Action Potential Initiation and Propagation in CA3 Pyramidal Axons

2007 ◽  
Vol 97 (5) ◽  
pp. 3460-3472 ◽  
Author(s):  
Julian P. Meeks ◽  
Steven Mennerick

Thin, unmyelinated axons densely populate the mammalian hippocampus and cortex. However, the location and dynamics of spike initiation in thin axons remain unclear. We investigated basic properties of spike initiation and propagation in CA3 neurons of juvenile rat hippocampus. Sodium channel alpha subunit distribution and local applications of tetrodotoxin demonstrate that the site of first threshold crossing in CA3 neurons is ∼35 μm distal to the soma, somewhat more proximal than our previous estimates. This discrepancy can be explained by the finding, obtained with simultaneous whole cell somatic and extracellular axonal recordings, that a zone of axon stretching to ∼100 μm distal to the soma reaches a maximum rate of depolarization nearly synchronously by the influx of sodium from the high-density channels. Models of the proximal axon incorporating observed distributions of sodium channel staining recapitulated salient features of somatic and axonal spike waveforms, including the predicted initiation zone, characteristic spike latencies, and conduction velocity. The preferred initiation zone was unaltered by stimulus strength or repetitive spiking, but repetitive spiking increased threshold and significantly slowed initial segment recruitment time and conduction velocity. Our work defines the dynamics of initiation and propagation in hippocampal principal cell axons and may help reconcile recent controversies over initiation site in other axons.

2002 ◽  
Vol 88 (5) ◽  
pp. 2755-2764 ◽  
Author(s):  
Wei R. Chen ◽  
Gongyu Y. Shen ◽  
Gordon M. Shepherd ◽  
Michael L. Hines ◽  
Jens Midtgaard

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.


1986 ◽  
Vol 60 (4) ◽  
pp. 1107-1115 ◽  
Author(s):  
P. Grigg

Mechanoreception can be viewed as a series of sequential mechanical and ionic processes that take place in mechanosensitive end organs and in the terminals of the nerves that innervate them. Stimuli act on a transducer after being transmitted through some material having a combination of elastic and viscoelastic properties. Channels that open under membrane loading have recently been described in muscle cells and are presented as a model for transduction. When open these channels are cation specific. Ions passing through transducer channels depolarize a spike-initiating zone on the cell. These currents may also activate other conductances in the cell, so that the total generator current may have many components. In many mechanoreceptors, action potential initiation results in activation of an electrogenic Na+ pump at the spike-initiation zone, which modifies the threshold for subsequent action potentials. Action potentials initiated in the many branches of a single sensory axon interact at the branching point of the axon. The rules governing this interaction are complex. The above factors, together or separately, are responsible for the dynamic responses and adaptation observed in mechanoreceptors.


1980 ◽  
Vol 86 (1) ◽  
pp. 49-61
Author(s):  
G. F. GWILLIAM ◽  
M. BURROWS

1. The electrical properties of the membrane of an identified locust motor neurone, the fast extensor tibiae in the metathoracic ganglion, have been investigated to determine: the distribution of excitable and inexcitable membrane; the impulse initiation zone; and the conduction velocity of the spike in the ganglion and in the axon. 2. The waveform of extracellularly recorded spikes indicates that the transition from inactive to active membrane occurs along the region of the neurite which bears many arborizations within the neuropile. 3. Measurements of the delay between orthodromically or antidromically evoked spikes, recorded at the soma and other points along the neurite, place the impulse initiating zone close to the transition between active and inactive membrane. 4. Within the ganglion, the spike is conducted at different velocities over different parts of the neurite. The average velocity within the ganglion is, however, only about a seventh of that in the axon (0.54 m.s−1 against 4.1 m.s−1).


2019 ◽  
Vol 122 (6) ◽  
pp. 2576-2590
Author(s):  
Susan T. Lubejko ◽  
Bertrand Fontaine ◽  
Sara E. Soueidan ◽  
Katrina M. MacLeod

Single neurons function along a spectrum of neuronal operating modes whose properties determine how the output firing activity is generated from synaptic input. The auditory brain stem contains a diversity of neurons, from pure coincidence detectors to pure integrators and those with intermediate properties. We investigated how intrinsic spike initiation mechanisms regulate neuronal operating mode in the avian cochlear nucleus. Although the neurons in one division of the avian cochlear nucleus, nucleus magnocellularis, have been studied in depth, the spike threshold dynamics of the tonically firing neurons of a second division of cochlear nucleus, nucleus angularis (NA), remained unexplained. The input-output functions of tonically firing NA neurons were interrogated with directly injected in vivo-like current stimuli during whole cell patch-clamp recordings in vitro. Increasing the amplitude of the noise fluctuations in the current stimulus enhanced the firing rates in one subset of tonically firing neurons (“differentiators”) but not another (“integrators”). We found that spike thresholds showed significantly greater adaptation and variability in the differentiator neurons. A leaky integrate-and-fire neuronal model with an adaptive spike initiation process derived from sodium channel dynamics was fit to the firing responses and could recapitulate >80% of the precise temporal firing across a range of fluctuation and mean current levels. Greater threshold adaptation explained the frequency-current curve changes due to a hyperpolarized shift in the effective adaptation voltage range and longer-lasting threshold adaptation in differentiators. The fine-tuning of the intrinsic properties of different NA neurons suggests they may have specialized roles in spectrotemporal processing. NEW & NOTEWORTHY Avian cochlear nucleus angularis (NA) neurons are responsible for encoding sound intensity for sound localization and spectrotemporal processing. An adaptive spike threshold mechanism fine-tunes a subset of repetitive-spiking neurons in NA to confer coincidence detector-like properties. A model based on sodium channel inactivation properties reproduced the activity via a hyperpolarized shift in adaptation conferring fluctuation sensitivity.


Neuron ◽  
2019 ◽  
Vol 102 (4) ◽  
pp. 801-812.e5 ◽  
Author(s):  
Robert H. Goldstein ◽  
Omer Barkai ◽  
Almudena Íñigo-Portugués ◽  
Ben Katz ◽  
Shaya Lev ◽  
...  

As predicted by Hodgkin (1975), calculation of conduction velocities in squid giant axons shows that if each sodium channel is gated by charged particles moving in the membrane field there will be a maximum in the relation between sodium conductance and conduction velocity.


2008 ◽  
Vol 586 (7) ◽  
pp. 1849-1857 ◽  
Author(s):  
Christoph Schmidt-Hieber ◽  
Peter Jonas ◽  
Josef Bischofberger

2002 ◽  
Vol 87 (3) ◽  
pp. 1572-1585 ◽  
Author(s):  
Mark A. Masino ◽  
Ronald L. Calabrese

Motor pattern generating networks that produce segmentally distributed motor outflow are often portrayed as a series of coupled segmental oscillators that produce a regular progression (constant phase differences) in their rhythmic activity. The leech heartbeat central pattern generator is paced by a core timing network, which consists of two coupled segmental oscillators in segmental ganglia 3 and 4. The segmental oscillators comprise paired mutually inhibitory oscillator interneurons and the processes of intersegmental coordinating interneurons. As a first step in understanding the coordination of segmental motor outflow by this pattern generator, we describe the functional synaptic interactions, and activity and phase relationships of the heart interneurons of the timing network, in isolated nerve cord preparations. In the timing network, most (∼75%) of the coordinating interneuron action potentials were generated at a primary spike initiation site located in ganglion 4 (G4). A secondary spike initiation site in ganglion 3 (G3) became active in the absence of activity at the primary site. Generally, the secondary site was characterized by a reluctance to burst and a lower spike frequency, when compared with the primary site. Oscillator interneurons in G3 inhibited spike activity at both initiation sites, whereas oscillator interneurons in G4 inhibited spike activity only at the primary initiation site. This asymmetry in the control of spike activity in the coordinating interneurons may account for the observation that the phase of the coordinating interneurons is more tightly linked to the G3 than G4 oscillator interneurons. The cycle period of the timing network and the phase difference between the ipsilateral G3 and G4 oscillator interneurons were regular within individual preparations, but varied among preparations. This variation in phase differences observed across preparations implies that modulated intrinsic membrane and synaptic properties, rather than the pattern of synaptic connections, are instrumental in determining phase within the timing network.


Sign in / Sign up

Export Citation Format

Share Document