Impaired motor learning in the vestibulo-ocular reflex in mice with multiple climbing fiber input to cerebellar Purkinje cells

Journal of Neuroscience

Volumn 27, Issue 21, 2007, Pages 5672-5682

  Kimpo, Rhea R ^a   Raymond, Jennifer L ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Cerebellum; Climbing fiber; Motor learning; Mouse; Oculomotor; Vestibulo ocular reflex

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; LEARNING; LEARNING DISORDER; MALE; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SENSORIMOTOR FUNCTION; VESTIBULOOCULAR REFLEX; ANIMAL; CEREBELLUM; COMPARATIVE STUDY; CYTOLOGY; HEAD MOVEMENT; METHODOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; TRANSGENIC MOUSE;

ANIMALS; CEREBELLUM; HEAD MOVEMENTS; LEARNING; MALE; MICE; MICE, TRANSGENIC; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; PURKINJE CELLS; REFLEX, VESTIBULO-OCULAR;

EID: 34250672720     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0801-07.2007     Document Type: Article

References (105)

1. Abeliovich A, Chen C, Goda Y, Silva AJ, Stevens CF, Tonegawa S (1993a) Modified hippocampal long-term potentiation in PKCγ-mutant mice. Cell 75:1253-1262.
2. Abeliovich A, Paylor R, Chen C, Kim JJ, Wehner JM, Tonegawa S (1993b) PKCγ mutant mice exhibit mild deficits in spatial and contextual learning. Cell 75:1263-1271.
3. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25-61.
4. Bannerman DM, Deacon RM, Seeburg PH, Rawlins JN (2003) GluR-A-Deficient mice display normal acquisition of a hippocampus-dependent spatial reference memory task but are impaired during spatial reversal. Behav Neurosci 117:866-870.
5. Bao S, Chen L, Kim JJ, Thompson RF (2002) Cerebellar cortical inhibition and classical eyeblink conditioning. Proc Natl Acad Sci USA 99:1592-1597.
6. Bareggi R, Narducci P, Grill V, Lach S, Martelli AM (1996) Selective distribution of multiple protein kinase C isoforms in mouse cerebellar cortex. Biol Cell 87:55-63.
7. Barmack NH, Qian Z, Yoshimura J (2000) Regional and cellular distribution of protein kinase C in rat cerebellar Purkinje cells. J Comp Neurol 427:235-254.
8. Beck JC, Gilland E, Tank DW, Baker R (2004) Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 92:3546-3561.
9. Ben-Shlomo H, Sigmund O, Stabel S, Reiss N, Naor Z (1991) Preferential release of catecholamine from permeabilized PC12 cells by alpha- and beta-type protein kinase C subspecies. Biochem J 280:65-69.
10. Boyden ES, Raymond JL (2003) Active reversal of motor memories reveals rules governing memory encoding. Neuron 39:1031-1042.
11. Boyden ES, Katoh A, Pyle JL, Chatila TA, Tsien RW, Raymond JL (2006) Selective engagement of plasticity mechanisms for motor memory sorage. Neuron 51:823-834.
12. Brandon NJ, Uren JM, Kittler JT, Wang H, Olsen R, Parker PJ, Moss SJ (1999) Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci 19:9228-9234.
13. Cambray-Deakin M, Adu J, Burgoyne R (1990) Neuritogenesis in cerebellar granule cells in vitro: a role for protein kinase C. Brain Res Dev Brain Res 53:40-46.
14. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim J, Hashimoto K, Thompson RF, Tonegawa S (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKCγ mutant mice. Cell 83:1233-1242.
15. Chen L, Bao S, Lockard J, Kim J, Thompson R (1996) Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J Neurosci 16:2829-2838.
16. Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691-700.
17. Coffey E, Sihra T, Nicholls D (1993) Protein kinase C and the regulation of glutamate exocytosis from cerebrocortical synaptosomes. J Biol Chem 268:21060-21065.
18. Colin F, Manil J, Desclin JC (1980) The olivocerebellar system. I. Delayed and slow inhibitory effects: an overlooked salient feature of cerebellar climbing fibers. Brain Res 187:3-27.
19. De Zeeuw CI, van Alphen AM, Koekkoek SK, Buharin E, Coesmans M, Morpurgo MM, van den Burg J (1998a) Recording eye movements in mice: a new approach to investigate the molecular basis of cerebellar control of motor learning and motor timing. Otolaryngol Head Neck Surg 119:193-203.
20. De Zeeuw CI, Hansel C, Bian F, Koekkoek SK, van Alphen AM, Linden DJ, Oberdick J (1998b) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495-508.
21. Demer JL, Echelman DA, Robinson DA (1985) Effects of electrical stimulation and reversible lesions of the olivocerebellar pathway on Purkinje cell activity in the flocculus of the cat. Brain Res 346:22-31.
22. Eccles JC, Ito M, Szentagothai J (1967) The cerebellum as a neuronal learning machine. Berlin: Springer.
23. 2+ signaling induces cerebellar long-term depression. Learn Mem 4:159-168.
24. Fan H-Y, Tong C, Li M-Y, Lian L, Chen D-Y, Schatten H, Sun Q-Y (2002) Translocation of the classic protein kinase C isoforms in porcine oocytes: implications of protein kinase C involvement in the regulation of nuclear activity and cortical granule exocytosis. Exp Cell Res 277:183-191.
25. Garcia MM, Harlan RE (1997) Protein kinase C in central vestibular, cerebellar, and precerebellar pathways of the rat. J Comp Neurol 385:26-42.
26. Gerwig M, Hajjar K, Dimitrova A, Maschke M, Kolb FP, Frings M, Thilmann AF, Forsting M, Diener HC, Timmann D (2005) Timing of conditioned eyeblink responses is impaired in cerebellar patients. J Neurosci 25:3919-3931.
27. Ghoumari AM, Wehrle R, De Zeeuw CI, Sotelo C, Dusart I (2002) Inhibition of protein kinase C prevents Purkinje cell death but does not affect axonal regeneration. J Neurosci 22:3531-3542.
28. Gilbert PF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309-328.
29. Godaux E, Gobert C, Halleux J (1983) Vestibuloocular reflex, optokinetic response, and their interactions in the alert cat. Exp Neurol 80:42-54.
30. Goossens J, Daniel H, Rancillac A, van der Steen J, Oberdick J, Crepel F, De Zeeuw CI, Frens MA (2001) Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice. J Neurosci 21:5813-5823.
31. Gruart A, Schreurs BG, Dominguez del Toro E, Delgado-Garcia JM (2000) Kinetic and frequency-domain properties of reflex and conditioned eyelid responses in the rabbit. J Neurophysiol 83:836-852.
32. Gundlfinger A, Kapfhammer J, Kruse F, Leitges M, Metzger M (2003) Different regulation of Purkinje cell dendritic development in cerebellar slice cultures by protein kinase C alpha and beta. J Neurobiol 57:95-109.
33. Haddad GM, Demer JL, Robinson DA (1980) The effect of lesions of the dorsal cap of the inferior olive on the vestibulo-ocular and optokinetic systems of the cat. Brain Res 185:265-275.
34. Hansel C, Linden DJ (2000) Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Neuron 26:473-482.
35. Hansel C, de Jeu M, Belmeguenai A, Houtman SH, Buitendijk GH, Andreev D, De Zeeuw CI, Elgersma Y (2006) αCaMKII is essential for cerebellar LTD and motor learning. Neuron 51:835-843.
36. Hartell NA (1996) Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron 16:601-610.
37. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796.
38. Hashimoto T, Ase K, Sawamura S, Kikkawa U, Saito N, Tanaka C, Nishizuka Y (1988) Postnatal development of a brain-specific subspecies of protein kinase C in rat. J Neurosci 8:1678-1683.
39. Hesslow G, Ivarsson M (1996) Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Exp Brain Res 110:36-46.
40. Huang F, Young W, Yoshida Y, Huang K (1990) Developmental expression of protein kinase C isozymes in rat cerebellum. Brain Res Dev Brain Res 52:121-130.
41. Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in Rhesus monkey. J Neurophysiol 88:13-28.
42. Ito M (1972) Neural design of the cerebellar motor control system. Brain Res 40:81-84.
43. Ito M, Sakurai M, Tongroach P (1982a) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol (Lond) 324:113-134.
44. Ito M, Jastreboff PJ, Miyashita Y (1982b) Specific effects of unilateral lesions in the flocculus upon eye movements in albino rabbits. Exp Brain Res 42:233-242.
45. Ivarsson M, Svensson P (2000) Conditioned eyeblink response consists of two distinct components. J Neurophysiol 83:796-807.
46. Ivkovich D, Thompson RF (1997) Motor cortex lesions do not affect learning or performance of the eyeblink response in rabbits. Behav Neurosci 111:727-738.
47. Iwashita M, Kanai R, Funabiki K, Matsuda K, Hirano T (2001) Dynamic properties, interactions and adaptive modifications of vestibulo-ocular reflex and optokinetic response in mice. Neurosci Res 39:299-311.
48. Jirenhed D-A, Bengtsson F, Hesslow G (2007) Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci 27:2493-2502.
49. Jorntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34:797-806.
50. Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535-538.
51. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, Watanabe M, Inoue Y, Tonegawa S (1995) Impaired synapse elimination during cerebellar development in PKC gamma mutant mice. Cell 83:1223-1231.
52. Katoh A, Kitazawa H, Itohara S, Nagao S (1998) Dynamic characteristics and adaptability of mouse vestibulo-ocular and optokinetic response eye movements and the role of the flocculo-olivary system revealed by chemical lesions. Proc Natl Acad Sci USA 95:7705-7710.
53. Katoh A, Yoshida T, Himeshima Y, Mishina M, Hirano T (2005) Defective control and adaptation of reflex eye movements in mutant mice deficient in either the glutamate receptor 2 subunit or Purkinje cells. Eur J Neurosci 21:1315-1326.
54. Katoh A, Jindal JA, Raymond JL (2007) Motor deficits in homozygous and heterozygous P/Q-type calcium channel mutants. J Neurophysiol 97:1280-1287.
55. Kim JJ, Krupa DJ, Thompson RF (1998) Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279:570-573.
56. Kimpo RR, Boyden ES, Katoh A, Ke MC, Raymond JL (2005) Distinct patterns of stimulus generalization of increases and decreases in VOR gain. J Neurophysiol 94:3092-3100.
57. Kishimoto Y, Kawahara S, Fujimichi R, Mori H, Mishina M, Kirino Y (2001) Impairment of eyeblink conditioning in GluRdelta2-mutant mice depends on the temporal overlap between conditioned and unconditioned stimuli. Eur J Neurosci 14:1515-1521.
58. Koekkoek SK, van Alphen AM, van den Burg J, Grosveld F, Galjart N, De Zeeuw CI (1997) Gain adaptation and phase dynamics of compensatory eye movements in mice. Genes Funct 1:175-190.
59. Koekkoek SK, Hulscher HC, Dortland BR, Hensbroek RA, Elgersma Y, Ruigrok TJ, De Zeeuw CI (2003) Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301:1736-1739.
60. Koekkoek SKE, Yamaguchi K, Milojkovic BA, Dortland BR, Ruigrok TJH, Maex R, De Graaf W, Smit AE, VanderWerf F, Bakker CE (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.
61. Kotani S, Kawahara S, Kirino Y (2006) Purkinje cell activity during classical eyeblink conditioning in decerebrate guinea pigs. Brain Res 1068:70-81.
62. Le Marec N, Lalonde R (1997) Sensorimotor learning and retention during equilibrium tests in Purkinje cell degeneration mutant mice. Brain Res 768:310-316.
63. Lee T, Kim JJ (2004) Differential effects of cerebellar, amygdalar, and hippocampal lesions on classical eyeblink conditioning in rats. J Neurosci 24:3242-3250.
64. Leitges M, Kovac J, Plomann M, Linden DJ (2004) A unique PDZ ligand in PKCα confers induction of cerebellar long-term synaptic depression. Neuron 44:585-594.
65. Lisberger SG (1984) The latency of pathways containing the site of motor learning in the monkey vestibulo-ocular reflex. Science 225:74-76.
66. Lisberger SG, Miles FA, Zee DS (1984) Signals used to compute errors in monkey vestibuloocular reflex: possible role of flocculus. J Neurophysiol 52:1140-1153.
67. Lisberger SG, Pavelko TA, Broussard DM (1994) Responses during eye movements of brain stem neurons that receive monosynaptic inhibition from the flocculus and ventral paraflocculus in monkeys. J Neurophysiol 72:909-927.
68. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, Hausser M (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation 8:202-211.
69. Luebke AE, Robinson DA (1994) Gain changes of the cat's vestibulo-ocular reflex after flocculus deactivation. Exp Brain Res 98:379-390.
70. Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437-470.
71. Marsh E, Baker R (1997) Normal and adapted visuooculomotor reflexes in goldfish. J Neurophysiol 77:1099-1118.
72. Martin WJ, Malmberg AB, Basbaum AI (2001) PKCγ contributes to a subset of the NMDA-dependent spinal circuits that underlie injury-induced persistent pain. J Neurosci 21:5321-5327.
73. Mauk MD, Ruiz BP (1992) Learning-dependent timing of Pavlovian eyelid responses: differential conditioning using multiple interstimulus intervals. Behav Neurosci 106:666-681.
74. Mauk MD, Steinmetz JE, Thompson RF (1986) Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc Natl Acad Sci USA 83:5349-5353.
75. McElligott JG, Beeton P, Polk J (1998) Effect of cerebellar inactivation by lidocaine microdialysis on the vestibuloocular reflex in goldfish. J Neurophysiol 79:1286-1294.
76. McKay BE, Engbers JD, Mehaffey WH, Gordon GRJ, Molineux ML, Bains JS, Turner RW (2007) Climbing fiber discharge regulates cerebellar functions by controlling the intrinsic characteristics of Purkinje cell output. J Neurophysiol 97:2590-2604.
77. Moriya M, Tanaka S (1994) Prominent expression of protein kinase Cγ mRNA in the dendrite-rich neuropil of mice cerebellum at the critical period for synaptogenesis. NeuroReport 5:929-932.
78. Nagao S (1983) Effects of vestibulocerebellar lesions upon dynamic characteristics and adaptation of the vestibulo-ocular and optokinetic responses in pigmented rabbits. Exp Brain Res 53:36-46.
79. Nishiyama H, Linden DJ (2004) Differential maturation of climbing fiber innervation in cerebellar vermis. J Neurosci 24:3926-3932.
80. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13:1708-1718.
81. 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.
82. 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.
83. Raymond JL, Lisberger SG (1996) Behavioral analysis of signals that guide learned changes in the amplitude and dynamics of the vestibulo-ocular reflex. J Neurosci 16:7791-7802.
84. Raymond JL, Lisberger SG (1998) Neural learning rules for the vestibuloocular reflex. J Neurosci 18:9112-9129.
85. Reisel D, Bannerman DM, Schmitt WB, Deacon RM, Flint J, Borchardt T, Seeburg PH, Rawlins JN (2002) Spatial memory dissociations in mice lacking GluR1. Nat Neurosci 5:868-873.
86. Robinson DA (1963) Method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Electronics 10:137-145.
87. Saito N, Shirai Y (2002) Protein kinase Cγ (PKCγ): function of neuron specific isotype. J Biochem (Tokyo) 132:683-687.
88. Saito N, Kikkawa U, Nishizuka Y, Tanaka C (1988) Distribution of protein kinase C-like immunoreactive neurons in rat brain. J Neurosci 8:369-382.
89. 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.
90. Schrenk K, Kapfhammer JP, Metzger F (2002) Altered dendritic development of cerebellar Purkinje cells in slice cultures from protein kinase Cγ-deficient mice. Neuroscience 110:675-689.
91. Schweigart G, Mergner T, Evdokimidis I, Morand S, Becker W (1997) Gaze stabilization by optokinetic reflex (OKR) and vestibulo-ocular reflex (VOR) during active head rotation in man. Vision Res 37:1643-1652.
92. Sears LL, Steinmetz JE (1991) Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545:114-122.
93. Shutoh F, Katoh A, Kitazawa H, Aiba A, Itohara S, Nagao S (2002) Loss of adaptability of horizontal optokinetic response eye movements in mGluR1 knockout mice. Neurosci Res 42:141-145.
94. Shutoh F, Katoh A, Ohki M, Itohara S, Tonegawa S, Nagao S (2003) Role of protein kinase C family in the cerebellum-dependent adaptive learning of horizontal optokinetic response eye movements in mice. Eur J Neurosci 18:134-142.
95. Silinsky EM, Searl TJ (2003) Phorbol esters and neurotransmitter release: more than just protein kinase C? Br J Pharmacol 138:1191-1201.
96. Smith MC, Coleman SR, 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.
97. Stahl JS, van Alphen AM, De Zeeuw CI (2000) A comparison of video and magnetic search coil recordings of mouse eye movements. J Neurosci Methods 99:101-110.
98. Tanaka C, Saito N (1992) Localization of subspecies of protein kinase C in the mammalian central nervous system. Neurochem Int 21:499-512.
99. Tatsukawa T, Chimura T, Miyakawa H, Yamaguchi K (2006) Involvement of basal protein kinase C and extracellular signal-regulated kinase 1/2 activities in constitutive internalization of AMPA receptors in cerebellar Purkinje cells. J Neurosci 26:4820-4825.
100. 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.
101. Van Alphen AM, Stahl JS, De Zeeuw CI (2001) The dynamic characteristics of the mouse horizontal vestibulo-ocular and optokinetic response. Brain Res 890:296-305.
102. Van Beugen BJ, Nagaraja RY, Hansel C (2006) Climbing fiber-evoked endocannabinoid signaling heterosynaptically suppresses presynaptic cerebellar long-term potentiation. J Neurosci 26:8289-8294.
103. Van Der Zee EA, Luiten PGM, Disterhoft JF (1997) Learning-induced alterations in hippocampal PKC-immunoreactivity: a review and hypothesis of its functional significance. Prog Neurorsychopharmacol Biol Psychiatry 21:531-572.
104. Villarreal RP, Steinmetz JE (2005) Neuroscience and learning: lessons from studying the involvement of a region of cerebellar cortex in eyeblink classical conditioning. J Exp Anal Behav 84:631-652.
105. Watanabe E (1984) Neuronal events correlated with long-term adaptation of the horizontal vestibulo-ocular reflex in the primate flocculus. Brain Res 297:169-174.