz, D.J. (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci., 100, 729-744.
38. Thompson, R.F., Bao, S., Chen, L., Cipriano, B.D., Grethe, J.S., Kim, J.J., Thompson, J.K., Tracy, J.A., Weninger, M.S. & Krupa, D.J. (1997) Associative learning. In Schmahmann, J.D. (ed.), Cerebellum and Cognition. Academic Press, San Diego, pp. 151-189.
39. Thompson, R.F. & Kim, J.J. (1996) Memory systems in the brain and localization of a memory. Proc. Natl Acad. Sci. USA, 93, 13438-13444.
40. Thompson, R.F. & Krupa, D.J. (1994) Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci., 17, 519-549.
41. Weiss, C., Bouwmeester, H., Power, J.M. & Disterhoft, J.F. (1999) Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav. Brain Res., 99, 123-132.
42. Woodruff-Pak, D.S., Lavond, D.G. & Thompson, R.F. (1985) Trace conditioning: Abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations. Brain Res., 348, 249-260.
43. Woodruff-Pak, D.S., Logan, C.G. & Thompson, R.F. (1990) Neurobiological substrates of classical conditioning across the life span. Ann. NY Acad. Sci., 608, 150-173.
44. Zeki, S. (1983) Colour coding in the cerebral cortex: The reaction of cells in monkey visual cortex to wavelengths and colours. Neuroscience, 9, 741-765.