Purkinje cell loss affects differentially the execution, acquisition and prepulse inhibition of skeletal and facial motor responses in Lurcher mice

European Journal of Neuroscience

Volumn 21, Issue 4, 2005, Pages 979-988

  Porras García, Elena ^a   Cendelin, Jan ^b   Domínguez Del Toro, Eduardo ^a   Vožeh, František ^b   Delgado García, José M ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Cerebellum; Classical conditioning; Eyelid responses; Motor learning; Startle response; Water maze

Indexed keywords

AMPLITUDE MODULATION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; BRAIN CORTEX; CELL LOSS; CEREBELLUM; CONDITIONING; CONTROLLED STUDY; EYELID; FACE MUSCLE; GRANULAR CELL; HETEROZYGOSITY; LATENT PERIOD; MALE; MAZE TEST; MOTOR ACTIVITY; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; PURKINJE CELL; SKELETAL MUSCLE; SPATIAL ORIENTATION; STARTLE REFLEX; STRAIN DIFFERENCE; SWIMMING; TASK PERFORMANCE; WILD TYPE;

ACOUSTIC STIMULATION; ANIMALS; BEHAVIOR, ANIMAL; CEREBELLAR CORTEX; CEREBELLAR DISEASES; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; ELECTROMYOGRAPHY; EVOKED POTENTIALS; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MOTOR ACTIVITY; MUSCLE, SKELETAL; NERVE DEGENERATION; NEURAL INHIBITION; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS; REACTION TIME; REFLEX, ACOUSTIC; SPATIAL BEHAVIOR;

EID: 16244394511     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03940.x     Document Type: Article

References (62)

1. Araki, K., Meguro, H., Kushiya, E., Takayama, C., Inoue, Y. & Mishina, M. (1993) Selective expression of the glutamate receptor channel delta 2 subunit in cerebellar Purkinje cells. Biochem. Biophys. Res. Commun., 197, 1267-1276.
2. Borrell, J., Vela, J.M., Arévalo-Martin, A., Molina-Holgado, E. & Guaza, C. (2002) Prenatal immune challenge disrupts sensorimotor gating in adult rats: implications for the etiopathogenesis of schizophrenia. Neuropsychopharmacology, 26, 204-215.
3. Brown, S.H., Kessler, K.R., Hefter, H., Cooke, J.D. & Freund, H.J. (1993) Role of the cerebellum in visuomotor coordination. I. Delayed eye and arm initiation in patients with mild cerebellar ataxia. Exp. Brain Res., 94, 478-488.
4. Caddy, K.W. & Biscoe, T.J. (1979) Structural and quantitative studies on the normal C3H and Lurcher mutant mouse. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 287, 167-201.
5. Caston, J., Vasseur, F., Stelz, T., Chianale, C., Delhaye-Bouchaud, N. & Mariani, J. (1995a) Differential roles of cerebellar cortex and deep cerebellar nuclei in the learning of equilibrium behavior: studies in intact and cerebellectomized Lurcher mutant mice. Dev. Brain Res., 86, 311-316.
6. Chen, L., Bao, S., Lockard, J.M., Kim, J.K. & Thompson, R.F. (1996) Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J. Neurosci., 16, 2829-2838.
7. Cheng, S.S. & Heintz, N. (1997) Massive loss of mid- and hindbrain neurons during embryonic development of homozygous Lurcher mice. J. Neurosci., 17, 2400-2407.
8. Dahhaoui, M., Lannou, J., Stelz, T., Caston, J, & Guastavino, J.M. (1992a) Role of the cerebellum in spatial orientation in the rat. Behav. Neural. Biol., 58, 180-189.
9. Dahhaoui, M., Stelz, T. & Caston, J. (1992b) Effects of lesion of the inferior olivary complex by 3-acetylpyridine on learning and memory in the rat. J. Comp. Physiol. A, 171, 657-664.
10. Delgado-García, J.M. & Gruart, A. (2002) The role of interpositus nucleus in eyelid conditioned responses. Cerebellum, 1, 289-308.
11. Domínguez-del-Toro, E., Rodríguez-Moreno, A., Porras-García, E., Sánchez-Campusano, R., Blanchard, V., Laville, M., Bohme, G.A., Benavides, J. & Delgado-García, J.M. (2004) An in vitro and in vivo study of early deficits in associative learning in transgenic mice that over-express a mutant form of human APP associated with Alzheimer's disease. Eur. J. Neurosci., 20, 1945-1952.
12. Doughty, M.L., De Jager, P.L., Korsmeyer, S.J. & Heintz, N. (2000) Neurodegeneration in Lurcher mice occurs via multiple cell death pathways. J. Neurosci., 20, 3687-3694.
13. Fendt, M., Li, L. & Yeomans, J.S. (2001) Brain stem circuits mediating prepulse inhibition of the startle reflex. Psychopharmacology, 156, 216-224.
14. Gandhi, C.C., Kelly, R.M., Wiley, R.G. & Walsh, T.J. (2000) Impaired acquisition of a Morris water maze task following selective destruction of cerebellar Purkinje cells with OX7-saporin. Behav. Brain Res., 109, 37-47.
15. Gruart, A., Blázquez, P. & Delgado-García, J.M. (1995) Kinematics of unconditioned and conditioned eyelid movements in the alert cat. J. Neurophysiol., 74, 226-248.
16. Gruart, A., Schreurs, B.G., Domínguez del Toro, E. & Delgado-García, J.M. (2000) Kinetic and frequency-domain properties of reflex and conditioned eyelid responses in the rabbit. J. Neurophysiol., 83, 836-852.
17. Heckroth, J.A. (1994) Quantitative morphological analysis of the cerebellar nuclei in normal and Lurcher mutant mice. I. Morphology and cell number. J. Comp. Neurol., 343, 173-182.
18. Heckroth, J.A. & Eisenman, L.M. (1991) Olivary morphology and olivocerebellar pathology in adult Lurcher mutant mice. J. Comp. Neurol., 312, 641-651.
19. Hilber, P. & Caston, J. (2001) Motor skills and motor learning in Lurcher mutant mice during aging. Neuroscience, 102, 615-623.
20. Hilber, P., Jouen, F., Delhaye-Bouchaud, N., Mariani, J. & Caston, J. (1998) Differential roles of cerebellar cortex and deep cerebellar nuclei in learning and retention of a spatial task: studies in intact and cerebellectomized Lurcher mutant mice. Behav. Genet., 28, 299-308.
21. Ivry, R.B. & Baldo, J.V. (1992) Is the cerebellum involved in learning and cognition? Curr. Opin. Neurobiol., 2, 212-216.
22. 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.
23. Kishimoto, Y., Fujimichi, R., Araishi, K., Kawahara, S., Kano, M., Aiba, A. & Kirino, Y. (2002) mGluR1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Eur. J. Neurosci., 16, 2416-2424.
24. Kishimoto, Y., Kawahara, S., Suzuki, M., Mori, H., Mishina, M. & Kirino, Y. (2001) 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.
25. Koch, M. (1999) The neurobiology of startle. Prog. Neurobiol., 59, 107-128.
26. Koekkoek, S.K.E., Hulscher, H.C., Dortland, B.R., Hensbroek, R.A., Elgersma, Y., Ruigrok, T.J.H. & De Zeeuw, C.I. (2003) Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science, 301, 1736-1739.
27. Křižkova, A. & Vožeh, F. (2004) Development of early motor learning and topical motor skills in a model of cerebellar degeneration. Behav. Brain Res., 150, 65-72.
28. Kugelberg, E. (1952) Facial reflexes. Brain, 75, 385-396.
29. Lalonde, R. (1987) Exploration and spatial learning in staggerer mutant mice. J. Neurogenet., 4, 285-292.
30. Lalonde, R. (1994a) Cerebellar contributions to instrumental learning. Neurosci. Biobehav. Rev., 18, 161-170.
31. Lalonde, R. (1994b) Motor learning in Lurcher mutant mice. Brain Res., 639, 351-353.
32. Lalonde, R., Botez, M.I., Joyal, C.C. & Caumartin, M. (1992) Motor abnormalities in Lurcher mutant mice. Physiol. Behav., 51, 523-525.
33. Lalonde, R. & Strazielle, C. (2003) The effects of cerebellar damage on maze learning in animals. Cerebellum, 2, 300-309.
34. 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.
35. Le Marec, N., Caston, J. & Lalonde, R. (1997) Impaired motor skills on static and mobile beams in Lurcher mutant mice. Exp. Brain Res., 116, 131-138.
36. Leaton, R.N. & Supple, W.F. Jr (1986) Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science, 232, 513-515.
37. Leaton, R.N. & Supple, W.F. Jr (1991) Medial cerebellum and long-term habituation of acoustic startle in rats. Behav. Neurosci., 105, 804-816.
38. Leggio, M.G., Neri, P., Graziano, A., Mandolesi, L., Molinari, M. & Petrosini, L. (1999) Cerebellar contribution to spatial event processing: characterization of procedural learning. Exp. Brain Res., 127, 1-11.
39. Leiner, H.C., Leiner, A.L. & Dow, R.S. (1993) Cognitive and language functions of the human cerebellum. Trends Neurosci., 16, 444-447.
40. Lomeli, H., Sprengel, R., Laurie, D.J., Kohr, G., Herb, A., Seeburg, P.H. & Wisden, W. (1993) The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett., 315, 318-322.
41. Martin, L.A., Goldowitz, D. & Mittleman, G. (2003) The cerebellum and spatial ability: dissection of motor and cognitive components with a mouse model system. Eur. J. Neurosci., 18, 2002-2010.
42. Mayat, E., Petralia, R.S., Wang, Y.X. & Wenthold, R.J. (1995) Immunoprecipitation, immunoblotting, and immunocytochemistry studies suggest that glutamate receptor delta subunits form novel postsynaptic receptor complexes. J. Neurosci., 15, 2533-2546.
43. Molinari, M., Petrosini, L., Misciagna, S. & Leggio, M.G. (2004) Visuospatial abilities in cerebellar disorders. J. Neurol. Neurosurg. Psychiatry, 75, 235-240.
44. Morcuende, S., Trigo, J.A., Delgado-García, J.M. & Gruart, A. (2001) Harmaline induces different motor effects on facial vs. skeletal-motor systems in alert cats. Neurotox. Res., 3, 527-535.
45. Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Meth., 11, 47-60.
46. Norman, D.J., Feng, L., Cheng, S.S., Gubbay, J., Chan, E. & Heintz, N. (1995) The Lurcher gene induces apoptotic death in cerebellar Purkinje cells. Development, 121, 1183-1193.
47. Ogura, H., Aruga, J. & Mikoshiba, K. (2001) Behavioral abnormalities of Zic1 and Zic2 mutant mice: implications as models for human neurological disorders. Behav. Genet., 31, 317-324.
48. Petrosini, L., Molinari, M. & Dell'Anna, M.E. (1996) Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur. J. Neurosci., 8, 1882-1896.
49. Phillips, R.J.S. (1960) Lurcher, a new gene in linkage group XI of house mouse. J. Genet., 57, 35-42.
50. Raymond, J.L., Lisberger, S.G. & Mauk, M.D. (1996) The cerebellum: a neuronal learning machine? Science, 272, 1126-1131.
51. Resibois, A., Cuvelier, L. & Goffinet, A.M. (1997) Abnormalities in the cerebellum and brainstem in homozygous Lurcher mice. Neuroscience, 80, 175-190.
52. de'Sperati, C., Lopiano, L. & Montarolo, P.O. (1989) Lesions of the inferior olive do not affect long- or short-term habituation of the acoustic startle response in rats. Neurosci. Lett., 100, 164-168.
53. Takatsuki, K., Kawahara, S., Kotani, S., Fukunaga, S., Mori, H., Mishina, M. & Kirino, Y. (2003) The hippocampus plays an important role in eyeblink conditioning with a short trace interval in glutamate receptor subunit δ2 mutant mice. J. Neurosci., 23, 17-22.
54. Takayama, C., Nakagawa, S., Watanabe, M., Mishina, M. & Inoue, Y. (1995) Light- and electron-microscopic localization of the glutamate receptor channel delta 2 subunit in the mouse Purkinje cell. Neurosci. Lett., 188, 89-92.
55. Takayama, C., Nakagawa, S., Watanabe, M., Mishina, M. & Inoue, Y. (1996) Developmental changes in expression and distribution of the glutamate receptor channel delta 2 subunit according to the Purkinje cell maturation. Brain Res. Dev. Brain Res., 92, 147-155.
56. 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.
57. Van Alphen, A.M., Schepers, T., Luo, C. & De Zeeuw, C.I. (2002) Motor performance and motor learning in Lurcher mice. Ann. NY Acad. Sci., 978, 413-424.
58. Wetts, R. & Herrup, K. (1982a) Interaction of granule, Purkinje and inferior olivary neurons in Lurcher chimaeric mice. I. Qualitative studies. J. Embryol. Exp. Morph., 68, 87-98.
59. Wetts, R. & Herrup, K. (1982b) Interaction of granule, Purkinje and inferior olivary neurons in Lurcher chimaeric mice. II. Granule cell death. Brain Res., 250, 358-362.
60. Wetts, R. & Herrup, K. (1982c) Cerebellar Purkinje cells are descended from a small number of progenitors committed during early development: quantitative analysis of Lurcher chimaeric mice. J. Neurosci., 2, 1494-1498.
61. Wullner, U., Loschmann, P.A., Weller, M. & Klockgether, T. (1995) Apoptotic cell death in the cerebellum of mutant weaver and Lurcher mice. Neurosci. Lett., 200, 109-112.
62. Zuo, J., De Jager, P.L., Takahashi, K.A., Jiang, W., Linden, D.J. & Heintz, N. (1997) Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature, 388, 769-773.