Frequency-tuned cerebellar channels and burst-induced LTD lead to the cancellation of redundant sensory inputs

Journal of Neuroscience

Volumn 31, Issue 30, 2011, Pages 11028-11038

  Bol, Kieran ^a   Marsat, Gary ^a   Harvey Girard, Erik ^a   Longtin, André ^a   Maler, Leonard ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; ELECTRIC FISH; IN VITRO STUDY; IN VIVO STUDY; LONG TERM DEPRESSION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SENSORY FEEDBACK; SENSORY GATING; SIGNAL DETECTION; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; CEREBELLUM; COMPUTER SIMULATION; ELECTRIC FISH; ELECTRIC STIMULATION; FEEDBACK, PHYSIOLOGICAL; LATERAL LINE SYSTEM; LONG-TERM SYNAPTIC DEPRESSION; MODELS, NEUROLOGICAL; NERVE NET; SENSORY RECEPTOR CELLS;

EID: 79960940761     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0193-11.2011     Document Type: Article

References (59)

1. Albus S (1971) A theory of cerebellar function. Math Biosci 10:25-61.
2. Bastian J (1986) Gain-control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6:553-562.
3. Bastian J, Bratton B (1990) Descending control of electroreception. 1. Properties of nucleus-praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe. J Neurosci 10:1226-1240.
4. Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85:10-22.
5. Bastian J, Chacron MJ, Maler L (2004) Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41:767-779.
6. Bell C, Bodznick D, Montgomery J, Bastian J (1997) The generation and subtraction of sensory expectations within cerebellum-like structures. Brain BehavEvol 50:17-31.
7. Benda J, Longtin A, Maler L (2005) Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci 25:2312-2321.
8. Berman NJ, Maler L (1998a) Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). J Neurophysiol 80:3173-3196.
9. Berman NJ, Maler L (1998b) Distal versus proximal inhibitory shaping of feedback excitation in the electrosensory lateral line lobe: implications for sensory filtering. J Neurophysiol 80:3214-3232.
10. Berman NJ, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202:1243-1253.
11. Berman N, Dunn RJ, Maler L (2001) Function of NMDA receptors and persistent sodium channels in a feedback pathway of the electrosensory system. J Neurophysiol 86:1612-1621.
12. Carr CE, Maler L (1986) Electroreception in gymnotiform fish: central anatomy and physiology. In: Electroreception (Bullock TH, Heiligenberg W, eds), pp 319-374. New York: Wiley.
13. Chacron MJ, Doiron B, Maler L, Longtin A, Bastian J (2003) Non-classical receptive field mediates switch in a sensory neuron's frequency tuning. Nature 423:77-81.
14. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
15. D'Angelo E, De Zeeuw CI (2009) Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci 32:30-40.
16. D'Angelo E, Nieus T, Maffei A, Armano S, Rossi P, Taglietti V, Fontana A, Naldi G (2001) Theta-frequency bursting and resonance in cerebellar granule cells: experimental evidence and modeling of a slow Kndependent mechanism. J Neurosci 21:759-770.
17. D'Angelo E, Koekkoek SKE, Lombardo P, Solinas S, Ros E, Garrido J, Schone-wille M, de Zeeuw CI (2009) Timing in the cerebellum: oscillations and resonance in the granular layer. Neuroscience 162:805-815.
18. Dean P, Porrill J, Ekerot CF, Jorntell H (2010) The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat Rev Neurosci 11:30-43.
19. de Zeeuw CI, Hansel C, Bian F, Koekkoek SKE, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495-508.
20. Doiron B, Longtin A, Turner RW, Maler L (2001) Model of gamma fre-quency burst discharge generatedbyconditional backpropagation. JNeu-rophysiol 86:1523-1545.
21. Dugué GP, Brunel N, Hakim V, Schwartz E, Chat M, Lévesque M, Courte-manche R, Léna C, Dieudonné S (2009) Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar golgi cell network. Neuron 61:126-139.
22. du Lac S, Raymond JL, Sejnowski TJ, Lisberger SG (1995) Learning and memory in the vestibuloocular reflex. Annu Rev Neurosci 18:409-441.
23. Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384:564-567.
24. Gussin D, Benda J, Maler L (2007) Limits of linear rate coding of dynamic stimuli by electroreceptor afferents. J Neurophysiol 97:2917-2929.
25. Harvey-Girard E, Dunn RJ, Maler L (2007) Regulated expression of N-methyl-D-aspartate receptors and associated proteins in teleost elec-trosensory system and telencephalon. J Comp Neurol 505:644-668.
26. Harvey-Girard E, Lewis J, Maler L (2010) Burst-induced anti-Hebbian depression acts through short-term synaptic dynamics to cancel redundant sensory signals. J Neurosci 30:6152-6169.
27. Ito M (1984) The cerebellum and neural control. New York: Raven.
28. Jande SS, Maler L, Lawson DEM (1981) Immunohistochemical mapping of vitamin-D-dependent calcium-binding protein in brain. Nature 294: 765-767.
29. Kistler WM, van Hemmen JL, De Zeeuw CI (2000) Time window control: a model for cerebellar function based on synchronization, reverberation, and time slicing. In: Cerebellar modules: molecules, morphology, and function, pp 275-297. New York: Elsevier Science.
30. Lemon N, Turner RW (2000) Conditional spike backpropagation generates burst discharge in a sensory neuron. J Neurophysiol 84:1519-1530.
31. Lewis JE, Maler L (2002) Dynamics of electrosensory feedback: short-term plasticity and inhibition in a parallel fiber pathway. J Neurophysiol 88:1695-1706.
32. Lewis JE, Maler L (2004) Synaptic dynamics on different time scales in a parallel fiber feedback pathway of the weakly electric fish. J Neurophysiol 91:1064-1070.
33. Lisberger SG, Sejnowski TJ (1992) Motor learning in a recurrent network model based on the vestibuloocular reflex. Nature 360:159-161.
34. Lisberger SG, Miles FA, Optican LM (1983) Frequency-selective adaptation-evidence for channels in the vestibulo-ocular reflex. J Neurosci 3:1234-1244.
35. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-366.
36. Maler L (1979) Posterior lateral line lobe of certain gymnotoid fish-quantitative light-microscopy. J Comp Neurol 183:323-363.
37. Maler L (2007) Neural strategies for optimal processing of sensory signals. Prog Brain Res 165:135-154.
38. Maler L, Mugnaini E (1994) Correlating gamma-aminobutyric acidergic circuits and sensory function in the electrosensory lateral line lobe of a gymnotiform fish. J Comp Neurol 345:224-252.
39. Maler L, Jande S, Lawson EM (1984) Localization of vitamin-D-dependent calcium-binding proteininthe electrosensory and electromotor system of high-frequency gymnotid fish. Brain Res 301:166-170.
40. Maler L, Sas E, Johnston S, Ellis W (1991) An atlasof the brain ofthe electric fish Apteronotus leptorhynchus. J Chem Neuroanat 4:1-38.
41. Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437-470.
42. Marsat G, Maler L (2010) Neural heterogeneity and efficient population codes for communication signals. J Neurophysiol 104:2543-2555.
43. Marsat G, Proville RD, Maler L (2009) Transient signals trigger synchronous bursts in an identified population of neurons. J Neurophysiol 102:714-723.
44. Meek J (1992) Why run parallel fibers parallel-teleostean Purkinje-cells as possible coincidence detectors, in a timing device subserving spatial coding of temporal differences. Neuroscience 48:249-283.
45. Mehaffey WH, Doiron B, Maler L, Turner RW (2005) Deterministic multiplicative gain control with active dendrites. J Neurosci 25:9968-9977.
46. Middleton JW, Longtin A, Benda J, Maler L (2006) The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope. Proc Natl Acad Sci U S A 103:14596-14601.
47. Nelson ME, MacIver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences. J Exp Biol 202:1195-1203.
48. Noonan L, Doiron B, Laing C, Longtin A, Turner RW (2003) A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. J Neurosci 23:1524-1534.
49. Oertel D, Young ED (2004) What's a cerebellar circuit doing in the auditory system? Trends Neurosci 27:104-110.
50. Oswald AM, Chacron MJ, Doiron B, Bastian J, Maler L (2004) Parallel processing of sensory input by bursts and isolated spikes. J Neurosci 24:4351-4362.
51. Rancz EA, Ishikawa T, Duguid I, Chadderton P, Mahon S, Häusser M (2007) High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450:1245-1248.
52. Roberts PD, Bell CC (2000) Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J Comput Neu-rosci 9:67-83.
53. Roberts PD, Portfors CV (2008) Design principles of sensory processing in cerebellum-like structures. Biol Cybern 98:491-507.
54. Sas E, Maler L (1987) The organizationofafferent inputtothe caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anat Em-bryol 177:55-79.
55. Saunders J, Bastian J (1984) The physiology and morphology of 2 types of electrosensory neurons in the weakly electric fish Apteronotus lepto-rhynchus. J Comp Physiol 154:199-209.
56. Sawtell NB (2010) Multimodal integration in granule cells as a basis for associative plasticity and sensory prediction in a cerebellum-like circuit. Neuron 66:573-584.
57. Sawtell NB, Williams A (2008) Transformations of electrosensory encoding associated with an adaptive filter. J Neurosci 28:1598-1612.
58. Shumway CA, Maler L (1989) GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish. J Comp Physiol A 164:391-407.
59. Tzounopoulos T, Kraus N (2009) Learning to encode timing: mechanisms of plasticity in the auditory brainstem. Neuron 62:463-469.