 |
Previous Article | Next Article 
The Journal of Neuroscience, February 1, 2001, 21(3):759-770
Theta-Frequency Bursting and Resonance in Cerebellar Granule
Cells: Experimental Evidence and Modeling of a Slow
K+-Dependent Mechanism
Egidio
D'Angelo1, 2,
Thierry
Nieus1,
Arianna
Maffei1,
Simona
Armano1,
Paola
Rossi1,
Vanni
Taglietti1,
Andrea
Fontana3, and
Giovanni
Naldi4
1 Department of Molecular/Cellular Physiology and
Instituto Nazionale per la Fisica della Materia, University of
Pavia, I-27100 Pavia, Italy, 2 Department of
Evolutionary and Functional Biology, University of Parma, Parma, Italy,
3 Department of Nuclear and Theoretical Physics,
University of Pavia, Pavia, Italy, and
4 Department of Mathematics and Applications,
University of Milano Bicocca, Milan, Italy
Neurons process information in a highly nonlinear manner,
generating oscillations, bursting, and resonance, enhancing
responsiveness at preferential frequencies. It has been proposed that
slow repolarizing currents could be responsible for both
oscillation/burst termination and for high-pass filtering that causes
resonance (Hutcheon and Yarom, 2000). However, different mechanisms,
including electrotonic effects (Mainen and Sejinowski, 1996),
the expression of resurgent currents (Raman and Bean, 1997), and
network feedback, may also be important. In this study we report
theta-frequency (3-12 Hz) bursting and resonance in rat cerebellar
granule cells and show that these neurons express a previously
unidentified slow repolarizing K+ current
(IK-slow). Our experimental and
modeling results indicate that IK-slow was
necessary for both bursting and resonance. A persistent (and
potentially a resurgent) Na+ current exerted complex
amplifying actions on bursting and resonance, whereas electrotonic
effects were excluded by the compact structure of the granule cell.
Theta-frequency bursting and resonance in granule cells may play an
important role in determining synchronization, rhythmicity, and
learning in the cerebellum.
Key words:
bursting; resonance; M-current; cerebellum; granule cell; modeling
Copyright © 2001 Society for Neuroscience 0270-6474/01/213759-12$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
S. Chintawar, R. Hourez, A. Ravella, D. Gall, D. Orduz, M. Rai, D. P. Bishop, S. Geuna, S. N. Schiffmann, and M. Pandolfo
Grafting Neural Precursor Cells Promotes Functional Recovery in an SCA1 Mouse Model
J. Neurosci.,
October 21, 2009;
29(42):
13126 - 13135.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Mapelli, P. Rossi, T. Nieus, and E. D'Angelo
Tonic Activation of GABAB Receptors Reduces Release Probability at Inhibitory Connections in the Cerebellar Glomerulus
J Neurophysiol,
June 1, 2009;
101(6):
3089 - 3099.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Tohidi and F. Nadim
Membrane Resonance in Bursting Pacemaker Neurons of an Oscillatory Network Is Correlated with Network Frequency
J. Neurosci.,
May 20, 2009;
29(20):
6427 - 6435.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Diwakar, J. Magistretti, M. Goldfarb, G. Naldi, and E. D'Angelo
Axonal Na+ Channels Ensure Fast Spike Activation and Back-Propagation in Cerebellar Granule Cells
J Neurophysiol,
February 1, 2009;
101(2):
519 - 532.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. N. Mercer, C. S. Chan, T. Tkatch, J. Held, and D. J. Surmeier
Nav1.6 Sodium Channels Are Critical to Pacemaking and Fast Spiking in Globus Pallidus Neurons
J. Neurosci.,
December 5, 2007;
27(49):
13552 - 13566.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. G. Brickley, M. I. Aller, C. Sandu, E. L. Veale, F. G. Alder, H. Sambi, A. Mathie, and W. Wisden
TASK-3 Two-Pore Domain Potassium Channels Enable Sustained High-Frequency Firing in Cerebellar Granule Neurons
J. Neurosci.,
August 29, 2007;
27(35):
9329 - 9340.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Diana, Y. Otsu, G. Maton, T. Collin, M. Chat, and S. Dieudonne
T-Type and L-Type Ca2+ Conductances Define and Encode the Bimodal Firing Pattern of Vestibulocerebellar Unipolar Brush Cells
J. Neurosci.,
April 4, 2007;
27(14):
3823 - 3838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Castro-Alamancos, P. Rigas, and Y. Tawara-Hirata
Resonance (~10 Hz) of excitatory networks in motor cortex: effects of voltage-dependent ion channel blockers
J. Physiol.,
January 1, 2007;
578(1):
173 - 191.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Forti, E. Cesana, J. Mapelli, and E. D'Angelo
Ionic mechanisms of autorhythmic firing in rat cerebellar Golgi cells
J. Physiol.,
August 1, 2006;
574(3):
711 - 729.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. M. de Ruiter, C. I. De Zeeuw, and C. Hansel
Voltage-Gated Sodium Channels in Cerebellar Purkinje Cells of Mormyrid Fish
J Neurophysiol,
July 1, 2006;
96(1):
378 - 390.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Magistretti, L. Castelli, L. Forti, and E. D'Angelo
Kinetic and functional analysis of transient, persistent and resurgent sodium currents in rat cerebellar granule cells in situ: an electrophysiological and modelling study
J. Physiol.,
May 15, 2006;
573(1):
83 - 106.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Nieus, E. Sola, J. Mapelli, E. Saftenku, P. Rossi, and E. D'Angelo
LTP Regulates Burst Initiation and Frequency at Mossy Fiber-Granule Cell Synapses of Rat Cerebellum: Experimental Observations and Theoretical Predictions
J Neurophysiol,
February 1, 2006;
95(2):
686 - 699.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Osorio, G. Alcaraz, F. Padilla, F. Couraud, P. Delmas, and M. Crest
Differential targeting and functional specialization of sodium channels in cultured cerebellar granule cells
J. Physiol.,
December 15, 2005;
569(3):
801 - 816.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. R. Percaccio, N. D. Engineer, A. L. Pruette, P. K. Pandya, R. Moucha, D. L. Rathbun, and M. P. Kilgard
Environmental Enrichment Increases Paired-Pulse Depression in Rat Auditory Cortex
J Neurophysiol,
November 1, 2005;
94(5):
3590 - 3600.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Gall, F. Prestori, E. Sola, A. D'Errico, C. Roussel, L. Forti, P. Rossi, and E. D'Angelo
Intracellular Calcium Regulation by Burst Discharge Determines Bidirectional Long-Term Synaptic Plasticity at the Cerebellum Input Stage
J. Neurosci.,
May 11, 2005;
25(19):
4813 - 4822.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Sharifullina, K. Ostroumov, and A. Nistri
Metabotropic glutamate receptor activity induces a novel oscillatory pattern in neonatal rat hypoglossal motoneurones
J. Physiol.,
February 15, 2005;
563(1):
139 - 159.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. F. Cooke, P. J. E. Attwell, and C. H. Yeo
Temporal Properties of Cerebellar-Dependent Memory Consolidation
J. Neurosci.,
March 24, 2004;
24(12):
2934 - 2941.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. M. Grieco and I. M. Raman
Production of Resurgent Current in NaV1.6-Null Purkinje Neurons by Slowing Sodium Channel Inactivation with {beta}-Pompilidotoxin
J. Neurosci.,
January 7, 2004;
24(1):
35 - 42.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Gall, C. Roussel, I. Susa, E. D'Angelo, P. Rossi, B. Bearzatto, M. C. Galas, D. Blum, S. Schurmans, and S. N. Schiffmann
Altered Neuronal Excitability in Cerebellar Granule Cells of Mice Lacking Calretinin
J. Neurosci.,
October 15, 2003;
23(28):
9320 - 9327.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. M. Khaliq, N. W. Gouwens, and I. M. Raman
The Contribution of Resurgent Sodium Current to High-Frequency Firing in Purkinje Neurons: An Experimental and Modeling Study
J. Neurosci.,
June 15, 2003;
23(12):
4899 - 4912.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Hu, K. Vervaeke, and J. F Storm
Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells
J. Physiol.,
December 15, 2002;
545(3):
783 - 805.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. M. Grieco, F. S. Afshari, and I. M. Raman
A Role for Phosphorylation in the Maintenance of Resurgent Sodium Current in Cerebellar Purkinje Neurons
J. Neurosci.,
April 15, 2002;
22(8):
3100 - 3107.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|