 |
The Journal of Neuroscience, January 12, 2005, 25(2):454-463; doi:10.1523/JNEUROSCI.3045-04.2005
 Previous Article | Next Article 
Cellular/Molecular
Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons
Zayd M. Khaliq1 and
Indira M. Raman1,2
1Institute for Neuroscience and 2Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois 60208
In cerebellar Purkinje neurons, the reliability of propagation of high-frequency simple spikes and spikelets of complex spikes is likely to regulate inhibition of Purkinje target neurons. To test the extent to which a one-to-one correspondence exists between somatic and axonal spikes, we made dual somatic and axonal recordings from Purkinje neurons in mouse cerebellar slices. Somatic action potentials were recorded with a whole-cell pipette, and the corresponding axonal signals were recorded extracellularly with a loose-patch pipette. Propagation of spontaneous and evoked simple spikes was highly reliable. At somatic firing rates of  200 spikes/sec, <10% of spikes failed to propagate, with failures becoming more frequent only at maximal somatic firing rates (260 spikes/sec). Complex spikes were elicited by climbing fiber stimulation, and their somatic waveforms were modulated by tonic current injection, as well as by paired stimulation to depress the underlying EPSCs. Across conditions, the mean number of propagating action potentials remained just above two spikes per climbing fiber stimulation, but the instantaneous frequency of the propagating spikes changed, from 375 Hz during somatic hyperpolarizations that silenced spontaneous firing to 150 Hz during spontaneous activity. The probability of propagation of individual spikelets could be described quantitatively as a saturating function of spikelet amplitude, rate of rise, or preceding interspike interval. The results suggest that ion channels of Purkinje axons are adapted to produce extremely short refractory periods and that brief bursts of forward-propagating action potentials generated by complex spikes may contribute transiently to inhibition of postsynaptic neurons.
Key words: climbing fiber; deep cerebellar nuclei; floccular target neurons; Na channel; internode; action potential burst
Received July 26, 2004;
revised November 4, 2004;
accepted November 8, 2004.
This article has been cited by other articles:
|
|
|
|
 
S. P. Marshall and E. J. Lang
Local Changes in the Excitability of the Cerebellar Cortex Produce Spatially Restricted Changes in Complex Spike Synchrony
J. Neurosci.,
November 11, 2009;
29(45):
14352 - 14362.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Zheng and I. M. Raman
Ca Currents Activated by Spontaneous Firing and Synaptic Disinhibition in Neurons of the Cerebellar Nuclei
J. Neurosci.,
August 5, 2009;
29(31):
9826 - 9838.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Bradley, R. Luo, T. S. Otis, and D. A. DiGregorio
Submillisecond Optical Reporting of Membrane Potential In Situ Using a Neuronal Tracer Dye
J. Neurosci.,
July 22, 2009;
29(29):
9197 - 9209.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. F. Atherton, D. L. Wokosin, S. Ramanathan, and M. D. Bevan
Autonomous initiation and propagation of action potentials in neurons of the subthalamic nucleus
J. Physiol.,
December 1, 2008;
586(23):
5679 - 5700.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. T. Roberts, K. J. Bender, and L. O. Trussell
Fidelity of Complex Spike-Mediated Synaptic Transmission between Inhibitory Interneurons
J. Neurosci.,
September 17, 2008;
28(38):
9440 - 9450.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. T. Davie, B. A. Clark, and M. Hausser
The Origin of the Complex Spike in Cerebellar Purkinje Cells
J. Neurosci.,
July 23, 2008;
28(30):
7599 - 7609.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. J. Kress, M. J. Dowling, J. P. Meeks, and S. Mennerick
High Threshold, Proximal Initiation, and Slow Conduction Velocity of Action Potentials in Dentate Granule Neuron Mossy Fibers
J Neurophysiol,
July 1, 2008;
100(1):
281 - 291.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. C. Hurlock, A. McMahon, and R. H. Joho
Purkinje-Cell-Restricted Restoration of Kv3.3 Function Restores Complex Spikes and Rescues Motor Coordination in Kcnc3 Mutants
J. Neurosci.,
April 30, 2008;
28(18):
4640 - 4648.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. J. Sjostrom, E. A. Rancz, A. Roth, and M. Hausser
Dendritic Excitability and Synaptic Plasticity
Physiol Rev,
April 1, 2008;
88(2):
769 - 840.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Maruta, R. A. Hensbroek, and J. I. Simpson
Intraburst and Interburst Signaling by Climbing Fibers
J. Neurosci.,
October 17, 2007;
27(42):
11263 - 11270.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Piochon, T. Irinopoulou, D. Brusciano, Y. Bailly, J. Mariani, and C. Levenes
NMDA Receptor Contribution to the Climbing Fiber Response in the Adult Mouse Purkinje Cell
J. Neurosci.,
October 3, 2007;
27(40):
10797 - 10809.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. L. Scott, T. A. Hage, and N. L. Golding
Weak action potential backpropagation is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive
J. Physiol.,
September 1, 2007;
583(2):
647 - 661.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. D. Brenowitz and W. G. Regehr
Reliability and Heterogeneity of Calcium Signaling at Single Presynaptic Boutons of Cerebellar Granule Cells
J. Neurosci.,
July 25, 2007;
27(30):
7888 - 7898.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. F. Medina and S. G. Lisberger
Variation, Signal, and Noise in Cerebellar Sensory-Motor Processing for Smooth-Pursuit Eye Movements
J. Neurosci.,
June 20, 2007;
27(25):
6832 - 6842.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. P. Meeks and S. Mennerick
Action Potential Initiation and Propagation in CA3 Pyramidal Axons
J Neurophysiol,
May 1, 2007;
97(5):
3460 - 3472.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kim and L. O. Trussell
Ion Channels Generating Complex Spikes in Cartwheel Cells of the Dorsal Cochlear Nucleus
J Neurophysiol,
February 1, 2007;
97(2):
1705 - 1725.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Martina, A. E. Metz, and B. P. Bean
Voltage-Dependent Potassium Currents During Fast Spikes of Rat Cerebellar Purkinje Neurons: Inhibition by BDS-I Toxin
J Neurophysiol,
January 1, 2007;
97(1):
563 - 571.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. I. Levin, Z. M. Khaliq, T. K. Aman, T. M. Grieco, J. A. Kearney, I. M. Raman, and M. H. Meisler
Impaired Motor Function in Mice With Cell-Specific Knockout of Sodium Channel Scn8a (NaV1.6) in Cerebellar Purkinje Neurons and Granule Cells
J Neurophysiol,
August 1, 2006;
96(2):
785 - 793.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Carta, M. Mameli, and C. F. Valenzuela
Alcohol Potently Modulates Climbing Fiber->Purkinje Neuron Synapses: Role of Metabotropic Glutamate Receptors
J. Neurosci.,
February 15, 2006;
26(7):
1906 - 1912.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. M. Khaliq and I. M. Raman
Relative Contributions of Axonal and Somatic Na Channels to Action Potential Initiation in Cerebellar Purkinje Neurons
J. Neurosci.,
February 15, 2006;
26(7):
1935 - 1944.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. E McKay and R. W Turner
Physiological and morphological development of the rat cerebellar Purkinje cell
J. Physiol.,
September 15, 2005;
567(3):
829 - 850.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. P Meeks, X. Jiang, and S. Mennerick
Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus
J. Physiol.,
July 15, 2005;
566(2):
425 - 441.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. C. Gravielle, R. Faris, S. J. Russek, and D. H. Farb
GABA Induces Activity Dependent Delayed-onset Uncoupling of GABA/Benzodiazepine Site Interactions in Neocortical Neurons
J. Biol. Chem.,
June 3, 2005;
280(22):
20954 - 20960.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
