Multiple Sites of Spike Initiation in a Bifurcating Locust Neurone

1978 ◽  
Vol 76 (1) ◽  
pp. 63-84 ◽  
Author(s):  
W. J. HEITLER ◽  
COREY S. GOODMAN
Keyword(s):  
Action Potential ◽  
Branch Point ◽  
Peripheral Nerves ◽  
Action Potentials ◽  
Room Temperature ◽  
Initiation Site ◽  
Left And Right ◽  
Axon Branch ◽  
Spike Initiation ◽  
Dorsal Unpaired Median

Recordings were made from the metathoracic dorsal unpaired median neurone to the extensor tibiae muscle (DUMETi) in the locust. This is a bifurcating neurone with axons exiting both sideS of the ganglion, whose soma can support a full action potential. Four different spike types were recorded in the soma, each of which we associate with a different region of the neurone. These were (1) a soma (S) spike of 70-90 mV, (2) a neurite (N) spike of 20-40 mV, occurring between the axon hillock and axon branch point, (3) and (4) axon (A) spikes of 8–15 mV, occurring distal to the branch point on the left and right axons. Each of these regions must therefore have its own spike initiation site. At spike frequencies greater than about 10 Hz at room temperature or 1-5 Hz at 32 °C (the preferred environmental temperature of the locust) the S-spike may fail, revealing A-spikes, or more rarely N-spikes. A-spikes usually consist of two more-or-less separate components, Al and Ar, which can be correlated with action potentials in the left and right axon branches by recording spikes extracellularly in the peripheral nerves on each side. Occasionally single component A-spikes occur when an action potential is initiated in only one axon, and fails to propagate across the branch point to the contralateral axon. Thus, action potentials may occur independently in the branches of this bifurcating neurone. After unilateral axotomy only S-spikes and N-spikes are recorded, indicating that action potentials no longer fail to propagate across the branch point. Anatomical asymmetries in the axon branches of DUMETi have been correlated with physiological asymmetries recorded in the soma of the same neurone.

scholarly journals Action Potential Reflection and Failure at Axon Branch Points Cause Stepwise Changes in EPSPs in a Neuron Essential for Learning

2000 ◽  
Vol 83 (3) ◽  
pp. 1693-1700 ◽  
Author(s):  
Stephen A. Baccus ◽  
Brian D. Burrell ◽  
Christie L. Sahley ◽  
Kenneth J. Muller
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Conduction Block ◽  
Neuronal Morphology ◽  
Whole Body ◽  
Reverse Direction ◽  
Mammalian Brain ◽  
Branch Points ◽  
Individual Branch ◽  
Axon Branch

In leech mechanosensory neurons, action potentials reverse direction, or reflect, at central branch points. This process enhances synaptic transmission from individual axon branches by rapidly activating synapses twice, thereby producing facilitation. At the same branch points action potentials may fail to propagate, which can reduce transmission. It is now shown that presynaptic action potential reflection and failure under physiological conditions influence transmission to the same postsynaptic neuron, the S cell. The S cell is an interneuron essential for a form of nonassociative learning, sensitization of the whole body shortening reflex. The P to S synapse has components that appear monosynaptic (termed “direct”) and polysynaptic, both with glutamatergic pharmacology. Reflection at P cell branch points on average doubled transmission to the S cell, whereas action potential failure, or conduction block, at the same branch points decreased it by one-half. Each of two different branch points affected transmission, indicating that the P to S connection is spatially distributed around these branch points. This was confirmed by examining the locations of individual contacts made by the P cell with the S cell and its electrically coupled partner C cells. These results show that presynaptic neuronal morphology produces a range of transmission states at a set of synapses onto a neuron necessary for a form of learning. Reflection and conduction block are activity-dependent and are basic properties of action potential propagation that have been seen in other systems, including axons and dendrites in the mammalian brain. Individual branch points and the distribution of synapses around those branch points can substantially influence neuronal transmission and plasticity.

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.

Axon terminal hyperexcitability associated with epileptogenesis in vitro. I. Origin of ectopic spikes

1993 ◽  
Vol 70 (3) ◽  
pp. 961-975 ◽  
Author(s):  
S. F. Stasheff ◽  
M. Hines ◽  
W. A. Wilson
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Model Neuron ◽  
Extracellular Recording ◽  
Pyramidal Cells ◽  
Initiation Site ◽  
Electrographic Seizures ◽  
Ca3 Pyramidal Cells

1. Intracellular and extracellular recording techniques were used to study the increase in ectopic (i.e., nonsomatic) action-potential generation occurring among CA3 pyramidal cells during the kindling-like induction of electrographic seizures (EGSs) in this subpopulation of the hippocampal slice. Kindling-like stimulus trains (60 Hz, 2 s) were delivered to s. radiatum of CA3 at 10-min intervals. As EGSs developed, the frequency of ectopic firing increased markedly (by 10.33 +/- 3.29 spikes/min, mean +/- SE, P << 0.01). Several methods were applied to determine the initiation site for these action potentials within the cell (axons vs. dendrites). 2. Collision tests were conducted between known antidromic and orthodromic action potentials in CA3 cells to determine the critical period, c, for collision. Attempts were then made to collide ectopic spikes with known antidromic action potentials. At intervals less than c, ectopic spikes failed to collide with antidromic ones, in 5 of 10 cases. In these cells, this clearly indicates that the ectopic spikes were themselves of axonal origin. In the remaining five cases, ectopic spikes collided with antidromic action potentials at intervals approximately equal to c, most likely because of interactions within the complex system of recurrent axon collaterals in CA3. 3. Action potentials of CA3 pyramidal cells were simulated with the use of a compartmental computer model, NEURON. These simulations were based on prior models of CA3 pyramidal neurons and of the motoneuron action potential. Simulated action potentials generated in axonal compartments possessed a prominent inflection on their rising phase (IS-SD break), which was difficult to appreciate in those spikes generated in somatic or dendritic compartments. 4. An analysis of action potentials recorded experimentally from CA3 pyramidal cells also showed that antidromic spikes possess a prominent IS-SD break that is not present in orthodromic spikes. In addition to identified antidromic action potentials, ectopic spikes also possess such an inflection. Together with the predictions of computer simulations, this analysis also indicates that ectopic spikes originate in the axons of CA3 cells. 5. Tetrodotoxin (TTX, 50 microM) was locally applied by pressure injection while monitoring ectopic spike activity. Localized application of TTX to regions of the slice that could include the axons but not the dendrites of recorded cells abolished or markedly reduced the frequency of ectopic spikes (n = 5), further confirming the hypothesis that these action potentials arise from CA3 axons.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Contribution of the axon initial segment to action potentials recorded extracellularly

2018 ◽  
Author(s):  
Maria Teleńczuk ◽  
Romain Brette ◽  
Alain Destexhe ◽  
Bartosz Teleńczuk
Keyword(s):  
Action Potential ◽  
Electric Fields ◽  
Action Potentials ◽  
Initial Segment ◽  
Initiation Site ◽  
Axon Initial Segment ◽  
Neuron Activity ◽  
Classical Models ◽  
The Brain

AbstractAction potentials (APs) are electric phenomena that are recorded both intracellularly and extracellularly. APs are usually initiated in the short segment of the axon called the axon initial segment (AIS). It was recently proposed that at onset of an AP the soma and the AIS form a dipole. We study the extracellular signature (the extracellular action potential, EAP) generated by such a dipole. First, we demonstrate the formation of the dipole and its extracellular signature in detailed morphological models of a reconstructed pyramidal neuron. Then, we study the EAP waveform and its spatial dependence in models with axonal AP initiation and contrast it with the EAP obtained in models with somatic AP initiation. We show that in the models with axonal AP initiation the dipole forms between somatodendritic compartments and the AIS, and not between soma and dendrites as in the classical models. Soma-dendrites dipole is present only in models with somatic AP initiation. Our study has consequences for interpreting extracellular recordings of single-neuron activity and determining electrophysiological neuron types, but also for better understanding the origins of the high-frequency macroscopic electric fields recorded in the brain.New & NoteworthyWe studied the consequences of the action potential (AP) initiation site on the extracellular signatures of APs. We show that: (1) at the time of AP initiation the action initial segment (AIS) forms a dipole with the soma, (2) the width but not (3) amplitude of the extracellular AP generated by this dipole increases with the soma-AIS distance. This may help to monitor dynamic changes in the AIS position in experimental in vivo recordings.

scholarly journals Electrophysiological Assessment of the Cutaneous Arborization of Aδ-Fiber Nociceptors

1999 ◽  
Vol 82 (3) ◽  
pp. 1164-1177 ◽  
Author(s):  
Yuan B. Peng ◽  
Matthias Ringkamp ◽  
James N. Campbell ◽  
Richard A. Meyer
Keyword(s):  
Receptive Field ◽  
Action Potential ◽  
Branch Point ◽  
Functional Anatomy ◽  
Initiation Site ◽  
Propagation Time ◽  
Branch Points ◽  
Action Potential Initiation ◽  
The Mean ◽  
Potential Initiation

Little is known about the relationship between the branching structure and function of physiologically identified cutaneous nociceptor terminals. The axonal arborization itself, however, has an impact on the afferent signal that is conveyed along the parent axon to the CNS. We therefore developed electrophysiological techniques to investigate the branching structure of cutaneous nociceptors. Single-fiber recordings were obtained from physiologically identified nociceptors that innervated the hairy skin of the monkey. Electrodes for transcutaneous stimulation were fixed at two separate locations inside the receptive field. For 32 Aδ-fiber nociceptors, distinct steps in latency of the recorded action potential were observed as the intensity of the transcutaneous electrical stimulus increased, indicating discrete sites for action potential initiation. The number of discrete latencies at each stimulation location ranged from 1 to 9 (3.7 ± 0.2; mean ± SE) and the mean size of the latency step was 9.9 ± 1.0 ms (range: 0.4–89.1 ms). For seven Aδ fibers, collision techniques were used to locate the position of the branch point where the daughter fibers that innervated the two locations within the receptive field join the parent axon. To correct for changes in electrical excitability at the peripheral terminals, collision experiments between the two skin locations and between each skin location and a nerve trunk electrode were necessary. Nine branch points were studied in the seven Aδ fibers; the mean propagation time from the action potential initiation site to the branch point was 31 ± 5 ms corresponding to a distance of 54 ± 10 mm. Almost half of the daughter branches were unmyelinated. These results demonstrate that collision techniques can be used to study the functional anatomy of physiologically identified nociceptive afferent terminals. Furthermore these results indicate that some nociceptive afferents branch quite proximal to their peripheral receptive field. Occlusion of action potential activity can occur in these long branches such that the shorter branches dominate in the response to natural stimuli.

Temperature-sensitive conduction failure at axon branch points

1978 ◽  
Vol 41 (1) ◽  
pp. 1-8 ◽  
Author(s):  
M. Westerfield ◽  
R. W. Joyner ◽  
J. W. Moore
Keyword(s):  
Action Potential ◽  
High Temperatures ◽  
Computer Simulations ◽  
Action Potentials ◽  
Critical Ratio ◽  
Temperature Sensitive ◽  
Branch Points ◽  
Action Potential Propagation ◽  
Conduction Failure ◽  
Axon Branch

1. The propagation of action potentials through the branching regions of squid axons was examined experimentally and with computer simulations over a temperature range of 5-25 degrees C. 2. Above a critical ratio of postbranch to prebranch diameters, propagation of an action potential failed. The value of this critical ratio is very sensitive to temperature and is smaller at high temperatures. The experimentally measured Q10 of the critical ratio is 0.37 +/- 0.04. 3. Evaluation of a number of parameters of action-potential propagation showed that this effect is closely related to the change in the width of the action potential with temperature (Q10 = 0.29 +/- 0.01).

scholarly journals Control of sensory ectopic spike initiation by descending modulatory projection neurons

2015 ◽  
Author(s):  
Carola Städele ◽  
Wolfgang Stein
Keyword(s):  
Sensory Neurons ◽  
Action Potentials ◽  
Physiological Activity ◽  
Initiation Site ◽  
Projection Neurons ◽  
Dynamic Adjustment ◽  
Descending Pathways ◽  
Stomatogastric Nervous System ◽  
Sensory Activity ◽  
Spike Initiation

Descending pathways are important modulators of motor networks and allow the dynamic adjustment of behaviors to changing internal and external conditions. Central pattern generating networks (CPG) have been particularly amenable to study the modulation of motor networks and demonstrated that virtually all levels of information processing are controlled by descending projections. CPGs receive sensory feedback and while it is known that sensory activity can be gated by central pathways, we here present for the first time that descending projection neurons modulate action potential initiation in sensory neurons. We used the fact that the anterior gastric receptor neuron (AGR), a single-cell bipolar muscle tendon organ in the crustacean stomatogastric nervous system, generates spontaneous ectopic action potentials in its axon. We found that axonal spike initiation is under direct neuromodulatory control by a pair of descending projection neurons. These IV (inferior ventricular) neurons descend from the brain and are known to control CPGs in the stomatogastric ganglion (STG). Activation of the IV neurons elicited a long-lasting decrease in AGR ectopic spike activity. This decrease was only observed when spikes were generated ectopically in the central portion of the axon, i.e. the modulation was specific to the site of spontaneous spike initiation. The decrease could be mimicked by focal application of the IV neuron co-transmitter histamine and IV neuron actions were diminished after blocking H2 receptors, indicating a direct descending modulation of the axonal spike initiation site. In contrast, the propagation dynamics of en-passant action potentials were not affected. Descending modulatory projection neurons therefore control axonal spike initiation in sensory neurons without affecting afferent spike propagation to increase the physiological activity repertoire of sensory pathways.

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.

Presynaptic membrane potential and transmitter release at the crayfish neuromuscular junction

1984 ◽  
Vol 52 (1) ◽  
pp. 99-113 ◽  
Author(s):  
J. M. Wojtowicz ◽  
H. L. Atwood
Keyword(s):  
Membrane Potential ◽  
Action Potential ◽  
Transmitter Release ◽  
Action Potentials ◽  
Neuromuscular Junctions ◽  
Lucifer Yellow ◽  
Morphological Features ◽  
Calcium Dependent ◽  
Axon Branch ◽  
Set Up

Release of transmitter was evoked at neuromuscular junctions of the crayfish opener muscle by passage of current through an intracellular electrode impaling a branch of the motor axon close to a muscle fiber. Membrane-potential changes in the presynaptic axon branch were monitored, together with postsynaptic potentials. Depolarization of impaled secondary axonal branches by more than 10 mV led to an increase in asynchronous transmitter release. The release was facilitated by prolonged (50-500 ms) depolarizations and it decayed rapidly when depolarization was terminated. Ca2+ was essential for facilitated release; however, no indication of a Ca spike was found at the recording site. Input-output curves for the synapse were obtained by applying depolarizing pulses of varying amplitude to the axon branch. Transmitter output was strongly influenced by both amplitude and duration of the applied depolarization. During normal synaptic transmission, propagated Na+-dependent action potentials were recorded in the secondary axonal branches but there was no evidence for a calcium-dependent component for these action potentials. Evoked release was dependent on Ca2+ and was steeply dependent on the amplitude of the action potential, which could be made variable in size by application of tetrodotoxin (TTX). Prolonged depolarization of axonal branches resulted in enhancement of transmitter release evoked by an action potential. The enhancement occurred in spite of a simultaneous reduction of the amplitude of the action potential. Morphological features of the terminals were investigated after injection of lucifer yellow into the axon. An electrical model incorporating the morphological features suggests that membrane-potential changes set up in the main axon reach the nearest terminals with 30-40% attenuation, while events originating in the terminals would be severely attenuated in the main axon. Comparison of the crayfish synapse with other frequently studied synapses shows both similarities and differences, suggesting that it is not possible to apply findings made in one synapse to all others.

Calcium Dynamics and Compartmentalization in Leech Neurons

2005 ◽  
Vol 94 (6) ◽  
pp. 4430-4440 ◽  
Author(s):  
Sofija Andjelic ◽  
Vincent Torre
Keyword(s):  
Information Processing ◽  
Action Potential ◽  
Action Potentials ◽  
Time Course ◽  
Ccd Camera ◽  
Calcium Dynamics ◽  
Single Action ◽  
Single Action Potential ◽  
Calcium Indicator ◽  
Mechanosensory Neurons

Calcium dynamics in leech neurons were studied using a fast CCD camera. Fluorescence changes (Δ F/ F) of the membrane impermeable calcium indicator Oregon Green were measured. The dye was pressure injected into the soma of neurons under investigation. Δ F/ F caused by a single action potential (AP) in mechanosensory neurons had approximately the same amplitude and time course in the soma and in distal processes. By contrast, in other neurons such as the Anterior Pagoda neuron, the Annulus Erector motoneuron, the L motoneuron, and other motoneurons, APs evoked by passing depolarizing current in the soma produced much larger fluorescence changes in distal processes than in the soma. When APs were evoked by stimulating one distal axon through the root, Δ F/ F was large in all distal processes but very small in the soma. Our results show a clear compartmentalization of calcium dynamics in most leech neurons in which the soma does not give propagating action potentials. In such cells, the soma, while not excitable, can affect information processing by modulating the sites of origin and conduction of AP propagation in distal excitable processes.

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