Computational Analysis of Action Potential Initiation in Mitral Cell Soma and Dendrites Based on Dual Patch Recordings

1999 ◽  
Vol 82 (6) ◽  
pp. 3006-3020 ◽  
Author(s):  
Gongyu Y. Shen ◽  
Wei R. Chen ◽  
Jens Midtgaard ◽  
Gordon M. Shepherd ◽  
Michael L. Hines
Keyword(s):  
Action Potential ◽  
Sodium Channel ◽  
Primary Dendrite ◽  
Mitral Cell ◽  
Voltage Gradient ◽  
Dendritic Region ◽  
Channel Density ◽  
Site Of Action ◽  
Action Potential Initiation ◽  
Potential Initiation

In olfactory mitral cells, dual patch recordings show that the site of action potential initiation can shift between soma and distal primary dendrite and that the shift is dependent on the location and strength of electrode current injection. We have analyzed the mechanisms underlying this shift, using a model of the mitral cell that takes advantage of the constraints available from the two recording sites. Starting with homogeneous Hodgkin-Huxley-like Na+-K+ channel distribution in the soma-dendritic region and much higher sodium channel density in the axonal region, the model's channel kinetics and density were adjusted by a fitting algorithm so that the model response was virtually identical to the experimental data. The combination of loading effects and much higher sodium channel density in the axon relative to the soma-dendritic region results in significantly lower “voltage threshold” for action potential initiation in the axon; the axon therefore fires first unless the voltage gradient in the primary dendrite is steep enough for it to reach its higher threshold. The results thus provide a quantitative explanation for the stimulus strength and position dependence of the site of action potential initiation in the mitral cell.

Multiple Modes of Action Potential Initiation and Propagation in Mitral Cell Primary Dendrite

2002 ◽  
Vol 88 (5) ◽  
pp. 2755-2764 ◽  
Author(s):  
Wei R. Chen ◽  
Gongyu Y. Shen ◽  
Gordon M. Shepherd ◽  
Michael L. Hines ◽  
Jens Midtgaard
Keyword(s):  
Action Potential ◽  
Primary Dendrite ◽  
Back Propagation ◽  
Olfactory Nerve ◽  
Mitral Cell ◽  
Initiation Site ◽  
Initiation And Propagation ◽  
Action Potential Initiation ◽  
Dendritic Spike ◽  
Spike Initiation

The mitral cell primary dendrite plays an important role in transmitting distal olfactory nerve input from olfactory glomerulus to the soma-axon initial segment. To understand how dendritic active properties are involved in this transmission, we have combined dual soma and dendritic patch recordings with computational modeling to analyze action-potential initiation and propagation in the primary dendrite. In response to depolarizing current injection or distal olfactory nerve input, fast Na+ action potentials were recorded along the entire length of the primary dendritic trunk. With weak-to-moderate olfactory nerve input, an action potential was initiated near the soma and then back-propagated into the primary dendrite. As olfactory nerve input increased, the initiation site suddenly shifted to the distal primary dendrite. Multi-compartmental modeling indicated that this abrupt shift of the spike-initiation site reflected an independent thresholding mechanism in the distal dendrite. When strong olfactory nerve excitation was paired with strong inhibition to the mitral cell basal secondary dendrites, a small fast prepotential was recorded at the soma, which indicated that an action potential was initiated in the distal primary dendrite but failed to propagate to the soma. As the inhibition became weaker, a “double-spike” was often observed at the dendritic recording site, corresponding to a single action potential at the soma. Simulation demonstrated that, in the course of forward propagation of the first dendritic spike, the action potential suddenly jumps from the middle of the dendrite to the axonal spike-initiation site, leaving the proximal part of primary dendrite unexcited by this initial dendritic spike. As Na+conductances in the proximal dendrite are not activated, they become available to support the back-propagation of the evoked somatic action potential to produce the second dendritic spike. In summary, the balance of spatially distributed excitatory and inhibitory inputs can dynamically switch the mitral cell firing among four different modes: axo-somatic initiation with back-propagation, dendritic initiation either with no forward propagation, forward propagation alone, or forward propagation followed by back-propagation.

scholarly journals Modeling Action Potential Initiation and Back-Propagation in Dendrites of Cultured Rat Motoneurons

1998 ◽  
Vol 80 (2) ◽  
pp. 715-729 ◽  
Author(s):  
Hans-R. Lüscher ◽  
Matthew E. Larkum
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Initial Segment ◽  
Back Propagation ◽  
Channel Density ◽  
Axon Hillock ◽  
Dendritic Membrane ◽  
Action Potential Initiation ◽  
Spike Initiation ◽  
Potential Initiation

Lüscher, Hans-R. and Matthew E. Larkum. Modeling action potential initiation and back-propagation in dendrites of cultured rat motoneurons. J. Neurophysiol. 80: 715–729, 1998. Regardless of the site of current injection, action potentials usually originate at or near the soma and propagate decrementally back into the dendrites. This phenomenon has been observed in neocortical pyramidal cells as well as in cultured motoneurons. Here we show that action potentials in motoneurons can be initiated in the dendrite as well, resulting in a biphasic dendritic action potential. We present a model of spinal motoneurons that is consistent with observed physiological properties of spike initiation in the initial segment/axon hillock region and action potential back-propagation into the dendritic tree. It accurately reproduces the results presented by Larkum et al. on motoneurons in organotypic rat spinal cord slice cultures. A high Na+-channel density of ḡ Na = 700 mS/cm2 at the axon hillock/initial segment region was required to secure antidromic invasion of the somato-dendritic membrane, whereas for the orthodromic direction, a Na+-channel density of ḡ Na = 1,200 mS/cm2 was required. A “weakly” excitable ( ḡ Na = 3 mS/cm2) dendritic membrane most accurately describes the experimentally observed attenuation of the back-propagated action potential. Careful analysis of the threshold conditions for action potential initiation at the initial segment or the dendrites revealed that, despite the lower voltage threshold for spike initiation in the initial segment, an action potential can be initiated in the dendrite before the initial segment fires a spike. Spike initiation in the dendrite depends on the passive cable properties of the dendritic membrane, its Na+-channel density, and local structural properties, mainly the diameter of the dendrites. Action potentials are initiated more easily in distal than in proximal dendrites. Whether or not such a dendritic action potential invades the soma with a subsequent initiation of a second action potential in the initial segment depends on the actual current source-load relation between the action potential approaching the soma and the electrical load of the soma together with the attached dendrites.

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