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Published in: The Cerebellum 5/2013

01-10-2013 | Original Paper

Gain Control of Synaptic Response Function in Cerebellar Nuclear Neurons by a Calcium-Activated Potassium Conductance

Authors: Steven Si Feng, Risa Lin, Volker Gauck, Dieter Jaeger

Published in: The Cerebellum | Issue 5/2013

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Abstract

Small conductance Ca2+-activated potassium (SK) current provides an important modulator of excitatory synaptic transmission, which undergoes plastic regulation via multiple mechanisms. We examined whether inhibitory input processing is also dependent on SK current in the cerebellar nuclei (CN) where inhibition provides the only route of information transfer from the cerebellar cortical Purkinje cells. We employed dynamic clamping in conjunction with computer simulations to address this question. We found that SK current plays a critical role in the inhibitory synaptic control of spiking output. Specifically, regulation of SK current density resulted in a gain control of spiking output, such that low SK current promoted large output signaling for large inhibitory cell input fluctuations due to Purkinje cell synchronization. In contrast, smaller nonsynchronized Purkinje cell input fluctuations were not amplified. Regulation of SK density in the CN therefore would likely lead to important consequences for the transmission of synchronized Purkinje cell activity to the motor system.
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Literature
1.
go back to reference Palkovits M, Mezey E, Hamori J, Szentagothai J. Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and synapses. Exp Brain Res. 1977;28:189–209.PubMed Palkovits M, Mezey E, Hamori J, Szentagothai J. Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and synapses. Exp Brain Res. 1977;28:189–209.PubMed
2.
go back to reference Jaeger D. Mini-review: synaptic integration in the cerebellar nuclei—perspectives from dynamic clamp and computer simulation studies. Cerebellum. 2011;10:659–66.PubMedCrossRef Jaeger D. Mini-review: synaptic integration in the cerebellar nuclei—perspectives from dynamic clamp and computer simulation studies. Cerebellum. 2011;10:659–66.PubMedCrossRef
3.
go back to reference Walter JT, Khodakhah K. The linear computational algorithm of cerebellar Purkinje cells. J Neurosci. 2006;26:12861–72.PubMedCrossRef Walter JT, Khodakhah K. The linear computational algorithm of cerebellar Purkinje cells. J Neurosci. 2006;26:12861–72.PubMedCrossRef
4.
go back to reference Walter JT, Khodakhah K. The advantages of linear information processing for cerebellar computation. Proc Natl Acad Sci U S A. 2009;106:4471–6.PubMedCrossRef Walter JT, Khodakhah K. The advantages of linear information processing for cerebellar computation. Proc Natl Acad Sci U S A. 2009;106:4471–6.PubMedCrossRef
5.
go back to reference Gauck V, Jaeger D. The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci. 2000;20:3006–16.PubMed Gauck V, Jaeger D. The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci. 2000;20:3006–16.PubMed
6.
go back to reference De Zeeuw CI, Hoebeek FE, Bosman LWJ, Schonewille M, Witter L, Koekkoek SK. Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci. 2011;12:327–44.PubMedCrossRef De Zeeuw CI, Hoebeek FE, Bosman LWJ, Schonewille M, Witter L, Koekkoek SK. Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci. 2011;12:327–44.PubMedCrossRef
7.
go back to reference Shin SL, De Schutter E. Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol. 2006;96:3485–91.PubMedCrossRef Shin SL, De Schutter E. Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol. 2006;96:3485–91.PubMedCrossRef
8.
go back to reference Jahnsen H. Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol. 1986;372:129–47.PubMed Jahnsen H. Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol. 1986;372:129–47.PubMed
9.
go back to reference Uusisaari M, Obata K, Knopfel T. Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol. 2007;97:901–11.PubMedCrossRef Uusisaari M, Obata K, Knopfel T. Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol. 2007;97:901–11.PubMedCrossRef
10.
go back to reference Molineux ML, Mehaffey WH, Tadayonnejad R, Anderson D, Tennent AF, Turner RW. Ionic factors governing rebound burst phenotype in rat deep cerebellar neurons. J Neurophysiol. 2008;100:2684–701.PubMedCrossRef Molineux ML, Mehaffey WH, Tadayonnejad R, Anderson D, Tennent AF, Turner RW. Ionic factors governing rebound burst phenotype in rat deep cerebellar neurons. J Neurophysiol. 2008;100:2684–701.PubMedCrossRef
11.
go back to reference Molineux ML, McRory JE, McKay BE, Hamid J, Mehaffey WH, Rehak R, et al. Specific t-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc Natl Acad Sci U S A. 2006;103:5555–60.PubMedCrossRef Molineux ML, McRory JE, McKay BE, Hamid J, Mehaffey WH, Rehak R, et al. Specific t-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc Natl Acad Sci U S A. 2006;103:5555–60.PubMedCrossRef
12.
go back to reference Alvina K, Ellis-Davies G, Khodakhah K. T-type calcium channels mediate rebound firing in intact deep cerebellar neurons. Neuroscience. 2009;158:635–41.PubMedCrossRef Alvina K, Ellis-Davies G, Khodakhah K. T-type calcium channels mediate rebound firing in intact deep cerebellar neurons. Neuroscience. 2009;158:635–41.PubMedCrossRef
13.
go back to reference Sangrey T, Jaeger D. Multiple components of rebound spiking in deep cerebellar nucleus neurons. Eur J Neurosci. 2010;32:1646–57.PubMedCrossRef Sangrey T, Jaeger D. Multiple components of rebound spiking in deep cerebellar nucleus neurons. Eur J Neurosci. 2010;32:1646–57.PubMedCrossRef
14.
go back to reference 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;107:8410–5.PubMedCrossRef 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;107:8410–5.PubMedCrossRef
15.
go back to reference Bengtsson F, Ekerot CF, Jorntell H. In vivo analysis of inhibitory synaptic inputs and rebounds in deep cerebellar nuclear neurons. PLoS One. 2011;6:e18822. Bengtsson F, Ekerot CF, Jorntell H. In vivo analysis of inhibitory synaptic inputs and rebounds in deep cerebellar nuclear neurons. PLoS One. 2011;6:e18822.
16.
go back to reference Lang EJ, Sugihara I, Welsh JP, Llinas R. Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J Neurosci. 1999;19:2728–39.PubMed Lang EJ, Sugihara I, Welsh JP, Llinas R. Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J Neurosci. 1999;19:2728–39.PubMed
17.
go back to reference Schultz SR, Kitamura K, Post-Uiterweer A, Krupic J, Hausser M. Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje cells. J Neurosci. 2009;29:8005–15.PubMedCrossRef Schultz SR, Kitamura K, Post-Uiterweer A, Krupic J, Hausser M. Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje cells. J Neurosci. 2009;29:8005–15.PubMedCrossRef
18.
go back to reference Ozden I, Sullivan MR, Lee HM, Wang SSH. Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar purkinje neurons. J Neurosci. 2009;29:10463–73.PubMedCrossRef Ozden I, Sullivan MR, Lee HM, Wang SSH. Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar purkinje neurons. J Neurosci. 2009;29:10463–73.PubMedCrossRef
19.
go back to reference 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.PubMed 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.PubMed
20.
go back to reference Raman IM, Gustafson AE, Padgett D. Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci. 2000;20:9004–16.PubMed Raman IM, Gustafson AE, Padgett D. Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci. 2000;20:9004–16.PubMed
21.
go back to reference Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal ca1 pyramidal neurons. J Neurosci. 1998;18:7613–24.PubMed Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal ca1 pyramidal neurons. J Neurosci. 1998;18:7613–24.PubMed
22.
go back to reference Chan CS, Shigemoto R, Mercer JN, Surmeier DJ. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J Neurosci. 2004;24:9921–32.PubMedCrossRef Chan CS, Shigemoto R, Mercer JN, Surmeier DJ. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J Neurosci. 2004;24:9921–32.PubMedCrossRef
23.
go back to reference Wolfart J, Roeper J. Selective coupling of t-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J Neurosci. 2002;22:3404–13.PubMed Wolfart J, Roeper J. Selective coupling of t-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J Neurosci. 2002;22:3404–13.PubMed
24.
go back to reference Deister CA, Chan CS, Surmeier DJ, Wilson CJ. Calcium-activated SK channels influence voltage-gated ion channels to determine the precision of firing in globus pallidus neurons. J Neurosci. 2009;29:8452–61.PubMedCrossRef Deister CA, Chan CS, Surmeier DJ, Wilson CJ. Calcium-activated SK channels influence voltage-gated ion channels to determine the precision of firing in globus pallidus neurons. J Neurosci. 2009;29:8452–61.PubMedCrossRef
25.
go back to reference Canavier CC, Landry RS. An increase in AMPA and a decrease in SK conductance increase burst firing by different mechanisms in a model of a dopamine neuron in vivo. J Neurophysiol. 2006;96:2549–63.PubMedCrossRef Canavier CC, Landry RS. An increase in AMPA and a decrease in SK conductance increase burst firing by different mechanisms in a model of a dopamine neuron in vivo. J Neurophysiol. 2006;96:2549–63.PubMedCrossRef
26.
go back to reference 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.PubMed 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.PubMed
27.
go back to reference Person AL, Raman IM. Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature. 2012;481:502–6.CrossRef Person AL, Raman IM. Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature. 2012;481:502–6.CrossRef
28.
go back to reference Pugh JR, Raman IM. GABAA receptor kinetics in the cerebellar nuclei: evidence for detection of transmitter from distant release sites. Biophys J. 2005;88:1740–54.PubMedCrossRef Pugh JR, Raman IM. GABAA receptor kinetics in the cerebellar nuclei: evidence for detection of transmitter from distant release sites. Biophys J. 2005;88:1740–54.PubMedCrossRef
29.
go back to reference Anchisi D, Scelfo B, Tempia F. Postsynaptic currents in deep cerebellar nuclei. J Neurophysiol. 2001;85:323–31.PubMed Anchisi D, Scelfo B, Tempia F. Postsynaptic currents in deep cerebellar nuclei. J Neurophysiol. 2001;85:323–31.PubMed
30.
go back to reference Steuber V, Schultheiss NW, 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 Comput Neurosci. 2011;30:633–58.PubMedCrossRef Steuber V, Schultheiss NW, 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 Comput Neurosci. 2011;30:633–58.PubMedCrossRef
31.
go back to reference Steuber V, De Schutter E, Jaeger D. Passive models of neurons in the deep cerebellar nuclei: the effect of reconstruction errors. Neurocomputing. 2004;58–60:563–8.CrossRef Steuber V, De Schutter E, Jaeger D. Passive models of neurons in the deep cerebellar nuclei: the effect of reconstruction errors. Neurocomputing. 2004;58–60:563–8.CrossRef
32.
go back to reference Jahnsen H. Extracellular activation and membrane conductances of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol. 1986;372:149–68.PubMed Jahnsen H. Extracellular activation and membrane conductances of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol. 1986;372:149–68.PubMed
33.
go back to reference Llinas R, Muhlethaler M. Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol. 1988;404:241–58.PubMed Llinas R, Muhlethaler M. Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol. 1988;404:241–58.PubMed
34.
go back to reference Bower J, Beeman D. The book of genesis. New York: Springer; 1997. Bower J, Beeman D. The book of genesis. New York: Springer; 1997.
35.
go back to reference Lin RJ, Jaeger D. Using computer simulations to determine the limitations of dynamic clamp stimuli applied at the soma in mimicking distributed conductance sources. J Neurophysiol. 2011;105:2610–24.PubMedCrossRef Lin RJ, Jaeger D. Using computer simulations to determine the limitations of dynamic clamp stimuli applied at the soma in mimicking distributed conductance sources. J Neurophysiol. 2011;105:2610–24.PubMedCrossRef
36.
go back to reference Feng S, Jaeger D. The role of SK calcium-dependent potassium currents in regulating the activity of deep cerebellar nucleus neurons: a dynamic clamp study. Cerebellum. 2008;7:542–6.PubMedCrossRef Feng S, Jaeger D. The role of SK calcium-dependent potassium currents in regulating the activity of deep cerebellar nucleus neurons: a dynamic clamp study. Cerebellum. 2008;7:542–6.PubMedCrossRef
37.
go back to reference Bennett BD, Callaway JC, Wilson CJ. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci. 2000;20:8493–503.PubMed Bennett BD, Callaway JC, Wilson CJ. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci. 2000;20:8493–503.PubMed
38.
go back to reference Nedergaard S, Flatman JA, Engberg I. Nifedipine-conotoxin-sensitive and omega-conotoxin-sensitive Ca2+ conductances in guinea-pig substantia nigra-pars-compacta neurons. J Physiol Lond. 1993;466:727–47.PubMed Nedergaard S, Flatman JA, Engberg I. Nifedipine-conotoxin-sensitive and omega-conotoxin-sensitive Ca2+ conductances in guinea-pig substantia nigra-pars-compacta neurons. J Physiol Lond. 1993;466:727–47.PubMed
39.
go back to reference De Waele C, Serafin M, Khateb A, Yabe T, Vidal PP, Muhlethaler M. Medial vestibular nucleus in the guinea-pig—apamin-induced rhythmic burst firing—an in-vitro and in-vivo study. Exp Brain Res. 1993;95:213–22.PubMedCrossRef De Waele C, Serafin M, Khateb A, Yabe T, Vidal PP, Muhlethaler M. Medial vestibular nucleus in the guinea-pig—apamin-induced rhythmic burst firing—an in-vitro and in-vivo study. Exp Brain Res. 1993;95:213–22.PubMedCrossRef
40.
go back to reference McKay BE, McRory JE, Molineux ML, Hamid J, Snutch TP, Zamponi GW, et al. Ca(v)3 t-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur J Neurosci. 2006;24:2581–94.PubMedCrossRef McKay BE, McRory JE, Molineux ML, Hamid J, Snutch TP, Zamponi GW, et al. Ca(v)3 t-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur J Neurosci. 2006;24:2581–94.PubMedCrossRef
41.
go back to reference 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 Lond. 2008;586:2523–38.PubMedCrossRef 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 Lond. 2008;586:2523–38.PubMedCrossRef
42.
go back to reference Giessel AJ, Sabatini BL. M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron. 2010;68:936–47.PubMedCrossRef Giessel AJ, Sabatini BL. M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron. 2010;68:936–47.PubMedCrossRef
43.
go back to reference Maylie J, Adelman JP. Cholinergic signaling through synaptic SK channels: it's a protein kinase but which one? Neuron. 2010;68:809–11.PubMedCrossRef Maylie J, Adelman JP. Cholinergic signaling through synaptic SK channels: it's a protein kinase but which one? Neuron. 2010;68:809–11.PubMedCrossRef
44.
go back to reference Womack MD, Chevez C, Khodakhah K. Calcium-activated potassium channels are selectively coupled to p/q-type calcium channels in cerebellar purkinje neurons. J Neurosci. 2004;24:8818–22.PubMedCrossRef Womack MD, Chevez C, Khodakhah K. Calcium-activated potassium channels are selectively coupled to p/q-type calcium channels in cerebellar purkinje neurons. J Neurosci. 2004;24:8818–22.PubMedCrossRef
45.
go back to reference Hosy E, Piochon C, Teuling E, Rinaldo L, Hansel C. SK2 channel expression and function in cerebellar Purkinje cells. J Physiol Lond. 2011;589:3433–40.PubMedCrossRef Hosy E, Piochon C, Teuling E, Rinaldo L, Hansel C. SK2 channel expression and function in cerebellar Purkinje cells. J Physiol Lond. 2011;589:3433–40.PubMedCrossRef
46.
go back to reference Belmeguenai A, Hosy E, Bengtsson F, Pedroarena CM, Piochon C, Teuling E, et al. Intrinsic plasticity complements long-term potentiation in parallel fiber input gain control in cerebellar Purkinje cells. J Neurosci. 2010;30:13630–43.PubMedCrossRef Belmeguenai A, Hosy E, Bengtsson F, Pedroarena CM, Piochon C, Teuling E, et al. Intrinsic plasticity complements long-term potentiation in parallel fiber input gain control in cerebellar Purkinje cells. J Neurosci. 2010;30:13630–43.PubMedCrossRef
47.
go back to reference Schonewille M, Belmeguenai A, Koekkoek SK, Houtman SH, Boele HJ, van Beugen BJ, et al. Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron. 2010;67:618–28.PubMedCrossRef Schonewille M, Belmeguenai A, Koekkoek SK, Houtman SH, Boele HJ, van Beugen BJ, et al. Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron. 2010;67:618–28.PubMedCrossRef
48.
go back to reference Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J, et al. Small conductance Ca2+-activated k+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci. 2004;24:5301–6.PubMedCrossRef Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J, et al. Small conductance Ca2+-activated k+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci. 2004;24:5301–6.PubMedCrossRef
49.
go back to reference Bond CT, Maylie J, Adelman JP. Sk channels in excitability, pacemaking and synaptic integration. Curr Opin Neurobiol. 2005;15:305–11.PubMedCrossRef Bond CT, Maylie J, Adelman JP. Sk channels in excitability, pacemaking and synaptic integration. Curr Opin Neurobiol. 2005;15:305–11.PubMedCrossRef
50.
go back to reference De Schutter E, Steuber V. Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience. 2009;162:816–26.PubMedCrossRef De Schutter E, Steuber V. Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience. 2009;162:816–26.PubMedCrossRef
51.
go back to reference Destexhe A, Pare D. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol. 1999;81:1531–47.PubMed Destexhe A, Pare D. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol. 1999;81:1531–47.PubMed
52.
go back to reference Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ. Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience. 2001;107:13–24.PubMedCrossRef Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ. Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience. 2001;107:13–24.PubMedCrossRef
53.
go back to reference Alvina K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K. Questioning the role of rebound firing in the cerebellum. Nat Neurosci. 2008;11:1256–8.PubMedCrossRef Alvina K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K. Questioning the role of rebound firing in the cerebellum. Nat Neurosci. 2008;11:1256–8.PubMedCrossRef
54.
go back to reference Tadayonnejad R, Anderson D, Molineux ML, Mehaffey WH, Jayasuriya K, Turner RW. Rebound discharge in deep cerebellar nuclear neurons in vitro. Cerebellum. 2010;9:352–74.PubMedCrossRef Tadayonnejad R, Anderson D, Molineux ML, Mehaffey WH, Jayasuriya K, Turner RW. Rebound discharge in deep cerebellar nuclear neurons in vitro. Cerebellum. 2010;9:352–74.PubMedCrossRef
55.
go back to reference Tadayonnejad R, Mehaffey WH, Anderson D, Turner RW. Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons. Channels (Austin). 2009;3:149–55.CrossRef Tadayonnejad R, Mehaffey WH, Anderson D, Turner RW. Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons. Channels (Austin). 2009;3:149–55.CrossRef
56.
go back to reference Medina JF, Lisberger SG. Encoding and decoding of learned smooth-pursuit eye movements in the floccular complex of the monkey cerebellum. J Neurophysiol. 2009;102:2039–54.PubMedCrossRef Medina JF, Lisberger SG. Encoding and decoding of learned smooth-pursuit eye movements in the floccular complex of the monkey cerebellum. J Neurophysiol. 2009;102:2039–54.PubMedCrossRef
57.
go back to reference Cao Y, Maran SK, Dhamala M, Jaeger D, Heck DH. Behavior-related pauses in simple-spike activity of mouse Purkinje cells are linked to spike rate modulation. J Neurosci. 2012;32:8678–85.PubMedCrossRef Cao Y, Maran SK, Dhamala M, Jaeger D, Heck DH. Behavior-related pauses in simple-spike activity of mouse Purkinje cells are linked to spike rate modulation. J Neurosci. 2012;32:8678–85.PubMedCrossRef
58.
go back to reference Sourdet V, Russier M, Daoudal G, Ankri N, Debanne D. Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci. 2003;23:10238–48.PubMed Sourdet V, Russier M, Daoudal G, Ankri N, Debanne D. Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci. 2003;23:10238–48.PubMed
59.
go back to reference Turrigiano GG, Nelson SB. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol. 2000;10:358–64.PubMedCrossRef Turrigiano GG, Nelson SB. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol. 2000;10:358–64.PubMedCrossRef
60.
61.
go back to reference Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature. 2001;409:88–92.PubMedCrossRef Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature. 2001;409:88–92.PubMedCrossRef
62.
go back to reference Pedroarena C. BK and KV3.1 potassium channels control different aspects of deep cerebellar nuclear neurons action potentials and spiking activity. Cerebellum. 2011;10:647–58.PubMedCrossRef Pedroarena C. BK and KV3.1 potassium channels control different aspects of deep cerebellar nuclear neurons action potentials and spiking activity. Cerebellum. 2011;10:647–58.PubMedCrossRef
64.
go back to reference Eilers J, Konnerth A. Dendritic signal integration [review] [55 refs]. Curr Opin Neurobiol. 1997;7:385–90.PubMedCrossRef Eilers J, Konnerth A. Dendritic signal integration [review] [55 refs]. Curr Opin Neurobiol. 1997;7:385–90.PubMedCrossRef
65.
go back to reference Johnston D, Magee JC, Colbert CM, Christie BR. Active properties of neuronal dendrites. Annu Rev Neurosci. 1996;19:165–86.PubMedCrossRef Johnston D, Magee JC, Colbert CM, Christie BR. Active properties of neuronal dendrites. Annu Rev Neurosci. 1996;19:165–86.PubMedCrossRef
67.
go back to reference Beck H, Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. Nat Rev Neurosci. 2008;9:357–69.PubMedCrossRef Beck H, Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. Nat Rev Neurosci. 2008;9:357–69.PubMedCrossRef
68.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
69.
go back to reference Levin SI, Khaliq ZM, Aman TK, Grieco TM, Kearney JA, Raman IM, et al. Impaired motor function in mice with cell-specific knockout of sodium channel Scn8A (Na(v)1.6) in cerebellar Purkinje neurons and granule cells. J Neurophysiol. 2006;96:785–93.PubMedCrossRef Levin SI, Khaliq ZM, Aman TK, Grieco TM, Kearney JA, Raman IM, et al. Impaired motor function in mice with cell-specific knockout of sodium channel Scn8A (Na(v)1.6) in cerebellar Purkinje neurons and granule cells. J Neurophysiol. 2006;96:785–93.PubMedCrossRef
70.
go back to reference Sausbier M, Hu H, Arntz C, Feil S, Kamm S, Adelsberger H, et al. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated k+ channel deficiency. Proc Natl Acad Sci U S A. 2004;101:9474–8.PubMedCrossRef Sausbier M, Hu H, Arntz C, Feil S, Kamm S, Adelsberger H, et al. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated k+ channel deficiency. Proc Natl Acad Sci U S A. 2004;101:9474–8.PubMedCrossRef
71.
go back to reference Cheron G, Sausbier M, Sausbier U, Neuhuber W, Ruth P, Dan B, Servais L. BK channels control cerebellar purkinje and golgi cell rhythmicity in vivo. Plos One. 2009;4:e7991. Cheron G, Sausbier M, Sausbier U, Neuhuber W, Ruth P, Dan B, Servais L. BK channels control cerebellar purkinje and golgi cell rhythmicity in vivo. Plos One. 2009;4:e7991.
72.
go back to reference Calderon DP, Fremont R, Kraenzlin F, Khodakhah K. The neural substrates of rapid-onset dystonia-parkinsonism. Nat Neurosci. 2011;14:357–65.PubMedCrossRef Calderon DP, Fremont R, Kraenzlin F, Khodakhah K. The neural substrates of rapid-onset dystonia-parkinsonism. Nat Neurosci. 2011;14:357–65.PubMedCrossRef
73.
go back to reference Jinnah HA, Hess EJ, LeDoux MS, Sharma N, Baxter MG, DeLong MR. Rodent models for dystonia research: characteristics, evaluation, and utility. Mov Disord. 2005;20:283–92.PubMedCrossRef Jinnah HA, Hess EJ, LeDoux MS, Sharma N, Baxter MG, DeLong MR. Rodent models for dystonia research: characteristics, evaluation, and utility. Mov Disord. 2005;20:283–92.PubMedCrossRef
74.
go back to reference LeDoux MS, Lorden JF. Abnormal spontaneous and harmaline-stimulated Purkinje cell activity in the awake genetically dystonic rat. Exp Brain Res. 2002;145:457–67.PubMedCrossRef LeDoux MS, Lorden JF. Abnormal spontaneous and harmaline-stimulated Purkinje cell activity in the awake genetically dystonic rat. Exp Brain Res. 2002;145:457–67.PubMedCrossRef
75.
76.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
77.
go back to reference Alvina K, Khodakhah K. The therapeutic mode of action of 4-aminopyridine in cerebellar ataxia. J Neurosci. 2010;30:7258–68.PubMedCrossRef Alvina K, Khodakhah K. The therapeutic mode of action of 4-aminopyridine in cerebellar ataxia. J Neurosci. 2010;30:7258–68.PubMedCrossRef
Metadata
Title
Gain Control of Synaptic Response Function in Cerebellar Nuclear Neurons by a Calcium-Activated Potassium Conductance
Authors
Steven Si Feng
Risa Lin
Volker Gauck
Dieter Jaeger
Publication date
01-10-2013
Publisher
Springer US
Published in
The Cerebellum / Issue 5/2013
Print ISSN: 1473-4222
Electronic ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-013-0476-9

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