Multiple extra-synaptic spillover mechanisms regulate prolonged activity in cerebellar Golgi cell-granule cell loops

Journal of Physiology

Volumn 589, Issue 15, 2011, Pages 3837-3854

  Holtzman, Tahl ^a,b   Sivam, Vanessa ^a   Zhao, Tian ^a   Frey, Oivier ^d   van der Wal, Peter Dow ^d   de Rooij, Nico F ^d   Dalley, Jeffrey W ^b,c   Edgley, Steve A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR 2; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL POPULATION; CEREBELLUM CORTEX; CONTROLLED STUDY; GOLGI COMPLEX; GRANULE CELL; IN VIVO STUDY; INFORMATION PROCESSING; INTERNEURON; INTRACELLULAR SIGNALING; NEGATIVE FEEDBACK; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SENSORY SYSTEM; SYNAPTIC INHIBITION;

ANIMALS; CEREBELLAR CORTEX; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; NEURAL INHIBITION; NEURONS; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 79960756287     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.207167     Document Type: Article

References (59)

1. Albus JS (1971). A theory of cerebellar function. Math Biosci 10, 25-61.
2. Barbour B (1993). Synaptic currents evoked in Purkinje cells by stimulating individual granule cells. Neuron 11, 759-769.
3. Barmack NH & Yakhnitsa V (2008). Functions of interneurons in mouse cerebellum. J Neurosci 28, 1140-1152.
4. Bengtsson F & Jorntell H (2009). Sensory transmission in cerebellar granule cells relies on similarly coded mossy fiber inputs. Proc Natl Acad Sci U S A 106, 2389-2394.
5. A receptors. J Physiol 497, 753-759.
6. Chadderton P, Margrie TW & Hausser M (2004). Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860.
7. Cirone J & Salt TE (2001). Group II and III metabotropic glutamate receptors contribute to different aspects of visual response processing in the rat superior colliculus. J Physiol 534, 169-178.
8. Crowley JJ, Fioravante D & Regehr WG (2009). Dynamics of fast and slow inhibition from cerebellar golgi cells allow flexible control of synaptic integration. Neuron 63, 843-853.
9. D'Angelo E & De Zeeuw CI (2009). Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci 32, 30-40.
10. Davey NJ, Ellaway PH & Stein RB (1986). Statistical limits for detecting change in the cumulative sum derivative of the peristimulus time histogram. J Neurosci Methods 17, 153-166.
11. Dino MR, Willard FH & Mugnaini E (1999). Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex. J Neurocytol 28, 99-123.
12. Dugue GP, Brunel N, Hakim V, Schwartz E, Chat M, Levesque M, Courtemanche R, Lena C & Dieudonne S (2009). Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron 61, 126-139.
13. Dugue GP, Dumoulin A, Triller A & Dieudonne S (2005). Target-dependent use of co-released inhibitory transmitters at central synapses. J Neurosci 25, 6490-6498.
14. Dumoulin A, Triller A & Dieudonne S (2001). IPSC kinetics at identified GABAergic and mixed GABAergic and glycinergic synapses onto cerebellar Golgi cells. J Neurosci 21, 6045-6057.
15. Eccles JC, Faber DS, Murphy JT, Sabah NH & Taborikova H (1971). Afferent volleys in limb nerves influencing impulse discharges in cerebellar cortex. I. In mossy fibers and granule cells. Exp Brain Res 13, 15-35.
16. Eccles JC, Llinas R & Sasaki K (1966). The mossy fibre-granule cell relay of the cerebellum and its inhibitory control by Golgi cells. Exp Brain Res 1, 82-101.
17. Eckhorn R & Thomas U (1993). A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors. J Neurosci Methods 49, 175-179.
18. Edgley SA & Lidierth M (1987). The discharges of cerebellar Golgi cells during locomotion in the cat. J Physiol 392, 315-332.
19. Frey O, Holtzman T, McNamara RM, Theobald DE, van der Wal PD, de Rooij NF, Dalley JW & Koudelka-Hep M (2010). Enzyme-based choline and L-glutamate biosensor electrodes on silicon microprobe arrays. Biosens Bioelectron 26, 477-484.
20. Gabbiani F, Midtgaard J & Knopfel T (1994). Synaptic integration in a model of cerebellar granule cells. J Neurophysiol 72, 999-1009.
21. Gai Y & Carney LH (2008). Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. J Neurophysiol 99, 1077-1095.
22. Holtzman T, Cerminara NL, Edgley SA & Apps R (2009). Characterization in vivo of bilaterally branching pontocerebellar mossy fibre to Golgi cell inputs in the rat cerebellum. J Neurosci 29, 328-339.
23. Holtzman T, Rajapaksa T, Mostofi A & Edgley SA (2006). Different responses of rat cerebellar Purkinje cells and Golgi cells evoked by widespread convergent sensory inputs. J Physiol 574, 491-507.
24. Iwamoto Y, Kaneko H, Yoshida K & Shimazu H (2009). Role of glycinergic inhibition in shaping activity of saccadic burst neurons. J Neurophysiol 101, 3063-3074.
25. Jaarsma D, Dino MR, Ohishi H, Shigemoto R & Mugnaini E (1998). Metabotropic glutamate receptors are associated with non-synaptic appendages of unipolar brush cells in rat cerebellar cortex and cochlear nuclear complex. J Neurocytol 27, 303-327.
26. Jakab RL & Hamori J (1988). Quantitative morphology and synaptology of cerebellar glomeruli in the rat. Anat Embryol (Berl) 179, 81-88.
27. Jorntell H & Ekerot CF (2006). Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci 26, 11786-11797.
28. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S & Schoepp DD (1998). LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37, 1-12.
29. Kutscher A & Covey E (2009). Functional role of GABAergic and glycinergic inhibition in the intermediate nucleus of the lateral lemniscus of the big brown bat. J Neurophysiol 101, 3135-3146.
30. Lujan R, Roberts JD, Shigemoto R, Ohishi H & Somogyi P (1997). Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1α, mGluR2 and mGluR5, relative to neurotransmitter release sites. J Chem Neuroanat 13, 219-241.
31. Ma D, Hongqi T, Hongbin S, Kozikowski AP, Pshenichkin S & Wroblewski JT (1997). Synthesis and biological activity of cyclic analogues of MPPG and MCPG as metabotropic glutamate receptor antagonists. Bioorg Med Chem Lett 7, 1195-1198.
32. Maex R & De Schutter E (1998). Synchronization of golgi and granule cell firing in a detailed network model of the cerebellar granule cell layer. J Neurophysiol 80, 2521-2537.
33. B receptors reduces release probability at inhibitory connections in the cerebellar glomerulus. J Neurophysiol 101, 3089-3099.
34. Marr D (1969). A theory of cerebellar cortex. J Physiol 202, 437-470.
35. Medina JF & Mauk MD (2000). Computer simulation of cerebellar information processing. Nat Neurosci 3, 1205-1211.
36. Mitchell SJ & Silver RA (2000a). Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404, 498-502.
37. Mitchell SJ & Silver RA (2000b). GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J Neurosci 20, 8651-8658.
38. Mitchell SJ & Silver RA (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445.
39. A receptors. J Physiol 588, 1251-1268.
40. A receptor ion channels by full and partial agonists. J Physiol 557, 389-413.
41. Ohishi H, Ogawa-Meguro R, Shigemoto R, Kaneko T, Nakanishi S & Mizuno N (1994). Immunohistochemical localization of metabotropic glutamate receptors, mGluR2 and mGluR3, in rat cerebellar cortex. Neuron 13, 55-66.
42. Ohyama T, Nores WL, Murphy M & Mauk MD (2003). What the cerebellum computes. Trends Neurosci 26, 222-227.
43. Perroy J, Prezeau L, De Waard M, Shigemoto R, Bockaert J & Fagni L (2000). Selective blockade of P/Q-type calcium channels by the metabotropic glutamate receptor type 7 involves a phospholipase C pathway in neurons. J Neurosci 20, 7896-7904.
44. Prsa M, Dash S, Catz N, Dicke PW & Thier P (2009). Characteristics of responses of Golgi cells and mossy fibers to eye saccades and saccadic adaptation recorded from the posterior vermis of the cerebellum. J Neurosci 29, 250-262.
45. Rancz EA, Ishikawa T, Duguid I, Chadderton P, Mahon S & Hausser M (2007). High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450, 1245-1248.
46. A receptors and glomerular geometry. Neuron 20, 783-795.
47. Sanchez JT, Gans D & Wenstrup JJ (2008). Glycinergic 'inhibition' mediates selective excitatory responses to combinations of sounds. J Neurosci 28, 80-90.
48. Shambes GM, Gibson JM & Welker W (1978). Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15, 94-140.
49. A receptors: Functional selectivity for extrasynaptic receptors is dependent on the absence of γ2. J Pharmacol Exp Ther 316, 1351-1359.
50. Tempia F, Miniaci MC, Anchisi D & Strata P (1998). Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J Neurophysiol 80, 520-528.
51. Thach WT Jr (1967). Somatosensory receptive fields of single units in cat cerebellar cortex. J Neurophysiol 30, 675-696.
52. Thompson RF & Steinmetz JE (2009). The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162, 732-755.
53. Van Welie I & Hausser M (2009). Sensory-driven excitation in cerebellar Lugaro cells revealed by in vivo targeted patch-clamp recordings. 2009 Abstract Viewer/Itinerary Planner, Programme No. 367.18/DD40. Society for Neuroscience, Washington, DC.
54. Vervaeke K, Lorincz A, Gleeson P, Farinella M, Nusser Z & Silver RA (2010). Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 67, 435-451.
55. Vos BP, Volny-Luraghi A & De Schutter E (1999). Cerebellar Golgi cells in the rat: receptive fields and timing of responses to facial stimulation. Eur J Neurosci 11, 2621-2634.
56. Watanabe D & Nakanishi S (2003). mGluR2 postsynaptically senses granule cell inputs at Golgi cell synapses. Neuron 39, 821-829.
57. Yamamoto C, Yamashita H & Chujo T (1976). Inhibitory action of glutamic acid on cerebellar interneurones. Nature 262, 786-787.
58. Yamazaki T & Tanaka S (2009). Computational models of timing mechanisms in the cerebellar granular layer. Cerebellum 8, 423-432.
59. Yeo CH & Hesslow G (1998). Cerebellum and conditioned reflexes. Trends Cogn Sci 2, 322-330.