In vivo analysis of inhibitory synaptic inputs and rebounds in deep cerebellar nuclear neurons

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Bengtsson, Fredrik ^a   Ekerot, Carl Fredrik ^a   Jörntell, Henrik ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CAT; CELL ACTIVATION; CELL ACTIVITY; CELL INTERACTION; CELL STIMULATION; CEREBELLUM NUCLEUS; CONTROLLED STUDY; IN VIVO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL INHIBITION; NONHUMAN; PATCH CLAMP; PURKINJE CELL; SENSORY STIMULATION; SPIKE WAVE; SYNAPTIC INHIBITION; WHOLE CELL; ANIMAL; CYTOLOGY; ELECTROSTIMULATION; EVOKED RESPONSE; NERVE CELL; OLIVARY NUCLEUS; PHYSIOLOGY; SKIN;

ANIMALS; CATS; CEREBELLAR NUCLEI; ELECTRIC STIMULATION; EVOKED POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; NEURONS; OLIVARY NUCLEUS; PURKINJE CELLS; SKIN;

EID: 79955744271     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018822     Document Type: Article

References (69)

1. Destexhe A, Contreras D, (2006) Neuronal computations with stochastic network states. Science 314: 85-90.
2. Destexhe A, Rudolph M, Pare D, (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751.
3. Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T, (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8: 1760-1767.
4. Gauck V, Jaeger D, (2000) The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. Journal of Neuroscience 20: 3006-3016.
5. Anderson JS, Lampl I, Gillespie DC, Ferster D, (2000) The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290: 1968-1972.
6. Gauck V, Jaeger D, (2003) The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J Neurosci 23: 8109-8118.
7. Jahnsen H, (1986) Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. j 372: 129-147.
8. Aizenman CD, Manis PB, Linden DJ, (1998) Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron 21: 827-835.
9. Kistler WM, De Zeeuw CI, (2003) Time windows and reverberating loops: a reverse-engineering approach to cerebellar function. Cerebellum 2: 44-54.
10. Medina JF, Nores WL, Ohyama T, Mauk MD, (2000) Mechanisms of cerebellar learning suggested by eyelid conditioning. Current Opinion in Neurobiology 10: 717-724.
11. Wetmore DZ, Mukamel EA, Schnitzer MJ, (2008) Lock-and-key mechanisms of cerebellar memory recall based on rebound currents. J Neurophysiol 100: 2328-2347.
12. Jacobson GA, Rokni D, Yarom Y, (2008) A model of the olivo-cerebellar system as a temporal pattern generator. Trends in Neurosciences 31: 617-625.
13. Cerminara NL, Rawson JA, (2004) Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. Journal of Neuroscience 24: 4510-4517.
14. Hoebeek FE, Witter L, Ruigrok TJ, De Zeeuw CI, (2010) Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci U S A 107: 8410-8415.
15. Kitai ST, McCrea RA, Preston RJ, Bishop GA, (1977) Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. I. Climbing fiber system. Brain Res 122: 197-214.
16. Apps R, Hawkes R, (2009) Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10: 670-681.
17. Ekerot CF, Garwicz M, Schouenborg J, (1991) Topography and nociceptive receptive fields of climbing fibres projecting to the cerebellar anterior lobe in the cat. Journal of Physiology (London) 441: 257-274.
18. Garwicz M, Apps R, Trott JR, (1996) Micro-organization of olivocerebellar and corticonuclear connections of the paravermal cerebellum in the cat. European Journal of Neuroscience 8: 2726-2738.
19. Garwicz M, Ekerot CF, (1994) Topographical organization of the cerebellar cortical projection to nucleus interpositus anterior in the cat. Journal of Physiology (London) 474: 245-260.
20. Apps R, Garwicz M, (2005) Anatomical and physiological foundations of cerebellar information processing. Nature Reviews: Neuroscience 6: 297-311.
21. Apps R, Garwicz M, (2000) Precise matching of olivo-cortical divergence and cortico-nuclear convergence between somatotopically corresponding areas in the medial C1 and medial C3 zones of the paravermal cerebellum. European Journal of Neuroscience 12: 205-214.
22. Sugihara I, (2010) Compartmentalization of the Deep Cerebellar Nuclei Based on Afferent Projections and Aldolase C Expression. Cerebellum.
23. Ito M, (1984) The Cerebellum and Neural Control New York Raven Press.
24. Oscarsson O, (1979) Functional units of the cerebellum- sagittal zones and microzones. Trends in Neurosciences 2: 144-145.
25. Andersson G, Oscarsson O, (1978) Climbing fiber microzones in cerebellar vermis and their projection to different groups of cells in the lateral vestibular nucleus. Experimental Brain Research 32: 565-579.
26. Uusisaari M, Obata K, Knopfel T, (2007) Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol 97: 901-911.
27. Gauck V, Thomann M, Jaeger D, Borst A, (2001) Spatial distribution of low- and high-voltage-activated calcium currents in neurons of the deep cerebellar nuclei. J Neurosci 21: RC158.
28. Pedroarena CM, Schwarz C, (2003) Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons. J Neurophysiol 89: 704-715.
29. Cerminara NL, Apps R, Marple-Horvat DE, (2009) An internal model of a moving visual target in the lateral cerebellum. J Physiol 587: 429-442.
30. Palkovits M, Mezey E, Hamori J, Szentagothai J, (1977) Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and synapses. Exp Brain Res 28: 189-209.
31. Zheng N, Raman IM, (2009) Ca currents activated by spontaneous firing and synaptic disinhibition in neurons of the cerebellar nuclei. J Neurosci 29: 9826-9838.
32. Ekerot CF, Larson B, (1979) The dorsal spino-olivocerebellar system in the cat. II. Somatotopical organization. Experimental Brain Research 36: 219-232.
33. Sugihara I, Wu HS, Shinoda Y, (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to Cerebellar compartmentalization. J Neurosci 21: 7715-7723.
34. Chorev E, Yarom Y, Lampl I, (2007) Rhythmic episodes of subthreshold membrane potential oscillations in the rat inferior olive nuclei in vivo. J Neurosci 27: 5043-5052.
35. Bengtsson F, Jorntell H, (2009) Climbing Fiber Coupling between Adjacent Purkinje Cell Dendrites in Vivo. Front Cell Neurosci 3: 7.
36. Llinas R, Muhlethaler M, (1988) Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol 404: 241-258.
37. Alvina K, Ellis-Davies G, Khodakhah K, (2009) T-type calcium channels mediate rebound firing in intact deep cerebellar neurons. Neuroscience 158: 635-641.
38. 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.
39. Ekerot CF, Jorntell H, (2001) Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. EurJNeurosci 13: 1303-1310.
40. Jorntell H, Ekerot CF, (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34: 797-806.
41. De Zeeuw CI, Koekkoek SK, Wylie DR, Simpson JI, (1997) Association between dendritic lamellar bodies and complex spike synchrony in the olivocerebellar system. J Neurophysiol 77: 1747-1758.
42. Wise AK, Cerminara NL, Marple-Horvat DE, Apps R, (2010) Mechanisms of synchronous activity in cerebellar Purkinje cells. J Physiol 588: 2373-2390.
43. Sultan F, Konig T, Mock M, Thier P, (2002) Quantitative organization of neurotransmitters in the deep cerebellar nuclei of the Lurcher mutant. J Comp Neurol 452: 311-323.
44. Matsushita M, Iwahori N, (1971) Structural organization of the interpositus and the dentate nuclei. Brain Res 35: 17-36.
45. De Zeeuw CI, Berrebi AS, (1996) Individual Purkinje cell axons terminate on both inhibitory and excitatory neurons in the cerebellar and vestibular nuclei. AnnNYAcadSci 781: 607-610.
46. Raman IM, Gustafson AE, Padgett D, (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. Journal of Neuroscience 20: 9004-9016.
47. Ekerot CF, Jorntell H, (2003) Parallel fiber receptive fields: a key to understanding cerebellar operation and learning. Cerebellum 2: 101-109.
48. Jorntell H, Hansel C, (2006) Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron 52: 227-238.
49. Jorntell H, Bengtsson F, Schonewille M, De Zeeuw CI, (2010) Cerebellar molecular layer interneurons- computational properties and roles in learning. Trends Neurosci 33: 524-532.
50. Medina JF, Lisberger SG, (2007) Variation, signal, and noise in cerebellar sensory-motor processing for smooth-pursuit eye movements. J Neurosci 27: 6832-6842.
51. Alvina K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K, (2008) Questioning the role of rebound firing in the cerebellum. Nat Neurosci 11: 1256-1258.
52. Hesslow G, (1994) Inhibition of classically conditioned eyeblink responses by stimulation of the cerebellar cortex in the decerebrate cat. Journal of Physiology (London) 476: 245-256.
53. Molineux ML, McRory JE, McKay BE, Hamid J, Mehaffey WH, et al. (2006) Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc Natl Acad Sci U S A 103: 5555-5560.
54. Sangrey T, Jaeger D, (2010) Analysis of distinct short and prolonged components in rebound spiking of deep cerebellar nucleus neurons. Eur J Neurosci 32: 1646-1657.
55. Pasalar S, Roitman AV, Durfee WK, Ebner TJ, (2006) Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci 9: 1404-1411.
56. Armstrong DM, Rawson JA, (1979) Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. Journal of Physiology (London) 289: 425-448.
57. Lang EJ, Sugihara I, Welsh JP, Llinas R, (1999) Patterns of spontaneous purkinje cell complex spike activity in the awake rat. J Neurosci 19: 2728-2739.
58. Apps R, Atkins MJ, Garwicz M, (1997) Gating of cutaneous input to cerebellar climbing fibres during a reaching task in the cat. Journal of Physiology (London) 502 (Pt 1): 203-214.
59. van Kan PL, Houk JC, Gibson AR, (1993) Output organization of intermediate cerebellum of the monkey. J Neurophysiol 69: 57-73.
60. Gibson AR, Horn KM, Pong M, (2004) Activation of climbing fibers. Cerebellum 3: 212-221.
61. Horn KM, Pong M, Gibson AR, (2004) Discharge of inferior olive cells during reaching errors and perturbations. Brain Res 996: 148-158.
62. Sugihara I, Marshall SP, Lang EJ, (2007) Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in Crus IIa of the rat cerebellar cortex. Journal of Comparative Neurology 501: 13-29.
63. Horn KM, Van Kan PL, Gibson AR, (1996) Reduction of rostral dorsal accessory olive responses during reaching. J Neurophysiol 76: 4140-4151.
64. Mason CR, Miller LE, Baker JF, Houk JC, (1998) Organization of reaching and grasping movements in the primate cerebellar nuclei as revealed by focal muscimol inactivations. J Neurophysiol 79: 537-554.
65. Jorntell H, Ekerot CF, (2003) Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. Journal of Neuroscience 23: 9620-9631.
66. Jorntell H, Ekerot CF, (2006) Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. Journal of Neuroscience 26: 11786-11797.
67. Ekerot CF, Jorntell H, Garwicz M, (1995) Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat. Experimental Brain Research 106: 365-376.
68. Jorntell H, Ekerot CF, (1999) Topographical organization of projections to cat motor cortex from nucleus interpositus anterior and forelimb skin. Journal of Physiology (London) 514 (Pt 2): 551-566.
69. 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.