STD-dependent and independent encoding of input irregularity as spike rate in a computational model of a cerebellar nucleus neuron

Cerebellum

Volumn 10, Issue 4, 2011, Pages 667-682

  Luthman, Johannes ^a   Hoebeek, Freek E ^b   Maex, Reinoud ^a   Davey, Neil ^a   Adams, Rod ^a   De Zeeuw, Chris I ^b,c   Steuber, Volker ^a  

^a UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Ataxia; Cerebellar nuclei; Purkinje cell; Short term depression; Tottering

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL SYNCHRONIZATION; CEREBELLAR MOSSY FIBER; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; COMPUTER SIMULATION; CONTROLLED STUDY; MOTOR CONTROL; MOUSE; MOUSE MUTANT; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE FUNCTION; NERVE PROJECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SHORT TERM DEPRESSION; SPIKE; SYNAPSE; SYNAPTIC TRANSMISSION; WILD TYPE;

ACTION POTENTIALS; ANIMALS; CEREBELLAR NUCLEI; COMPUTATIONAL BIOLOGY; MICE; MICE, NEUROLOGIC MUTANTS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; PURKINJE CELLS;

EID: 84855942924     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-011-0295-9     Document Type: Article

References (71)

1. Daniel H, Billard JM, Angaut P, Batini C. The interposito-rubrospinal system. Anatomical tracing of a motor control pathway in the rat. Neurosci Res. 1987;5:87-112. (Pubitemid 18013034)
2. Fredette BJ, Mugnaini E. The GABAergic cerebello-olivary projection in the rat. Anat Embryol (Berl). 1991;184:225-43.
3. Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJ. Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res. 2000;124:141-72. (Pubitemid 30604528)
4. Czubayko U, Sultan F, Thier P, Schwarz C. Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings. J Neurophysiol. 2001;85:2017-29. (Pubitemid 32440680)
5. Sultan F, Czubayko U, Thier P. Morphological classification of the rat lateral cerebellar nuclear neurons by principal component analysis. J Comp Neurol. 2003;455:139-55. (Pubitemid 35424253)
6. Uusisaari M, Obata K, Knopfel T. Morphological and electro-physiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol. 2007;97:901-11. (Pubitemid 46143404)
7. Uusisaari M, Knopfel T. GABAergic synaptic communication in the GABAergic and non-GABAergic cells in the deep cerebellar nuclei. Neuroscience. 2008;156:537-49.
8. Uusisaari M, Knopfel T. GlyT2+ neurons in the lateral cerebellar nucleus. Cerebellum. 2010;9:42-55.
9. Gardette R, Debono M, Dupont JL, Crepel F. Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. II. Membrane conductances. Brain Res. 1985;352:97-106. (Pubitemid 15008520)
10. Gardette R, Debono M, Dupont JL, Crepel F. Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. I. Postsynaptic potentials. Brain Res. 1985;351:47-55. (Pubitemid 15075735)
11. Aizenman CD, Linden DJ. Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J Neurophysiol. 1999;82:1697-709. (Pubitemid 29471259)
12. Tadayonnejad R, Mehaffey WH, Anderson D, Turner RW. Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons. Channels (Austin). 2009;3:149-55.
13. De Zeeuw CI, Wylie DR, DiGiorgi PL, Simpson JI. Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol. 1994;349:428-47. (Pubitemid 24328532)
14. De Zeeuw CI, Berrebi AS. Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci. 1995;7:2322-33.
15. Palkovits M, Mezey É, Hámori J, Szentágothai J. Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses. Exp Brain Res. 1977;28:189-209. (Pubitemid 8091312)
16. Telgkamp P, Raman IM. Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci. 2002;22:8447-57. (Pubitemid 35387585)
17. Pedroarena CM, Schwarz C. Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons. J Neurophysiol. 2003;89:704-15. (Pubitemid 36206119)
18. De Zeeuw CI, Hoebeek FE, Schonewille M. Causes and consequences of oscillations in the cerebellar cortex. Neuron. 2008;58:655-8. (Pubitemid 351778474)
19. Shin SL, Hoebeek FE, Schonewille M, de Zeeuw CI, Aertsen A, de Schutter E. Regular patterns in cerebellar Purkinje cell simple spike trains. PLoS One. 2007;2:e485.
20. Hoebeek FE, Stahl JS, van Alphen AM, Schonewille M, Luo C, Rutteman M, et al. Increased noise level of Purkinje cell activities minimizes impact of their modulation during sensorimotor control. Neuron. 2005;45:953-65. (Pubitemid 40395272)
21. Walter JT, Alvina K, Womack MD, Chevez C, Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci. 2006;9:389-97. (Pubitemid 43290969)
22. Green MC, Sidman RL. Tottering - a neuromuscular mutation in the mouse. And its linkage with oligosyndactylism. J Hered. 1962;53:233-7.
23. Silver RA. Neuronal arithmetic. Nat Rev Neurosci. 2010;11:474-89.
24. Steuber V, Schultheiss N, Silver RA, De Schutter E, Jaeger D. Determinants of synaptic integration and heterogeneity in rebound firing explored with data-driven models of deep cerebellar nucleus cells. J Comp Neurosci. 2011;30(3):633-58.
25. Hines ML, Carnevale NT. The NEURON simulation environment. Neural Comput. 1997;9:1179-209. (Pubitemid 127469144)
26. Bower JM, Beeman D. The book of GENESIS: exploring realistic neural models with the GEneral NEural SImulation System. New York: Springer; 1998.
27. Hille B. Ion channels of excitable membranes. Sunderland, MA, USA: Sinauer; 2001.
28. Otis TS, Mody I. Modulation of decay kinetics and frequency of GABAA receptor-mediated spontaneous inhibitory postsynaptic currents in hippocampal neurons. Neuroscience. 1992;49:13-32.
29. Silver RA, Colquhoun D, Cull-Candy SG, Edmonds B. Deactivation and desensitization of non-NMDA receptors in patches and the time course of EPSCs in rat cerebellar granule cells. J Physiol. 1996;493:167-73. (Pubitemid 26152618)
30. Pugh JR, Raman IM. Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron. 2006;51:113-23. (Pubitemid 43963335)
31. Pugh JR, Raman IM. Mechanisms of potentiation of mossy fiber EPSCs in the cerebellar nuclei by coincident synaptic excitation and inhibition. J Neurosci. 2008;28:10549-60.
32. Anchisi D, Scelfo B, Tempia F. Postsynaptic currents in deep cerebellar nuclei. J Neurophysiol. 2001;85:323-31. (Pubitemid 32062142)
33. Gauck V, Jaeger D. The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J Neurosci. 2003;23:8109-18. (Pubitemid 37082464)
34. Telgkamp P, Padgett DE, Ledoux VA, Woolley CS, Raman IM. Maintenance of high-frequency transmission at purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron. 2004;41:113-26. (Pubitemid 38068439)
35. Holt GR, Softky WR, Koch C, Douglas RJ. Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol. 1996;75:1806-14. (Pubitemid 26159018)
36. Monsivais P, Clark BA, Roth A, Hausser M. Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci. 2005;25:464-72. (Pubitemid 40105617)
37. Hoebeek FE, Khosrovani S, Witter L, De Zeeuw CI. Purkinje cell input to cerebellar nuclei in tottering: ultrastructure and physiology. Cerebellum. 2008;7:547-58.
38. Murphy JT, Sabah NH. Spontaneous firing of cerebellar Purkinje cells in decerebrate and barbiturate anesthesized cats. Brain Res. 1970;17:515-9.
39. Armstrong DM, Rawson JA. Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J Physiol (London). 1979;289:425-48. (Pubitemid 9156874)
40. Kahlon M, Lisberger SG. Changes in the responses of Purkinje cells in the floccular complex of monkeys after motor learning in smooth pursuit eye movements. J Neurophysiol. 2000;84:2954-60.
41. Goossens J, Daniel H, Rancillac A, van der Steen J, Oberdick J, Crepel F, et al. Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice. J Neurosci. 2001;21:5813-23. (Pubitemid 32692180)
42. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, et al. Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci. 2005;8:202-11. (Pubitemid 40194051)
43. Shin SL, Rotter S, Aertsen A, De Schutter E. Stochastic description of complex and simple spike firing in cerebellar Purkinje cells. Eur J Neurosci. 2007;25:785-94.
44. Wakamori M, Yamazaki K, Matsunodaira H, Teramoto T, Tanaka I, Niidome T, et al. Single tottering mutations responsible for the neuropathic phenotype of the P-type calcium channel. J Biol Chem. 1998;273:34857-67. (Pubitemid 29028180)
45. Matsushita K, Wakamori M, Rhyu IJ, Arii T, Oda S, Mori Y, et al. Bidirectional alterations in cerebellar synaptic transmission of tottering and rolling Ca2+ channel mutant mice. J Neurosci. 2002;22:4388-98. (Pubitemid 37465655)
46. Zhou YD, Turner TJ, Dunlap K. Enhanced G protein-dependent modulation of excitatory synaptic transmission in the cerebellum of the Ca2+ channel-mutant mouse, tottering. J Physiol. 2003;547:497-507. (Pubitemid 36304983)
47. Meier H, MacPike AD. Three syndromes produced by two mutant genes in the mouse. Clinical, pathological, and ultrastructural bases of tottering, leaner, and heterozygous mice. J Hered. 1971;62:297-302.
48. Isaacs KR, Abbott LC. Development of the paramedian lobule of the cerebellum in wild-type and tottering mice. Dev Neurosci. 1992;14:386-93. (Pubitemid 23124849)
49. Rhyu IJ, Abbott LC, Walker DB, Sotelo C. An ultrastructural study of granule cell/Purkinje cell synapses in tottering (tg/tg), leaner (tg(la)/tg(la)) and compound heterozygous tottering/leaner (tg/tg(la)) mice. Neuroscience. 1999;90:717-28. (Pubitemid 29156738)
50. Hoebeek FE, Witter L, Ruigrok TJ, De Zeeuw CI. Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci U S A. 2010;107 (18):8410-5.
51. Borst JG. The low synaptic release probability in vivo. Trends Neurosci. 2010;33:259-66.
52. Fletcher CF, Lutz CM, O'Sullivan TN, Shaughnessy Jr JD, Hawkes R, Frankel WN, et al. Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell. 1996;87:607-17. (Pubitemid 26386935)
53. Chung YH, Shin C, Park KH, Cha CI. Immunohistochemical study on the distribution of the voltage-gated calcium channel alpha(1B) subunit in the mature rat brain. Brain Res. 2000;866:274-80. (Pubitemid 30313031)
54. Sawada K, Sakata-Haga H, Ando M, Takeda N, Fukui Y. An increased expression of Ca(2+) channel alpha(1A) subunit immunoreactivity in deep cerebellar neurons of rolling mouse Nagoya. Neurosci Lett. 2001;316:87-90. (Pubitemid 34001667)
55. Alvina K, Khodakhah K. Selective regulation of spontaneous activity of neurons of the deep cerebellar nuclei by N-type calcium channels in juvenile rats. J Physiol. 2008;586:2523-38. (Pubitemid 351689810)
56. Pedroarena CM. Mechanisms supporting transfer of inhibitory signals into the spike output of spontaneously firing cerebellar nuclear neurons in vitro. Cerebellum. 2010;9:67-76.
57. Alvina K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K. Questioning the role of rebound firing in the cerebellum. Nat Neurosci. 2008;11(11):1256-8.
58. De Schutter E, Steuber V. Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience. 2009;62(3):816-26.
59. Zucker RS. Short-term synaptic plasticity. Annu Rev Neurosci. 1989;12:13-31. (Pubitemid 19085445)
60. Zucker RS. Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol. 1999;9:305-13. (Pubitemid 29267601)
61. Jones MV, Westbrook GL. The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci. 1996;19:96-101. (Pubitemid 26059993)
62. Otis T, Zhang S, Trussell LO. Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci. 1996;16:7496-504. (Pubitemid 26389688)
63. Varela JA, Sen K, Gibson J, Fost J, Abbott LF, Nelson SB. A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci. 1997;17:7926-40. (Pubitemid 27426228)
64. Chance FS, Nelson SB, Abbott LF. Synaptic depression and the temporal response characteristics of V1 cells. J Neurosci. 1998;18:4785-99. (Pubitemid 28280186)
65. Fortune ES, Rose GJ. Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information. J Neurosci. 2000;20:7122-30.
66. Fortune ES, Rose GJ. Short-term synaptic plasticity as a temporal filter. Trends Neurosci. 2001;24:381-5. (Pubitemid 32938539)
67. Abbott LF, Regehr WG. Synaptic computation. Nature. 2004;431:796-803. (Pubitemid 39434069)
68. Tsodyks MV, Markram H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA. 1997;94:719-23. (Pubitemid 27053700)
69. Galarreta M, Hestrin S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci. 1998;1:587-94.
70. Abbott LF, Varela JA, Sen K, Nelson SB. Synaptic depression and cortical gain control. Science. 1997;275:220-4. (Pubitemid 27034764)
71. Rothman JS, Cathala L, Steuber V, Silver RA. Synaptic depression enables neuronal gain control. Nature. 2009;457:1015-8.