High-pass filtering and dynamic gain regulation enhance vertical bursts transmission along the mossy fiber pathway of cerebellum

Frontiers in Cellular Neuroscience

Volumn 4, Issue MAY, 2010, Pages

  Mapelli, Jonathan ^a,b   Gandolfi, Daniela ^a,b   D'Angelo, Egidio ^a,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b Consorzio Interuniversitario per le Scienze Fisiche della Materia ^*  (Italy)

^c C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

Author keywords

Cerebellum; GABA A receptors; Gain control; Imaging; NMDA receptors; Voltage sensitive dye

Indexed keywords

EID: 77957282024     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2010.00014     Document Type: Article

References (51)

1. Albus, J. S. (1971). A theory of cerebellar function. Math. Biosci. 10, 25-61.
2. Arenz, A., Silver, R. A., Schaefer, A. T., and Margrie, T. W. (2008). The contribution of single synapses to sensory representation in vivo. Science 321, 977-980.
3. Armano, S., Rossi, P., Taglietti, V., and 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.
4. Baginskas, A., Palani, D., Chiu, K., and Raastad, M. (2009). The H-current secures action potential transmission at high frequencies in rat cerebellar parallel fibers. Eur. J. Neurosci. 29, 87-96.
5. Bower, J. M., and Woolston, D. C. (1983). Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J. Neurophysiol. 49, 745-766.
6. Chadderton, P., Margrie, T. W., and Hausser, M. (2004). Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860.
7. Cohen, D., and Yarom, Y. (1998). Patches of synchronized activity in the cerebellar cortex evoked by mossy-fiber stimulation: questioning the role of parallel fibers. Proc. Natl. Acad. Sci. U.S.A. 95, 15032-15036.
8. Cull-Candy, S. G., Brickley, S. G., Misra, C., Feldmeyer, D., Momiyama, A., and Farrant, M. (1998). NMDA receptor diversity in the cerebellum: identification of subunits contributing to functional receptors. Neuropharmacology 37, 1369-1380.
9. D'Angelo, E. (2008). The critical role of Golgi cells in regulating spatio-temporal integration and plasticity at the cerebellum input stage. Front. Neurosci. 2, 35-46.
10. D'Angelo, E., De Filippi, G., Rossi, P., and Taglietti, V. (1995). Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J. Physiol. (Lond.) 484, 397-413.
11. D'Angelo, E., and De Zeeuw, C. I. (2009). Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci. 32, 30-40.
12. D'Angelo, E., Rossi, P., Armano, S., and Taglietti, V. (1999). Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fibre - granule cell transmission in rat cerebellum. J. Neurophysiol. 81, 277-287.
13. Dean, P., Porrill, J., Ekerot, C. F., and Jörntell, H. (2010). The cerebellar circuit as an adaptive filter: experimental and computational evidence. Nat. Rev. Neurosci. 11, 30-43.
14. + channels ensure fast spike activation and back-propagation in cerebellar granule cells. J. Neurophysiology 101, 519-532.
15. Dugué, G. P., Dumoulin, A., Triller, A., and Dieudonné, S. (2005). Target-dependent use of co-released inhibitory transmitters at central synapses. J. Neurosci. 23, 6490-6498.
16. Eccles, J. C., Ito, M., and Szentagothai, J. (1967). The Cerebellum as a Neuronal Machine. Berlin: Springer Verlag.
17. Fujita, M. (1982). Adaptive filter model of the cerebellum. Biol. Cybern. 45, 195-206.
18. Garthwaite, J., and Brodbelt, A. R. (1989). Synaptic activation of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptors in the mossy fibre pathway in adult and immature rat cerebellar slices. Neuroscience 29, 401-412.
19. Harvey, R. J., and Napper, R. M. (1991). Quantitative studies on mammalian cerebellum. Prog. Neurobiol. 36, 437-463.
20. Ito, M. (1984). The Cerebellum and Neural Control. New York: Raven publishing.
21. Jacobson, G. A., Rokni, D., and Yarom, Y. (2008). A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci. 31, 617-625.
22. Jörntell, H., and Ekerot, C. F. (2006). Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J. Neurosci. 26;11786-11797.
23. Kanichay, R. T., and Silver, R. A. (2008). Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex. J. Neurosci. 28, 8955-8967.
24. Kase, M., Miller, D. C., and Noda, H. (1980). Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation. J. Physiol. (Lond.) 300, 445-453.
25. Kinney, G. A., and Slater, N. T. (1993). Potentiation of NMDA receptor-mediated transmission in turtle cerebellar granule cells by activation of metabotropic glutamate receptors. J. Neurophysiol. 69, 585-594.
26. Llinas, R., and Sugimori, M. (1980a). Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. (Lond.) 305, 197-213.
27. Llinas, R., and Sugimori, M. (1980b). Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.) 305, 171-195.
28. Lu, H., Esquivel, A. V., and Bower, J. M. (2009). 3D electron microscopic reconstruction of segments of rat cerebellar Purkinje cell dendrites receiving ascending and parallel fiber granule cell synaptic inputs. J. Comp. Neurol. 514, 583-594.
29. Mapelli, J., and D'Angelo, E. (2007). The spatial organization of long-term synaptic plasticity at the input stage of the cerebellum. J. Neurosci. 27, 1285-1296.
30. Mapelli, J., Gandolfi, D., and D'Angelo, E. (2010). Combinatorial responses controlled by synaptic inhibition in the cerebellum granular layer. J. Neurophys. 103, 250-261.
31. Mapelli, L., Rossi, P., Nieus, T., and D'Angelo, E. (2009). Tonic activation of GABA-B receptors reduces release probability at inhibitory connections in the cerebellar glomerulus. J. Neurophysiol. 101, 3089-3099.
32. Marr, D. A. (1969). Theory of the cerebellar cortex. J. Physiol. (Lond.) 202, 437-470.
33. Mennerick, S., Chisari, M., Shu, H. J., Taylor, A., Vasek, M., Eisenman, L. N., and Zorumski, C. F. (2010). Diverse voltage-sensitive dyes modulate GABAA receptor function. J. Neurosci. 30, 2871-2879.
34. Mitchell, S. J., and Silver, R. A. (2000a). Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404, 498-502.
35. Mitchell, S. J., and Silver, R. A. (2000b). GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J. Neurosci. 20, 8651-8658.
36. Mitchell, S. J., and Silver, R. A. (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38; 433-445.
37. Palay, S. L., and Chan-Palay, V. (1974). Cerebellar Cortex. New York: Springer-Verlag.
38. Palkovits, M., Magyar, P., and Szentàgothai, J. (1971). Quantitative histological analysis of the cerebellar cortex in the cat. II. Cell numbers and densities in the granular layer. Brain Res. 32, 15-30.
39. Rancz, E. A., Ishikawa, T., Duguid, I., Chadderton, P., Mahon, S., and Hausser, M. (2007). High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450, 1245-1249.
40. Rokni, D., Llinas, R., and Yarom, Y. (2008). The morpho/functional discrepancy in the cerebellar cortex: looks alone are deceptive. Front Neurosci. 2, 192-198.
41. Rokni, D., Tal, Z., Byk, H., and Yarom, Y. (2009). Regularity, variability and bi-stability in the activity of cerebellar purkinje cells. Front. Cell. Neurosci. 3:12. doi:10.3389/neuro.03.012.2009.
42. Sacconi, L., Mapelli, J., Gandolfi, D., Lotti, J., O'Connor, R. P., D'Angelo, E., and Pavone, F. S. (2008). Optical recording of electrical activity in intact neuronal networks with random access second-harmonic generation microscopy. Opt. Express 16, 14910-14921.
43. Santamaria, F., Tripp, P. G., and Bower, J. M. (2007). Feedforward inhibition controls the spread of granule cell-induced Purkinje cell activity in the cerebellar cortex. J. Neurophysiol. 97, 248-263.
44. Sims, R. E., and Hartell, N. A. (2005). Differences in transmission properties and susceptibility to long-term depression reveal functional specialization of ascending axon and parallel fiber synapses to Purkinje cells. J. Neurosci. 23, 3246-3257.
45. Sims, R. E., and Hartell, N. A. (2006). Differential susceptibility to synaptic plasticity reveals a functional specialization of ascending axon and parallel fiber synapses to cerebellar Purkinje cells. J. Neurosci. 26, 5153-5159.
46. Solinas, S., Nieus, T., and D'Angelo, E. (2010). A realistic large-scale model of the cerebellum granular layer predicts circuit spatio-temporal filtering properties. Front. cell. Neurosci. 4:12. doi: 10.3389/fncel.2010.00012.
47. Sultan, F. (2001). Distribution of mossy fiber rosettes in the cerebellum of cat and mice: evidence for a parasagittal organization at the single fiber level. Eur. J. Neurosci. 13, 2123-2130.
48. Tominaga, T., Tominaga, Y., Yamada, H., Matsumoto, G., and Ichikawa, M. (2000). Quantification of optical signals with electrophysiological signals in neural activities of Di-4-Anepps stained rat hippocampal slices. J. Neurosci. Methods 102, 11-23.
49. Vranesic, I., Iijima, T., Ichikawa, M., Matsumoto, G., and Knöpfel, T. (1994). Signal transmission in the parallel fiber-Purkinje cell system visualized by high-resolution imaging. Proc. Natl. Acad. Sci. U.S.A. 20, 13014-13017.
50. Walter, J. T., Dizon, M. J., and Khodakhah, K. (2009). The functional equivalence of ascending and parallel fiber inputs in cerebellar computation. J. Neurosci. 29, 8462-8473.
51. Yae, H., Elias, S. A., and Ebner, T. J. (1992). Deblurring of 3-dimensional patterns of evoked rat cerebellar cortical activity: a study using voltage-sensitive dyes and optical sectioning. J. Neurosci. Methods 42, 195-209.