A biophysical model of synaptic delay learning and temporal pattern recognition in a cerebellar purkinje cell

Journal of Computational Neuroscience

Volumn 17, Issue 2, 2004, Pages 149-164

  Steuber, Volker ^a,b   Willshaw, David ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Calcium; Cerebellum; mGluR; Temporal coding

Indexed keywords

BRAIN; CALCIUM; CHEMICAL ACTIVATION; DIFFERENTIAL EQUATIONS; NEURONS; PATTERN RECOGNITION;

BIOPHYSICAL MODEL; CEREBELLUM; DELAY LEARNING; LEARNING PATTERNS; METABOTROPIC GLUTAMATE RECEPTORS; MGLUR; PURKINJE CELLS; SYNAPTIC DELAYS; TEMPORAL CODING; TIME-DELAYS;

TIME DELAY;

CALCIUM; GLUTAMATE RECEPTOR;

ARTICLE; BIOCHEMISTRY; BIOPHYSICS; CELL ACTIVITY; CONCEPT FORMATION; ELECTRIC POTENTIAL; EYELID REFLEX; GENE ACTIVATION; LEARNING; MATHEMATICAL MODEL; PATTERN RECOGNITION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; SIGNAL TRANSDUCTION; SPIKE WAVE; SYNAPSE;

EID: 4344610272     PISSN: 09295313     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:JCNS.0000037678.26155.b5     Document Type: Article

References (89)

1. Armstrong DM, Rawson JA (1979) Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J. Physiol 289: 425-448.
2. Batchelor AM, Garthwaite J (1993) Novel synaptic potentials in cerebellar Purkinje cells: Probable mediation by metabotropic glutamate receptors. Neuropharmacology 32: 11-20.
3. Batchelor AM, Garthwaite J (1997) Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385: 74-77.
4. Batchelor AM, Madge DJ, Garthwaite J (1994) Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63: 911-915.
5. Berridge MJ, Cobbold PH, Cuthbertson KSR (1988) Spatial and temporal aspects of cell signalling. Phil. Trans. R. Soc. Lond. B 320: 325-343.
6. Bezprozvanny I, Watras J, Ehrlich BE (1991) Bell-shaped calcium-dependent curves of Ins(1,4,5)-P3 gated and calcium gated channels from endoplasmic reticulum of cerebellum. Nature 351: 751-754.
7. Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381-387.
8. Bialek W, Rieke F, de Ruyter van Steveninck R, Warland D (1991) Reading a neural code. Science 252: 1854-1857.
9. Blackwell KT, Vogl TP, Alkon DL (1998) Pattern matching in a model of dendritic spines. Network 9: 107-121.
10. Bloedel JR, Roberts WJ (1971) Action of climbing fibres in cerebellar cortex of the cat. J. Neurophysiol. 34: 17-31.
11. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL, Worely FP (1997) Horner: A protein that selectively binds metabotropic glutamate receptors. Nature 386: 284-288.
12. Bray D (1995) Protein molecules as computational elements in living cells. Nature 376: 307-312.
13. Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347:768-770.
14. Carafoli E (1987) Intracellular calcium homeostasis. Ann. Rev. Biochem. 56: 395-433.
15. Clark RE, Manns JR, Squire LR (2001) Trace and delay eyeblink conditioning: Contrasting phenomena of declarative and nondeclarative memory. Psychol. Sci. 12: 304-308.
16. Daniel H, Levenes C, Crépel F (1998) Cellular mechanisms of cerebellar LTD. Trends Neurosci. 21: 401-407.
17. De Schutter E (1995) Cerebellar long-term depression might normalize excitation of Purkinje cells: A hypothesis. Trends Neurosci. 18: 291-295.
18. De Schunter E (1997) A new functional role for cerebellar long term depression. Prog. Brain Res. 114: 531-544.
19. De Schutter E, Bower JM (1994) An active membrane model of the cerebellar Purkinje cell. II. Simulation of synaptic responses. J. Neurophysiol 71: 401-419.
20. Eccles JC, Sabah NH, Schmidt RF, Taborikova H (1972a) Cutaneous mechanoreceptors influencing impulse discharges in cerebellar cortex. 2. In Purkyne cells by mossy fiber input. Exp. Brain Res. 15: 261-277.
21. Eccles JC, Sabah NH, Schmidt RF, Taborikova H (1972b) Cutaneous mechanoreceptors influencing impulse discharges in cerebellar cortex. 3. In Purkyne cells by climbing fiber input. Exp. Brain Res. 15: 484-497.
22. Eurich CW, Cowan JD, Milton JG (1997) Hebbian delay adaptation in a network of integrate-and-fire neurons. In: W Gerstner, A Germond, M Hasler, JD Nicoud, eds. Proceedings of the 7th International Conference on Artifical Neural Networks ICANN 97, Springer Verlag, Berlin, pp. 157-162.
23. Eurich CW, Ernst U, Pawelzik K (1998) Continous dynamics of neuronal delay adaptation. In: L Niklasson, M Bodén, T Ziemke, eds. Proceedings of the 8th International Conference on Artifical Neural Networks ICANN 98, Springer Verlag, Berlin, pp. 355-360.
24. + Channel by Stimulation of Glutamate Phosphoinositide-coupled Receptors in Cultured Cerebellar Granule Cells. Eur. J. Neurosci. 3: 778-789.
25. 2+ stores and ion channels in neurons. Trends Neurosci. 23: 80-88.
26. Fiala JC, Grossberg S, Bullock D (1996) Metabotropic glutamate receptor activation in cerebellar Purkinje cells as substrate for adaptive timing of the classically conditioned eye-blink response. J. Neurosci. 16: 3760-3774.
27. Finch EA, Augustine GJ (1998) Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396: 753-756.
28. Fiorillo CD, Williams JT (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394: 19-21.
29. Gerstner W, Kempter R, van Hemmen J, Wagner H (1996) A neuronal learning rule for sub-millisecond temporal coding. Nature 383: 76-48.
30. Hamori J, Szentagothai J (1966) Identification under the electron microscope of climbing fibers and their synaptic contacts. Exp. Brain Res. 1: 65-81.
31. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: The diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat. Neurosci. 4: 467-475.
32. Harata N, Katayama J, Takeshita Y, Murai Y, Akaike N (1996) Two components of metabotropic glutamate responses in acutely dissociated CA3 pyramidal neurons of the rat. Brain Res. 711:223-233.
33. Hartell NA (1994) cGMP acts within cerebellar Purkinje cells to produce long term depression via mechanisms involving PKC and PKG. Neuroreport 5: 833-836.
34. Hodgkin AL, Nunn BJ (1987) The effect of ions on sodium-calcium exchange in salamander rods. J. Physiol. 391: 371-398.
35. 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.
36. Hopfield JJ (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376: 33-36.
37. Huang K-P, Huang FL, Mahoney CW, Chen K-H (1991) Protein kinase C subtypes and their respective roles. Prog. Brain Res. 89: 143-155.
38. Hüning H, Glünder H, Palm G (1998) Synaptic delay learning in pulse-coupled neurons. Neural Comp. 10: 555-565.
39. Ito M (1996) The new hypothesis does not detract from the MAIT theory. Trends Neurosci. 19: 11.
40. Ito M, Karachot L (1992) Protein kinases and phosphatase inhibitors mediating long-term desensitization of glutamate receptors in cerebellar Purkinje cells. Neuroscience Res. 14: 27-38.
41. Ito M, Sakurai M, Tongroach P (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. 324: 133-134.
42. James GO, Hardiman MJ, Yeo CH (1987) Hippocampal lesions and trace conditioning in the rabbit. Behav. Brain Res. 23: 109-116.
43. Karachot L, Kado RT, Ito M (1994) Stimulus parameters for induction of long-term depression in in vitro rat Purkinje cells. Neurosci. Res. 21: 161-168.
44. Kehoe EJ, Graham-Clarke P, Schreurs BG (1989) Temporal patterns of the rabbit's nictitating membrane response to compound and component stimuli under mixed CS-US intervals. Behav. Neurosci. 103: 283-295.
45. 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.
46. 2+ release in rat cerebellar Purkinje neurones. J. Physiol. 487: 343-358.
47. Kishimoto Y, Kawahara S, Mori H, Mishina M, Kirino Y (2001) Long-trace interval eyeblink conditioning is impaired in mutant mice lacking the NMDA receptor subunit epsilon 1. Eur. J. Neurosci. 13: 1221-1227.
48. Laurent G (1996) Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci. 19: 489-496.
49. 2+ in the induction of cerebellar long-term depression. Neuron 18: 1025-1038.
50. Linden DJ, Connor JA (1993) Cellular mechanisms of long-term depression in the cerebellum. Curr. Opin. Neurobiol. 3: 401-406.
51. Lytton J, Westlin M, Burk SE, Shull GE, MacLennan DH (1992) Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J. Biol. Chem. 267: 14483-14489.
52. 1 and -γ peptide substrates. FEBS letters 277: 151-155.
53. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349: 760-765.
54. McCormick DA, Thompson RF (1984) Cerebellum: Essential involvement in the classically conditioned eyelid response. Science 223: 296-299.
55. McEchron MD, Weible AP, Disterhoft JF (2001) Aging and learning-specific changes in single-neuron activity in CA1 hippocampus during rabbit trace eyeblink conditioning. J. Neurophysiol. 86: 1839-1857.
56. Medina JF, Garcia KS, Notes WL, Taylor NM, Mauk MD (2000) Timing mechanisms in the cerebellum: Testing predictions of a large-scale computer simulation. J. Neurosci. 20: 5516-5525.
57. 2+ and adenine nucleotides. Biochemistry 25: 236-244.
58. 3 receptor. J. Biol. Chem. 267: 7450-7455.
59. Moyer JRJ, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosc. 104: 243-252.
60. Murphy JT, Sabah NH (1970) Spontaneous firing of cerebellar Purkinje cells in decerebrate and barbiturate anesthesized cats. Brain Res. 17: 515-519.
61. Napp-Zinn H, Jansen M, Eckmiller R (1996) Recognition and tracking of impulse patterns with delay adaptation in biology-inspired pulse processing neural net (BPN) hardware. Biol. Cybernetics 74: 449-453.
62. Natschlager T, Ruf B (1998) Spatial and temporal pattern analysis via spiking neurons. Network 9: 319-332.
63. 2+ levels via the phospholipase C transduction pathway in cultured Purkinje neurons. J. Neurophysiol. 78: 63-75.
64. Nishizuka Y, Shearman MS, Oda T, Berry N, Tanaka C (1991) Protein kinase C family and nervous function. Prog. Brain Res. 89: 125-141.
65. Ohyama T, Mauk MD (2001) Latent acquisition of timed responses in cerebellar cortex. J. Neurosci. 21: 682-690.
66. Rainnie DG, Holmes KH, Shinnick-Gallagher P (1994) Activation of postsynaptic metabotropic glutamate receptors by trans-ACPD hyperpolarizes neurons of the basolateral amygdala. J. Neurosci. 14: 7208-7220.
67. Rieke F, Warland D, de Ruyter van Steveninck R, Bialek W (1997) Spikes: Exploring the Neural Code. MIT Press, Cambridge, MA.
68. Ross RT, Scavio MJJ (1983) Perseveration of associative strength in rabbit nictitating membrane conditioning following ISI shifts. Anim. Learn. Behav. 11: 435-438.
69. Schreurs BG, Alkon DL (1993) Rabbit cerebellar slice analysis of long-term depression and its role in classical conditioning. Brain Res. 631: 235-240.
70. Schweighofer N, Ferriol G (2000) Diffusion of nitric oxide can facilitate cerebellar learning: A simulation study. Proc. Natl. Acad. Sci. USA 97: 10661-10665.
71. Sejnowski TJ (1995) Time for a new neural code? Nature 376: 21-22.
72. Shibuki K, Okada D (1991) Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349: 326-328.
73. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned eye-blink response. Behav. Neurosci. 100: 729-744.
74. Steinmetz JE (1990) Classical nictitating membrane conditioning in rabbits with varying interstimulus intervals and direct activation of cerebellar mossy fibres as the CS. Behav. Brain Res. 38: 97-108.
75. Stemmer PM, Klee CB (1994) Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 33: 6859-6866.
76. Steuber V, Willshaw DJ (1997) How a single Purkinje cell could learn the adaptive timing of the classically conditioned eye-blink response. In: W Gerstner, A Germond, M Hasler, JD Nicoud, eds. Proceedings of the 7th International Conference on Artifical Neural Networks ICANN 97, Springer Verlag, Berlin, pp. 115-120.
77. Steuber V, Willshaw DJ (1999) Adaptive leaky integrator models of cerebellar Purkinje cells can learn the clustering of temporal patterns. Neurocomputing 26: 271-276.
78. Takatsuki K, Kawahara S, Takehara K, Kishimoto Y, Kirino Y (2001) Effects of the noncompetitive NMDA receptor antagonist MK-801 on classical eyeblink conditioning in mice. Neuropharmacology 41: 618-628.
79. Tempia F, Miniaci MC, Anchisi D, Strata P (1998) Postsynaptic currents mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J. Neurophysiol. 80: 520-528.
80. Thompson RF, Kim JJ (1996) Memory systems in the brain and localization of a memory. Proc. Natl. Acad. Sci. USA 93: 13438-13444.
81. Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Ann. Rev. Neurosci. 17: 519-549.
82. Thorpe S, Fize F, Marlot C (1996) Speed of processing in the human visual system. Nature 381: 520-522.
83. Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K, Li M, Linden DJ, Worley PF (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21: 717-726.
84. Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46: 755-784.
85. Wang SS, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3: 1266-1273.
86. Wehr M, Laurent G (1996) Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384: 162-166.
87. Woodruff-Pak DS, Lavond DG, Thompson RF (1985) Trace conditioning: Abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations. Brain Res. 348: 249-260.
88. Yeo CH, Hesslow G (1998) Cerebellum and conditioned reflexes. Trends Cognitive Sci. 2: 322-330.
89. Yeo CH, Lobo DH, Baum A. (1997) Acquisition of a new-latency conditioned nictitating membrane response - Major, but not complete, dependence on the ipsilateral cerebellum. Learn. Mem. 3: 557-577.