scholarly journals Synaptic Information Transmission in a Two-State Model of Short-Term Facilitation

Entropy ◽  
2019 ◽  
Vol 21 (8) ◽  
pp. 756 ◽  
Author(s):  
Mehrdad Salmasi ◽  
Martin Stemmler ◽  
Stefan Glasauer ◽  
Alex Loebel
Keyword(s):  
Action Potential ◽  
Information Transmission ◽  
Action Potentials ◽  
Synaptic Activity ◽  
Information Rate ◽  
Short Term ◽  
Release Probability ◽  
Synaptic Facilitation ◽  
Synaptic Release ◽  
Asynchronous Release

Action potentials (spikes) can trigger the release of a neurotransmitter at chemical synapses between neurons. Such release is uncertain, as it occurs only with a certain probability. Moreover, synaptic release can occur independently of an action potential (asynchronous release) and depends on the history of synaptic activity. We focus here on short-term synaptic facilitation, in which a sequence of action potentials can temporarily increase the release probability of the synapse. In contrast to the phenomenon of short-term depression, quantifying the information transmission in facilitating synapses remains to be done. We find rigorous lower and upper bounds for the rate of information transmission in a model of synaptic facilitation. We treat the synapse as a two-state binary asymmetric channel, in which the arrival of an action potential shifts the synapse to a facilitated state, while in the absence of a spike, the synapse returns to its baseline state. The information bounds are functions of both the asynchronous and synchronous release parameters. If synchronous release facilitates more than asynchronous release, the mutual information rate increases. In contrast, short-term facilitation degrades information transmission when the synchronous release probability is intrinsically high. As synaptic release is energetically expensive, we exploit the information bounds to determine the energy–information trade-off in facilitating synapses. We show that unlike information rate, the energy-normalized information rate is robust with respect to variations in the strength of facilitation.

Dichotomy of Action-Potential Backpropagation in CA1 Pyramidal Neuron Dendrites

2001 ◽  
Vol 86 (6) ◽  
pp. 2998-3010 ◽  
Author(s):  
Nace L. Golding ◽  
William L. Kath ◽  
Nelson Spruston
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Synaptic Activity ◽  
Resting Potential ◽  
Model Parameters ◽  
Voltage Sensitivity ◽  
Whole Cell ◽  
Ca1 Pyramidal Neurons ◽  
Whole Cell Recordings

In hippocampal CA1 pyramidal neurons, action potentials are typically initiated in the axon and backpropagate into the dendrites, shaping the integration of synaptic activity and influencing the induction of synaptic plasticity. Despite previous reports describing action-potential propagation in the proximal apical dendrites, the extent to which action potentials invade the distal dendrites of CA1 pyramidal neurons remains controversial. Using paired somatic and dendritic whole cell recordings, we find that in the dendrites proximal to 280 μm from the soma, single backpropagating action potentials exhibit <50% attenuation from their amplitude in the soma. However, in dendritic recordings distal to 300 μm from the soma, action potentials in most cells backpropagated either strongly (26–42% attenuation; n = 9/20) or weakly (71–87% attenuation; n = 10/20) with only one cell exhibiting an intermediate value (45% attenuation). In experiments combining dual somatic and dendritic whole cell recordings with calcium imaging, the amount of calcium influx triggered by backpropagating action potentials was correlated with the extent of action-potential invasion of the distal dendrites. Quantitative morphometric analyses revealed that the dichotomy in action-potential backpropagation occurred in the presence of only subtle differences in either the diameter of the primary apical dendrite or branching pattern. In addition, action-potential backpropagation was not dependent on a number of electrophysiological parameters (input resistance, resting potential, voltage sensitivity of dendritic spike amplitude). There was, however, a striking correlation of the shape of the action potential at the soma with its amplitude in the dendrite; larger, faster-rising, and narrower somatic action potentials exhibited more attenuation in the distal dendrites (300–410 μm from the soma). Simple compartmental models of CA1 pyramidal neurons revealed that a dichotomy in action-potential backpropagation could be generated in response to subtle manipulations of the distribution of either sodium or potassium channels in the dendrites. Backpropagation efficacy could also be influenced by local alterations in dendritic side branches, but these effects were highly sensitive to model parameters. Based on these findings, we hypothesize that the observed dichotomy in dendritic action-potential amplitude is conferred primarily by differences in the distribution, density, or modulatory state of voltage-gated channels along the somatodendritic axis.

scholarly journals Doc2b Ca2+ binding site mutants enhance synaptic release at rest at the expense of sustained synaptic strength

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Quentin Bourgeois-Jaarsma ◽  
Matthijs Verhage ◽  
Alexander J. Groffen
Keyword(s):  
Binding Site ◽  
Neurotransmitter Release ◽  
Action Potentials ◽  
Synaptic Strength ◽  
Cultured Neurons ◽  
Loss Of Function ◽  
Short Term ◽  
Synaptic Release ◽  
Activated State ◽  
Primary Cultured Neurons

Abstract Communication between neurons involves presynaptic neurotransmitter release which can be evoked by action potentials or occur spontaneously as a result of stochastic vesicle fusion. The Ca2+-binding double C2 proteins Doc2a and –b were implicated in spontaneous and asynchronous evoked release, but the mechanism remains unclear. Here, we compared wildtype Doc2b with two Ca2+ binding site mutants named DN and 6A, previously classified as gain- and loss-of-function mutants. They carry the substitutions D218,220N or D163,218,220,303,357,359A respectively. We found that both mutants bound phospholipids at low Ca2+ concentrations and were membrane-associated in resting neurons, thus mimicking a Ca2+-activated state. Their overexpression in hippocampal primary cultured neurons had similar effects on spontaneous and evoked release, inducing high mEPSC frequencies and increased short-term depression. Together, these data suggest that the DN and 6A mutants both act as gain-of-function mutants at resting conditions.

Properties of Action-Potential Initiation in Neocortical Pyramidal Cells: Evidence From Whole Cell Axon Recordings

2007 ◽  
Vol 97 (1) ◽  
pp. 746-760 ◽  
Author(s):  
Yousheng Shu ◽  
Alvaro Duque ◽  
Yuguo Yu ◽  
Bilal Haider ◽  
David A. McCormick
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Initial Segment ◽  
Pyramidal Cells ◽  
Synaptic Activity ◽  
Up States ◽  
Action Potential Initiation ◽  
Potential Initiation

Cortical pyramidal cells are constantly bombarded by synaptic activity, much of which arises from other cortical neurons, both in normal conditions and during epileptic seizures. The action potentials generated by barrages of synaptic activity may exhibit a variable site of origin. Here we performed simultaneous whole cell recordings from the soma and axon or soma and apical dendrite of layer 5 pyramidal neurons during normal recurrent network activity (up states), the intrasomatic or intradendritic injection of artificial synaptic barrages, and during epileptiform discharges in vitro. We demonstrate that under all of these conditions, the real or artificial synaptic bombardments propagate through the dendrosomatic-axonal arbor and consistently initiate action potentials in the axon initial segment that then propagate to other parts of the cell. Action potentials recorded intracellularly in vivo during up states and in response to visual stimulation exhibit properties indicating that they are typically initiated in the axon. Intracortical axons were particularly well suited to faithfully follow the generation of action potentials by the axon initial segment. Action-potential generation was more reliable in the distal axon than at the soma during epileptiform activity. These results indicate that the axon is the preferred site of action-potential initiation in cortical pyramidal cells, both in vivo and in vitro, with state-dependent back propagation through the somatic and dendritic compartments.

Information Rate Analysis of a Synaptic Release Site Using a Two-State Model of Short-Term Depression

2017 ◽  
Vol 29 (6) ◽  
pp. 1528-1560 ◽  
Author(s):  
Mehrdad Salmasi ◽  
Martin Stemmler ◽  
Stefan Glasauer ◽  
Alex Loebel
Keyword(s):  
Information Transfer ◽  
Transmission Rate ◽  
Release Site ◽  
Synaptic Depression ◽  
Information Rate ◽  
Short Term ◽  
Time Step ◽  
Synaptic Release ◽  
Rate Analysis ◽  
Two State Model

Synapses are the communication channels for information transfer between neurons; these are the points at which pulse-like signals are converted into the stochastic release of quantized amounts of chemical neurotransmitter. At many synapses, prior neuronal activity depletes synaptic resources, depressing subsequent responses of both spontaneous and spike-evoked releases. We analytically compute the information transmission rate of a synaptic release site, which we model as a binary asymmetric channel. Short-term depression is incorporated by assigning the channel a memory of depth one. A successful release, whether spike evoked or spontaneous, decreases the probability of a subsequent release; if no release occurs on the following time step, the release probabilities recover back to their default values. We prove that synaptic depression can increase the release site’s information rate if spontaneous release is more strongly depressed than spike-evoked release. When depression affects spontaneous and evoked release equally, the information rate must invariably decrease, even when the rate is normalized by the resources used for synaptic transmission. For identical depression levels, we analytically disprove the hypothesis, at least in this simplified model, that synaptic depression serves energy- and information-efficient encoding.

scholarly journals Regulation of Backpropagating Action Potentials in Mitral Cell Lateral Dendrites by A-Type Potassium Currents

2003 ◽  
Vol 89 (5) ◽  
pp. 2466-2472 ◽  
Author(s):  
J. M. Christie ◽  
G. L. Westbrook
Keyword(s):  
Olfactory Bulb ◽  
Action Potential ◽  
Action Potentials ◽  
Calcium Transient ◽  
Mitral Cell ◽  
Synaptic Activity ◽  
Calcium Transients ◽  
Access Resistance ◽  
Lateral Dendrite ◽  
Apical Dendrites

Dendrodendritic synapses, distributed along mitral cell lateral dendrites, provide powerful and extensive inhibition in the olfactory bulb. Activation of inhibition depends on effective penetration of action potentials into dendrites. Although action potentials backpropagate with remarkable fidelity in apical dendrites, this issue is controversial for lateral dendrites. We used paired somatic and dendritic recordings to measure action potentials in proximal dendritic segments (0–200 μm from soma) and action potential-generated calcium transients to monitor activity in distal dendritic segments (200–600 μm from soma). Somatically elicited action potentials were attenuated in proximal lateral dendrites. The attenuation was not due to impaired access resistance in dendrites or to basal synaptic activity. However, a single somatically elicited action potential was sufficient to evoke a calcium transient throughout the lateral dendrite, suggesting that action potentials reach distal dendritic compartments. Block of A-type potassium channels ( I A) with 4-aminopyridine (10 mM) prevented action potential attenuation in direct recordings and significantly increased dendritic calcium transients, particularly in distal dendritic compartments. Our results suggest that I A may regulate inhibition in the olfactory bulb by controlling action potential amplitudes in lateral dendrites.

Propagation of action potentials in the dendrites of neurons from rat spinal cord slice cultures

1996 ◽  
Vol 75 (1) ◽  
pp. 154-170 ◽  
Author(s):  
M. E. Larkum ◽  
M. G. Rioult ◽  
H. R. Luscher
Keyword(s):  
Spinal Cord ◽  
Action Potential ◽  
Calcium Imaging ◽  
Action Potentials ◽  
Synaptic Activity ◽  
Rat Spinal Cord ◽  
Voltage Sensitive Dye ◽  
Single Action ◽  
Before And After ◽  
Time Courses

1. We examined the propagation of action potentials in the dendrites of ventrally located presumed motoneurons of organotypic rat spinal cord cultures. Simultaneous patch electrode recordings were made from the dendrites and somata of individual cells. In other experiments we visualized the membrane voltage over all the proximal dendrites simultaneously using a voltage-sensitive dye and an array of photodiodes. Calcium imaging was used to measure the dendritic rise in Ca2+ accompanying the propagating action potentials. 2. Spontaneous and evoked action potentials were recorded using high-resistance patch electrodes with separations of 30-423 microm between the somatic and dendritic electrodes. 3. Action potentials recorded in the dendrites varied considerably in amplitude but were larger than would be expected if the dendrites were to behave as passive cables (sometimes little or no decrement was seen for distances of > 100 microm). Because the amplitude of the action potentials in different dendrites was not a simple function of distance from the soma, we suggest that the conductance responsible for the boosting of the action potential amplitude varied in density from dendrite to dendrite and possibly along each dendrite. 4. The dendritic action potentials were usually smaller and broader and arrived later at the dendritic electrode than at the somatic electrode irrespective of whether stimulation occurred at the dendrite or soma or as a result of spontaneous synaptic activity. This is clear evidence that the action potential is initiated at or near the soma and spreads out into the dendrites. The conduction velocity of the propagating action potential was estimated to be 0.5 m/s. 5. The voltage time courses of previously recorded action potentials were generated at the soma using voltage clamp before and after applying 1 microM tetrodotoxin (TTX) over the soma and dendrites. TTX reduced the amplitude of the action potential at the dendritic electrode to a value in the range expected for dendrites that behave as passive cables. This indicates that the conductance responsible for the actively propagating action potentials is a Na+ conductance. 6. The amplitude of the dendritic action potential could also be initially reduced more than the somatic action potential using 1-10 mM QX-314 (an intracellular sodium channel blocker) in the dendritic electrode as the drug diffused from the dendritic electrode toward the soma. Furthermore, in some cases the action potential elicited by current injection into the dendrite had two components. The first component was blocked by QX-314 in the first few seconds of the diffusion of the blocker. 7. In some cells, an afterdepolarizing potential (ADP) was more prominent in the dendrite than in the soma. This ADP could be reversibly blocked by 1 mM Ni2+ or by perfusion of a nominally Ca2+-free solution over the soma and dendrites. This suggests that the back-propagating action potential caused an influx of Ca2+ predominantly in the dendrites. 8. With the use of a voltage-sensitive dye (di-8-ANEPPS) and an array of photodiodes, the action potential was tracked along all the proximal dendrites simultaneously. The results confirmed that the action potential propagated actively, in contrast to similarly measured hyperpolarizing pulses that spread passively. There were also indications that the action potential was not uniformly propagated in all the dendrites, suggesting the possibility that the distribution of Na+ channels over the dendritic membrane is not uniform. 9. Calcium imaging with the Ca2+ fluorescent indicator Fluo-3 showed a larger percentage change in fluorescence in the dendrites than in the soma. Both bursts and single action potentials elicited sharp rises in fluorescence in the proximal dendrites, suggesting that the back-propagating action potential causes a concomitant rise in intracellular calcium concentration...

scholarly journals A two-step docking site model predicting different short-term synaptic plasticity patterns

2018 ◽  
Vol 150 (8) ◽  
pp. 1107-1124 ◽  
Author(s):  
Camila Pulido ◽  
Alain Marty
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Site Occupancy ◽  
Synaptic Strength ◽  
Docking Site ◽  
Short Term ◽  
Site Model ◽  
Step Model ◽  
One Step ◽  
Using Data

The strength of synaptic transmission varies during trains of presynaptic action potentials, notably because of the depletion of synaptic vesicles available for release. It has remained unclear why some synapses display depression over time, whereas others facilitate or show a facilitation and depression sequence. Here we compare the predictions of various synaptic models assuming that several docking/release sites are acting in parallel. These models show variation of docking site occupancy during trains of action potentials due to vesicular release and site replenishment, which give rise to changes in synaptic strength. To conform with recent studies, we assume an initial docking site occupancy of &lt;1, thus permitting site occupancy to increase during action potential trains and facilitation to occur. We consider both a standard one-step model and a more elaborate model that assumes a predocked state (two-step model). Whereas the one-step model predicts monotonic changes of synaptic strength during a train, the two-step model allows nonmonotonic changes, including the often-observed facilitation/depression sequence. Both models predict a partitioning of parameter space between initially depressing and facilitating synapses. Using data obtained from interneuron synapses in the cerebellum, we demonstrate an unusual form of depression/facilitation sequence for very high release probability after prolonged depolarization-induced transmitter release. These results indicate a depletion of predocked vesicles in the two-step model. By permitting docking site occupancy to be &lt;1 at rest, and by incorporating a separate predocked state, we reveal that docking site models can be expanded to mimic the large variety of time-dependent changes of synaptic strength that have been observed during action potential trains. Furthermore, the two-step model provides an effective framework to identify the specific mechanisms responsible for short-term changes in synaptic strength.

scholarly journals Discharge of the Readily Releasable Pool With Action Potentials at Hippocampal Synapses

2007 ◽  
Vol 98 (6) ◽  
pp. 3221-3229 ◽  
Author(s):  
Charles F. Stevens ◽  
James H. Williams
Keyword(s):  
Cell Culture ◽  
Synaptic Vesicles ◽  
Action Potentials ◽  
Synaptic Function ◽  
Hypertonic Solution ◽  
Synaptic Release ◽  
Releasable Pool ◽  
Readily Releasable Pool ◽  
Hippocampal Synapses ◽  
Asynchronous Release

A readily releasable pool (RRP) of synaptic vesicles has been identified at hippocampal synapses with application of hypertonic solution. RRP size correlates with important properties of synaptic function such as release probability. However, a discrepancy in RRP size has been reported depending on the method used to evoke synaptic release. This study was undertaken to determine quantitative relationships between the RRP defined with hypertonic solution and that released with trains of action potentials. We find that asynchronous release at cell culture synapses contributes significantly to the discharge of the RRP with trains of action potentials and that RRP size is the same when elicited by either nerve stimuli or hypertonic challenge.

scholarly journals Calcium sensor regulation of the CaV2.1 Ca2+ channel contributes to short-term synaptic plasticity in hippocampal neurons

2016 ◽  
Vol 113 (4) ◽  
pp. 1062-1067 ◽  
Author(s):  
Evanthia Nanou ◽  
Jane M. Sullivan ◽  
Todd Scheuer ◽  
William A. Catterall
Keyword(s):  
Synaptic Plasticity ◽  
Action Potentials ◽  
Hippocampal Neurons ◽  
Hippocampal Slices ◽  
Short Term ◽  
Synaptic Facilitation ◽  
Hippocampal Synapses ◽  
Presynaptic Nerve Terminals ◽  
Sensor Proteins ◽  
Kinetics Of

Short-term synaptic plasticity is induced by calcium (Ca2+) accumulating in presynaptic nerve terminals during repetitive action potentials. Regulation of voltage-gated CaV2.1 Ca2+ channels by Ca2+ sensor proteins induces facilitation of Ca2+ currents and synaptic facilitation in cultured neurons expressing exogenous CaV2.1 channels. However, it is unknown whether this mechanism contributes to facilitation in native synapses. We introduced the IM-AA mutation into the IQ-like motif (IM) of the Ca2+ sensor binding site. This mutation does not alter voltage dependence or kinetics of CaV2.1 currents, or frequency or amplitude of spontaneous miniature excitatory postsynaptic currents (mEPSCs); however, synaptic facilitation is completely blocked in excitatory glutamatergic synapses in hippocampal autaptic cultures. In acutely prepared hippocampal slices, frequency and amplitude of mEPSCs and amplitudes of evoked EPSCs are unaltered. In contrast, short-term synaptic facilitation in response to paired stimuli is reduced by ∼50%. In the presence of EGTA-AM to prevent global increases in free Ca2+, the IM-AA mutation completely blocks short-term synaptic facilitation, indicating that synaptic facilitation by brief, local increases in Ca2+ is dependent upon regulation of CaV2.1 channels by Ca2+ sensor proteins. In response to trains of action potentials, synaptic facilitation is reduced in IM-AA synapses in initial stimuli, consistent with results of paired-pulse experiments; however, synaptic depression is also delayed, resulting in sustained increases in amplitudes of later EPSCs during trains of 10 stimuli at 10–20 Hz. Evidently, regulation of CaV2.1 channels by CaS proteins is required for normal short-term plasticity and normal encoding of information in native hippocampal synapses.

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