Short-Term Dynamics of Synaptic Transmission Within the Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex

The short-term plasticity of synaptic transmission between excitatory neurons within a barrel of layer 4 rat somatosensory neocortex was investigated. Action potentials in presynaptic neurons at frequencies ranging from 1 to 100 Hz evoked depressing postsynaptic excitatory postsynaptic potentials (EPSPs). Recovery from synaptic depression followed an exponential time course with best-fit parameters that differed greatly between individual synaptic connections. The average maximal short-term depression was close to 0.5 with a recovery time constant of around 500 ms. Analysis of each individual sweep showed that there was a correlation between the amplitude of the response to the first and second action potentials such that large first EPSPs were followed by smaller than average second EPSPs and vice versa. Short-term depression between excitatory layer 4 neurons can thus be termed use dependent. A simple model describing use-dependent short-term plasticity was able to closely simulate the experimentally observed dynamic behavior of these synapses for regular spike trains. More complex irregular trains of 10 action potentials occurring within 500 ms were initially well described, but during the train errors increased. Thus for short periods of time the dynamic behavior of these synapses can be predicted accurately. In conjunction with data describing the connectivity, this forms a first step toward computational modeling of the excitatory neuronal network of layer 4 barrel cortex. Simulation of whisking-evoked activity suggests that short-term depression may provide a mechanism for enhancing the detection of objects within the whisker space.

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Faculty Opinions recommendation of Short-term dynamics of synaptic transmission within the excitatory neuronal network of rat layer 4 barrel cortex.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1007939.99960 ◽

2002 ◽

Author(s):

Kevan A Martin

Keyword(s):

Synaptic Transmission ◽

Neuronal Network ◽

Barrel Cortex ◽

Short Term ◽

Layer 4

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Frequency-Dependent Modulation of Short-Term Plasticity of GABAergic Synaptic Transmission

International Journal of Physiology and Pathophysiology ◽

10.1615/intjphyspathophys.v9.i2.30 ◽

2018 ◽

Vol 9 (2) ◽

pp. 119-126

Author(s):

Oksana P. Kolesnyk ◽

Svetlana A. Fedulova ◽

Mycola S. Veselovsky

Keyword(s):

Synaptic Transmission ◽

Short Term ◽

Frequency Dependent ◽

Short Term Plasticity ◽

Gabaergic Synaptic Transmission

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Short-Term Plasticity at Inhibitory Synapses in Rat Striatum and Its Effects on Striatal Output

Journal of Neurophysiology ◽

10.1152/jn.2001.85.5.2088 ◽

2001 ◽

Vol 85 (5) ◽

pp. 2088-2099 ◽

Cited By ~ 25

Author(s):

John S. Fitzpatrick ◽

Garnik Akopian ◽

John P. Walsh

Keyword(s):

Action Potentials ◽

Brain Slices ◽

Current Injection ◽

Inhibitory Synapses ◽

Rat Striatum ◽

Short Term ◽

Short Term Plasticity ◽

Adult Rat ◽

Glutamate Receptor Antagonists

Two forms of short-term plasticity at inhibitory synapses were investigated in adult rat striatal brain slices using intracellular recordings. Intrastriatal stimulation in the presence of the ionotropic glutamate receptor antagonists 6-cyano-7-nitroquinoxaline-2,3-dione (20 μM) andd,l-2-amino-5-phosphonovaleric acid (50 μM) produced an inhibitory postsynaptic potential (IPSP) that reversed polarity at −76 ± 1 (SE) mV and was sensitive to bicuculline (30 μM). The IPSP rectified at hyperpolarized membrane potentials due in part to activation of K+ channels. The IPSP exhibited two forms of short-term plasticity, paired-pulse depression (PPD) and synaptic augmentation. PPD lasted for several seconds and was greatest at interstimulus intervals (ISIs) of several hundred milliseconds, reducing the IPSP to 80 ± 2% of its control amplitude at an ISI of 200 ms. Augmentation of the IPSP, elicited by a conditioning train of 15 stimuli applied at 20 Hz, was 119 ± 1% of control when sampled 2 s after the conditioning train. Augmentation decayed with a time constant of 10 s. We tested if PPD and augmentation modify the ability of the IPSP to prevent the generation of action potentials. A train of action potentials triggered by a depolarizing current injection of constant amplitude could be interrupted by stimulation of an IPSP. If this IPSP was the second in a pair of IPSPs, it was less effective in blocking spikes due to PPD. By contrast, augmented IPSPs were more effective in blocking spikes. The same results were achieved when action potentials were triggered by a depolarizing current injection of varying amplitude, a manipulation that produces nearly identical spike times from trial to trial and approximates the in vivo behavior of these neurons. These results demonstrate that short-term plasticity of inhibition can modify the output of the striatum and thus may be an important component of information processing during behaviors that involve the striatum.

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A General Model of Synaptic Transmission and Short-Term Plasticity

Neuron ◽

10.1016/j.neuron.2009.03.025 ◽

2009 ◽

Vol 62 (4) ◽

pp. 539-554 ◽

Cited By ~ 105

Author(s):

Bin Pan ◽

Robert S. Zucker

Keyword(s):

Synaptic Transmission ◽

General Model ◽

Short Term ◽

Short Term Plasticity

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The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex

Journal of Neuroscience ◽

10.1523/jneurosci.20-20-07579.2000 ◽

2000 ◽

Vol 20 (20) ◽

pp. 7579-7586 ◽

Cited By ~ 99

Author(s):

Carl C. H. Petersen ◽

Bert Sakmann

Keyword(s):

Neuronal Network ◽

Barrel Cortex ◽

Layer 4

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Pharmacological and kinetic characterization of two functional classes of serotonergic modulation in Aplysia sensory neurons

Journal of Neurophysiology ◽

10.1152/jn.1996.75.2.855 ◽

1996 ◽

Vol 75 (2) ◽

pp. 855-866 ◽

Cited By ~ 12

Author(s):

L. L. Stark ◽

A. R. Mercer ◽

N. J. Emptage ◽

T. J. Carew

Keyword(s):

Synaptic Transmission ◽

Sensory Neurons ◽

Time Course ◽

Behavioral Sensitization ◽

Input Resistance ◽

Short Term ◽

Synaptic Facilitation ◽

Functional Classes ◽

Kinetics Of ◽

Serotonergic Modulation

1. Modulation of mechanoafferent sensory neurons (SNs) by the neutrotransmitter serotonin (5HT) plays a significant role in behavioral sensitization of several withdrawal reflexes in Aplysia. The modulatory effects of 5HT on these SNs include increased excitability, increased input resistance, action potential broadening, and increased synaptic transmission. Based on a previously described dissociation of some of these modulatory effects, revealed with the 5HT-receptor antagonist, cyproheptadine, we investigated whether a similar dissociation could be found by systematically varying the concentration of the endogenous agonist, 5HT. 2. We first applied a range of 5HT concentrations to isolated pleural/pedal ganglia (containing tail SNs and tail motor neurons, respectively), and measured the magnitude of 5HT-induced modulation of spike broadening and increased excitability. The resulting dose-response curve showed that both forms of modulation increase monotonically as a function of 5HT concentration, but that excitability has a lower threshold for modulation by 5HT than does spike duration. 3. We further characterized the modulatory effects of 5HT on Aplysia SNs by comparing the time course of onset of modulation by 5HT and the time course of recovery after washout. Independent of 5HT concentration, modulation of excitability increases rapidly in the presence of 5HT and recovers rapidly (< 3 min) after washout. Similarly, input resistance increases and recovers rapidly, mirroring the profile of increased excitability. However, modulation of spike duration exhibits two profiles, dependent on 5HT concentration. Low concentrations of 5HT (0.5 and 1 microM) induce a rapid-onset and transient-recovery form of spike broadening, which resembles the kinetics of increased excitability and increased input resistance. Higher concentrations of 5HT (2.5 and 5 microM) induce a more slowly developing and prolonged-recovery form of spike broadening (> 9 min). At these higher concentrations, the recovery profile for prolonged spike broadening is significantly different from those observed for both increased excitability and increased input resistance. 4. We next compared the relationship between spike broadening and short-term synaptic facilitation. We found that significant facilitation of synaptic transmission requires a high 5HT concentration, which is comparable with that required to induce prolonged spike broadening. Similarly, the recovery profiles for spike broadening and synaptic facilitation are strikingly similar, recovering in parallel. 5. Our experiments show that the modulatory effects of 5HT in the tail SNs can be dissociated both by their sensitivity to different concentrations of 5HT and by their kinetics of serotonergic modulation. Based on these results, together with extensive evidence from other laboratories, we propose that the short-term modulatory effects of 5HT fall into two distinct functional classes. The first class, which includes excitability, input resistance, and transient spike broadening, has a low threshold for 5HT modulation and recovers rapidly. The second class, which includes prolonged spike broadening and short-term synaptic facilitation, has a higher threshold for modulation and recovers more slowly. It now will be of interest to determine the functional contribution of each of these classes to different aspects of sensitization.

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Synaptic transmission and short-term plasticity at the calyx of Held synapse revealed by multielectrode array recordings

Journal of Neuroscience Methods ◽

10.1016/j.jneumeth.2008.07.015 ◽

2008 ◽

Vol 174 (2) ◽

pp. 227-236 ◽

Cited By ~ 9

Author(s):

Martin D. Haustein ◽

Thomas Reinert ◽

Annika Warnatsch ◽

Bernhard Englitz ◽

Beatrice Dietz ◽

...

Keyword(s):

Synaptic Transmission ◽

Multielectrode Array ◽

Short Term ◽

Calyx Of Held ◽

Short Term Plasticity ◽

Array Recordings

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Two Dynamically Distinct Inhibitory Networks in Layer 4 of the Neocortex

Journal of Neurophysiology ◽

10.1152/jn.00283.2003 ◽

2003 ◽

Vol 90 (5) ◽

pp. 2987-3000 ◽

Cited By ~ 343

Author(s):

Michael Beierlein ◽

Jay R. Gibson ◽

Barry W. Connors

Keyword(s):

Barrel Cortex ◽

Dynamic Properties ◽

Inhibitory Synapses ◽

Projection Neurons ◽

Inhibitory Interneurons ◽

Short Term ◽

Layer 4 ◽

Recurrent Collaterals ◽

Chemical Synapses ◽

Excitatory And Inhibitory Synapses

Normal operations of the neocortex depend critically on several types of inhibitory interneurons, but the specific function of each type is unknown. One possibility is that interneurons are differentially engaged by patterns of activity that vary in frequency and timing. To explore this, we studied the strength and short-term dynamics of chemical synapses interconnecting local excitatory neurons (regular-spiking, or RS, cells) with two types of inhibitory interneurons: fast-spiking (FS) cells, and low-threshold spiking (LTS) cells of layer 4 in the rat barrel cortex. We also tested two other pathways onto the interneurons: thalamocortical connections and recurrent collaterals from corticothalamic projection neurons of layer 6. The excitatory and inhibitory synapses interconnecting RS cells and FS cells were highly reliable in response to single stimuli and displayed strong short-term depression. In contrast, excitatory and inhibitory synapses interconnecting the RS and LTS cells were less reliable when initially activated. Excitatory synapses from RS cells onto LTS cells showed dramatic short-term facilitation, whereas inhibitory synapses made by LTS cells onto RS cells facilitated modestly or slightly depressed. Thalamocortical inputs strongly excited both RS and FS cells but rarely and only weakly contacted LTS cells. Both types of interneurons were strongly excited by facilitating synapses from axon collaterals of corticothalamic neurons. We conclude that there are two parallel but dynamically distinct systems of synaptic inhibition in layer 4 of neocortex, each defined by its intrinsic spiking properties, the short-term plasticity of its chemical synapses, and (as shown previously) an exclusive set of electrical synapses. Because of their unique dynamic properties, each inhibitory network will be recruited by different temporal patterns of cortical activity.

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