Metabotropic glutamate receptor activation in cerebellar purkinje cells as substrate for adaptive timing of the classically conditioned eye-blink response

Journal of Neuroscience

Volumn 16, Issue 11, 1996, Pages 3760-3774

  Fiala, John C ^a   Grossberg, Stephen ^a   Bullock, Daniel ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

AMPA receptors; cerebellum; classical conditioning; long term depression; metabotropic glutamate receptors; neural network; nictitating membrane response

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR;

ADAPTATION; ANIMAL CELL; ARTICLE; CONDITIONING; EYELID REFLEX; LEARNING; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; NICTITATING MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PURKINJE CELL; SECOND MESSENGER;

EID: 0029876036     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-11-03760.1996     Document Type: Article

References (132)

1. 2+ signal transduction. J Biol Chem 267:13361-13368.
2. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
3. Ajima A, Ito M (1995) A unique role of protein phosphatases in cerebellar long-term depression. NeuroReport 6:297-300.
4. Alkon DL (1984) Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226:1037-1045.
5. Alkon DL (1986) Changes of membrane currents and calciumdependent phosphorylation during associative conditioning. In: Neural mechanisms of conditioning (Alkon DL, Woody CD, eds), pp. 3-18. New York: Plenum.
6. Bacigalupo J, Johnson EC, Vergara C, Lisman JE (1991) Cyclic GMP opens light-dependent channels in excised patches of Limulus ventral photoreceptors (Abstr). Biophys J 59:530A.
7. Baraban JM, Snyder SH, Alger BE (1985) Protein kinase C regulates ionic conductance in hippocampal pyramidal neurons: electrophysiological effects of phorbol esters. Proc Natl Acad Sci USA 82:2538-2542.
8. Bartha GT, Thompson RF (1992a) Control of rabbit nictitating membrane movements. I. A computer model of the retractor bulbi muscle and the associated orbital mechanics. Biol Cybern 68:135-143.
9. Bartha GT, Thompson RF (1992b) Control of rabbit nictitating membrane movements. II. Analysis of the relation of motoneuron activity to behavior. Biol Cybern 68:145-154.
10. Bartha GT, Thompson RF, Gluck MA (1991) Sensorimotor learning and the cerebellum. In: Visual structures and integrated functions (Arbib M, Ewert J, eds), pp 381-396. Berlin: Springer.
11. Batchelor AM, Garthwaite J (1993) Novel synaptic potentials in cerebellar Purkinje cells: probable mediation by metabotropic glutamate receptors. Neuropharmacology 32:11-20.
12. Batchelor AM, Madge DJ, Garthwaite J (1994) Synaptic activation of metabotropic glutamate receptors in the parallel fiber-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63:911-915.
13. Baumann O, Walz B, Somtyo AV, Somlyo AP (1991) Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors. Proc Natl Acad Sci USA 88:741-744.
14. Baylor DA, Hodgkin AL (1974) Changes in time scale and sensitivity in turtle photoreceptors. J Physiol (Lord) 242:729-758.
15. Berger TW, Berry SD, Thompson RF (1986) Role of the hippocampus in classical conditioning of aversive and appetitive behaviors. In: The hippocampus, Vol 4 (Isaacson RL, Pribram KH, eds), pp 203-239. New York: Plenum.
16. q/11 and phospholipase C-β1. J Biol Chem 267:8081-8088.
17. Berridge MJ, Cobbold PH, Cuthbertson KSR (1988) Spatial and temporal aspects of cell signalling. Philos Trans R Soc Lond [Biol] 320:325-343.
18. Berthier NE, Moore JW (1986) Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Brain Res 63:341-350.
19. Bezprozvanny I, Watras J, Ehrlich BE (1991) Bell-shaped calciumresponse curves of Ins(l,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351:751-754.
20. + channel in rat peptidergic nerve terminals. J Physiol (Lond) 475.2:241-254.
21. Blackstone CD, Supattapone S, Snyder SH (1989) Inositolphospholipid-linked glutamate receptors mediate cerebellar parallel fiber-Purkinje cell synaptic transmission. Proc Natl Acad Sci USA 86:4316-4320.
22. 2+ stores. Mol Cell Endocrinol 98:157-166.
23. Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770.
24. Bullock D, Fiala JC, Grossberg S (1994) A neural model of timed response learning in the cerebellum. Neural Networks 7:1101-1114.
25. Buonomano DV, Mauk MD (1994) Neural network model of the cerebellum: temporal discrimination and the timing of motor responses. Neural Comput 6:38-55.
26. Burroughs SE, Horrocks WD, Ren H, Klee CB (1994) Characterization of the lanthanide ion-binding properties of calcineurin-B using laserinduced luminescence spectroscopy. Biochemistry 33:10428-10436.
27. i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777-2787.
28. Carafoli E (1987) Intracellular calcium homeostasis. Annu Rev Biochem 56:395-433.
29. Carpenter GA, Grossberg S (1981) Adaptation and transmitter gating in vertebrate photoreceptors. J Theor Neurobiol 1:1-42.
30. 2′, a guanine nucleotide-binding protein with unique biochemical properties. J Biol Chem 265:2383-2390.
31. Catania MV, Aronica E, Sortino MA, Canonico PL, Nicoletti F (1991) Desensitization of metabotropic glutamate receptors in neuronal cultures. J Neurochem 56:1329-1335.
32. Chapeau-Blondeau F, Chauvet G (1991) A neural network model of the cerebellar cortex performing dynamic associations. Biol Cybern 65:267-279.
33. 2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J Biol Chem 269:22698-22704.
34. 2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J Biol Chem 267:23318-23326.
35. Clements JD, Lester RAJ, Tong G, Jahr CE, Westbrook GL (1992) The time course of glutamate in the synaptic cleft. Science 258:1496-1501.
36. Coleman SR, Gormezano I (1971) Classical conditioning of the rabbit's (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts. J Comp Physiol Psychol 77:447-455.
37. Crepel F, Jaillard D (1990) Protein kinases, nitric oxide and long-term depression of synapses in the cerebellum. NeuroReport 1:133-136.
38. Crow T (1988) Cellular and molecular analysis of associative learning and memory in Hermissenda. Trends Neurosci 11:136-142.
39. Daniel H, Hemart N, Jaillard D, Crepel F (1992) Coactivation of metabotropic glutamate receptors and of voltage-gated calcium channels induces long-term depression in cerebellar Purkinje cells in vitro. Exp Brain Res 90:327-331.
40. De Meis L, Inesi G (1982) The transport of calcium by sacroplasmic reticulum and various microsomal preparations. In: Membrane transport of calcium (Carafoli E, ed), pp 141-186. London: Academic.
41. De Schutter E, Bower JM (1994a) An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. J Neurophysiol 71:375-400.
42. De Schutter E, Bower JM (1994b) An active membrane model of the cerebellar Purkinje cell. II. Simulation of synaptic responses. J Neurophysiol 71:401-419.
43. 2+ in a secretory epithelial cell line, T84. Am J Physiol 260:C598-608.
44. 2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature 373:155-158.
45. + channel by stimulation of glutamate phosphoinositide-coupled receptors in cultured cerebellar granule cells. Eur J Neurosci 3:778-789.
46. Freeman JA (1969) The cerebellum as a timing device: an experimental study in the frog. In: Neurobiology of cerebellar evolution and development (Llinás R, ed), pp 397-420. Chicago: American Medical Association.
47. Fuortes MGF, Hodgkin AL (1964) Changes in time scale and sensitivity in the ommatidia of Limulus. J Physiol (Lond) 172:239-263.
48. 2+ signaling in the brain. J Neurochem 64:953-960.
49. Glaum SR, Slater NT, Rossi DJ, Miller RJ (1992) Role of metabotropic glutamate (ACPD) receptors at the parallel fiber-Purkinje cell synapse. J Neurophysiol 68:1453-1462.
50. Gormezano I (1966) Classical conditioning. In: Experimental methods and instrumentation in psychology (Sidowski JB, ed), pp 385-420. New York: McGraw-Hill.
51. Griffith LC, Wang J, Zhong Y, Wu C-F, Greenspan RJ (1994) Calcium/ calmodulin-dependent protein kinase II and potassium channel subunit Eag similarly aifect plasticity in Drosophila. Proc Natl Acad Sci USA 91:10044-10048.
52. Grossberg S, Merrill JWL (1992) A neural network model of adaptively timed reinforcement learning and hippocampal dynamics. Cognit Brain Res 1:3-38.
53. Grossberg S, Merrill JWL (1996) The hippocampus and cerebellum in adaptively timed learning, recognition, and movement. J Cognit Neurosci, in press.
54. Grossberg S, Schmajuk NA (1989) Neural dynamics of adaptive timing and temporal discrimination during associative learning. Neural Networks 2:79-102.
55. Hartell NA (1994) Induction of cerebellar long-term depression requires activation of glutamate metabotropic receptors. NeuroReport 5:913-916.
56. Herrero I, Miras-Portugal MT, Sanchez-Prieto J (1994) Rapid desensitization of the metabotropic glutamate receptor that facilitate glutamate release in rat cerebrocortical nerve terminals. Eur J Neurosci 6:115-120.
57. Hirano T (1990) Depression and potentiation of the synaptic transmission between a granule cell and a Purkinje cell in rat cerebellar culture. Neurosci Lett 119:141-144.
58. Hodgkin AL, Nunn BJ (1987) The effect of ions on sodium-calcium exchange in salamander rods. J Physiol (Lond) 391:371-398.
59. Hoehler FK, Leonard DW (1976) Double responding in classical nictitating membrane conditioning with single-CS dual-ISI training. Pavlov J Biol Sci 11:180-190.
60. Hoehler FK, Thompson RF (1980) Effects of the interstimulus (CSUCS) 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.
61. Homma Y, Imaki J, Nakanishi O, Takenawa T (1988) Isolation of characterization of two different forms of inositol phospholipid-specific phospholipase C from rat brain. J Biol Chem 263:6592-6598.
62. 2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinca pig Taenia caeci. J Gen Physiol 95:1103-1122.
63. Ito M (1984) The cerebellum and neural control. New York: Raven.
64. Ito M (1991) The cellular basis of cerebellar plasticity. Curr Opin Neurobiol 1:616-620.
65. Ito M, Karachot L (1992) Protein kinases and phosphatase inhibitors mediating long-term desensitization of glutamate receptors in cerebellar Purkinje cells. Neurosci Res 14:27-38.
66. Jaffe S (1992) A neuronal model for variable latency response. In: Analysis and modeling of neural systems (Eeckman FH, ed), pp 405-410. Boston: Kluwer Academic Publishers.
67. Joseph SK, Rice HL, Williamson JR (1989) The effect of external calcium and pH on inositol trisphosphate-mediated calcium release from cerebellum microsomal fractions. Biochem J 258:261-265.
68. Kasono K, Hirano T (1994) Critical role of postsynaptic calcium in cerebellar long-term depression. NeuroReport 6:17-20.
69. Kasono K, Hirano T (1995) Involvement of inositol trisphosphate in cerebellar long-term depression. NeuroReport 6:569-572.
70. Khodakhah K, Ogden D (1993) Functional heterogeneity of calcium release by inositol trisphosphate in single Purkinje neurones, cultured cerebellar astrocytes, and peripheral tissues. Proc Natl Acad Sci USA 90:4976-4980.
71. King MM, Huang CY, Chock PB, Nairn AC, Hemmings Jr HC, Chan K-FJ, Greengard P (1984) Mammalian brain phosphoproteins as substrates for calcineurin. J Biol Chem 259:8080-8083.
72. Konnerth A, Dreessen J, Augustine GJ (1992) Brief dendritic calcium signals initiate long-lasting synaptic depression in cerebellar Purkinje cells. Proc Natl Acad Sci USA 89:7051-7055.
73. Lamb TD, Pugh Jr EN (1992) A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol (Lond) 449:719-758.
74. Levitan I, Hillman P, Payne R (1993) Fast desensitization of the response to InsP3 in Limulus ventral photoreceptors. Biophys J 64:1354-1360.
75. Linden DJ, Connor JA (1991) Participation of postsynaptic PKC in cerebellar long-term depression in culture. Science 254:1656-1659.
76. Linden DJ, Connor JA (1993) Cellular mechanisms of long-term depression in the cerebellum. Curr Opin Neurobiol 3:401-406.
77. Linden DJ, Dawson TM, Dawson VL (1995) An evaluation of the nitric oxide/cGMP/cGMP-dependent protein kinase cascade in the induction of cerebellar long-term depression in culture. J Neurosci 15:5098-5105.
78. Linden DJ, Dickinson MH, Smeyne M, Conner JA (1991) A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons. Neuron 7:81-89.
79. Linden DJ, Smeyne M, Connor JA (1993) Induction of cerebellar longterm depression in culture requires postsynaptic action of sodium ions. Neuron 11:1093-1100.
80. Llinás R, Sugimori M (1992) The electrophysiology of the cerebellar Purkinje cell revisited. In: The cerebellum revisited (Llinás R, Sotelo C, eds), pp 167-181. New York: Springer.
81. Lonart G, Alagarsamy S, Johnson KM (1993) (R,S)-α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) receptors mediate a calcium-dependent inhibition of the metabotropic glutamate receptor-stimulated formation of inositol 1,4,5-trisphosphate. J Neurochem 60:1739-1745.
82. Matzel LD, Schreurs BG, Lederhendler I, Alkon DL (1990) Acquisition of conditioned associations in Hermissenda: additive effects of contiguity and the forward interstimulus interval. Behav Neurosci 104:597-606.
83. McCormick DA, Thompson RF (1984) Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J Neurosci 4:2811-2822.
84. McCormick DA, Clark GA, Lavond DG, Thompson RF (1982) Initial localization of the memory trace for a basic form of learning. Proc Natl Acad Sci USA 79:2731-2735.
85. McGonigle P, Molinoff PB (1994) Receptors and signal transduction: classification and quantitation. In: Basic neurochemistry: molecular, cellular, and medical aspects, 5th ed (Siegel GJ, Agranoff BW, Albers RW, Molinoff PB, eds), pp 417-428. New York: Raven.
86. 2+, and adenine nucleotides. Biochemistry 25:236-244.
87. 2+ influx in turtle Purkinje cell dendrites in vitro: Role of a transient outward current. J Neurophysiol 70:2455-2469.
88. 3, receptor. J Biol Chem 267:7450-7455.
89. Millenson JR, Kehoe EJ, Gormenzano I (1977) Classical conditioning of the rabbit's nictitating membrane response under fixed and mixed CS-US intervals. Learn Motiv 8:351-366.
90. Missiaen L, Parys JB, De Smedt H, Dike M, Casteels R (1994) Partial calcium release in response to submaximal inositol 1,4,5-trisphosphate receptor activation. Mol Cell Endocrinol 98:147-156.
91. Miyakawa H, Lev-Ram V, Lasser-Ross N, Ross WN (1992) Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J Neurophysiol 68:1178-1189.
92. Moore JW, Desmond JE, Berthier NE (1989) Adaptively timed conditioned responses and the cerebellum: a neural network approach. Biol Cybern 62:17-28.
93. Nagy K (1991) Biophysical processes in invertebrate photoreceptors: recent progress and a critical overview based on Limulus photoreceptors, Q Rev Biophys 24:165-226.
94. Nakanishi Y (1988) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661-665.
95. Nestler EJ, Duman RS (1994) G proteins and cyclic nucleotides in the nervous system. In: Basic neurochemistry: molecular, cellular, and medical aspects, 5th ed (Siegel GJ, Agranoff BW, Albers RW, Molinoff PB, eds), pp 429-448. New York: Raven.
96. Nestler EJ, Greengard P (1984) Protein phosphorylation in the nervous system. New York: Wiley.
97. Nishizuka Y (1986) Studies and perspectives of protein kinase C. Science 233:305-310.
98. Nishizuka Y (1988) The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661-665.
99. Nusser Z, Mulvihill E, Streit P, Somogyi P (1994) Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61:421-427.
100. Palay SL, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. New York: Springer.
101. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13:1708-1718.
102. Reinhart PH, Levitan IB (1995) Kinase and phosphatase activities intimately associated with a reconstituted calcium-dependent potassium channel. J Neurosci 15:4572-4579.
103. Richard EA, Sampat P, Lisman JE (1995) Distinguishing between roles for calcium in Limulus photoreceptor excitation. Cell Calcium 18:330-340.
104. Sakurai M (1989) Depression and potentiation of parallel fiber-Purkinje cell transmission in in vitro cerebellar slices. In: Olivo-cercbellar system in motor control (Strata P, ed), pp 221-230. Berlin: Springer.
105. Sakurai M (1990) Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc Natl Acad Sci USA 87:3383-3385.
106. Schwartz JH, Kandel ER (1991) Synaptic transmission mediated by second messengers. In: Principles of neural science. 3rd ed (Kandel ER, Schwartz JH, Jessell TM, eds), pp 173-193. New York: Elsevier.
107. Shibuki K, Okada D (1991) Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349:326-328.
108. 2+ activity. NeuroReport 3:231-234.
109. Shigemoto R, Abe T, Nomura S, Nakanishi S, Hirano T (1994) Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12:1245-1255.
110. Shigemoto R, Nakanishi S, Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121-135.
111. 2+ is an obligatory intermediate in the excitation cascade of Limulus photoreceptors. Neuron 11:845-855.
112. 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.
113. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100:729-744.
114. Staub C, Vranesic I, Knopfel T (1992) Responses to metabotropic glutamate receptor activation in cerebellar Purkinje cells: induction of an inward current. Eur J Neurosci 4:832-839.
115. Steinmetz JE (1990a) Classical nictitating membrane conditioning in rabbits with varying interstimulus intervals and direct activation of cerebellar mossy fibers as the CS. Behav Brain Res 38:97-108.
116. Steinmetz JE (1990b) Neuronal activity in the rabbit interpositus nucleus during classical NM-conditioning with a pontine-nucleus-stimulation CS. Psychol Sci 1:378-382.
117. Steinmetz JE, Lavond DG, Thompson RF (1989) Classical conditioning in rabbits using online nucleus stimulation as a conditioned stimulus and inferior olive stimulation as an unconditioned stimulus. Synapse 3:225-233.
118. Steinmetz JE, Logan CG, Rosen DJ, Thompson JK, Lavond DO, Thompson RF (1987) Initial localization of the acoustic conditioned stimulus projection to the cerebellum essential for classical eyelid conditioning. Proc Natl Acad Sci USA 84:3531-3535.
119. Steinmetz JE, Rosen DJ, Chapman PF, Lavond DG, Thompson RF (1986) Classical conditioning of the rabbit eyelid response with a mossy fiber stimulation CS: I. Pontine nuclei and middle cerebellar peduncle stimulation. Behav Neurosci 100:878-887.
120. Stemmer PM, Klee CB (1994) Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 33:6859-6866.
121. Takei K, Mignery GA, Mugnaini E, Südhof TC, De Camilli P (1994) Inositol 1,4,5-trisphosphate receptor causes formation of ER cisternal stacks in transfected fibroblasts and in cerebellar Purkinje cells. Neuron 12:327-342.
122. 2+ -ATPase, and calsequestrin. J Neurosci 12:489-505.
123. Thompson JH, Bower JM (1993) Electrophysiological dissection of the excitatory inputs to Purkinje cells. In: Computation and neural systems (Eeckman FH, Bower JM, eds), pp 349-353. Norwell, MA: Kluwer Academic Publishers.
124. Thompson RF (1990) Neural mechanisms of classical conditioning in mammals. Philos Trans R Soc Lond [Biol] 329:161-170.
125. Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Annu Rev Neurosci 17:519-549.
126. Thomsen C, Mulvihill ER, Haldeman B, Pickering DS, Hampson DR. Suzdak PD (1993) A pharmacological characterization of the mGluR1α subtype of the metabotropic glutamate receptor expressed in a cloned baby hamster kidney cell line. Brain Res 619:22-28.
127. 2+ ATPase and of the ER lumenal protein, Bip. J Cell Biol 113:779-791.
128. Wang SS-H, Alousi AA, Thompson SH (1995) The lifetime of inositol 1,4,5-trisphosphate in single cells. J Gen Physiol 105:149-171.
129. Watras J, Bezprozvanny I, Ehrlich BE (1991) Inositol 1,4,5-trisphosphategated channels in cerebellum: presence of multiple conductance states. J Neurosci 11:3239-3245.
130. Yamada WM, Koch C, Adams PR (1989) Multiple channels and calcium dynamics. In: Methods in neuronal modeling: from synapse to networks (Koch C, Segev I, eds), pp 97-133. Boston: MIT.
131. Yarfitz S, Hurley JB (1994) Transduction mechanisms of vertebrate and invertebrate photoreceptors. J Biol Chcm 269:14329-14332.
132. Zipser D (1986) A model of hippocampal learning during classical conditioning. Behav Neurosci 100:764-776.