scholarly journals A model of order-selectivity based on dynamic changes in the balance of excitation and inhibition produced by short-term synaptic plasticity

2015 ◽  
Vol 113 (2) ◽  
pp. 509-523 ◽  
Author(s):  
Vishwa Goudar ◽  
Dean V. Buonomano
Keyword(s):  
Synaptic Plasticity ◽  
Computational Models ◽  
Experimental Studies ◽  
Inhibitory Synapses ◽  
Speech Discrimination ◽  
Short Term ◽  
Dynamic Changes ◽  
Short Term Plasticity ◽  
Underlying Mechanisms ◽  
Parametric Analyses

Determining the order of sensory events separated by a few hundred milliseconds is critical to many forms of sensory processing, including vocalization and speech discrimination. Although many experimental studies have recorded from auditory order-sensitive and order-selective neurons, the underlying mechanisms are poorly understood. Here we demonstrate that universal properties of cortical synapses—short-term synaptic plasticity of excitatory and inhibitory synapses—are well suited for the generation of order-selective neural responses. Using computational models of canonical disynaptic circuits, we show that the dynamic changes in the balance of excitation and inhibition imposed by short-term plasticity lead to the generation of order-selective responses. Parametric analyses predict that among the forms of short-term plasticity expressed at excitatory-to-excitatory, excitatory-to-inhibitory, and inhibitory-to-excitatory synapses, the single most important contributor to order-selectivity is the paired-pulse depression of inhibitory postsynaptic potentials (IPSPs). A topographic model of the auditory cortex that incorporates short-term plasticity accounts for both context-dependent suppression and enhancement in response to paired tones. Together these results provide a framework to account for an important computational problem based on ubiquitous synaptic properties that did not yet have a clearly established computational function. Additionally, these studies suggest that disynaptic circuits represent a fundamental computational unit that is capable of processing both spatial and temporal information.

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

2001 ◽  
Vol 85 (5) ◽  
pp. 2088-2099 ◽  
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.

scholarly journals Short-term plasticity in glomerular inhibitory circuits shapes olfactory bulb output

2020 ◽  
Vol 123 (3) ◽  
pp. 1120-1132 ◽  
Author(s):  
Fu-Wen Zhou ◽  
Zuo-Yi Shao ◽  
Michael T. Shipley ◽  
Adam C. Puche
Keyword(s):  
Fluorescent Protein ◽  
Feedback Inhibition ◽  
Olfactory Nerve ◽  
Inhibitory Synapses ◽  
Acid Decarboxylase ◽  
Short Term ◽  
Short Term Plasticity ◽  
Inhibitory Circuits ◽  
Frequency Independent ◽  
Green Fluorescent

Short-term plasticity is a fundamental synaptic property thought to underlie memory and neural processing. The glomerular microcircuit comprises complex excitatory and inhibitory interactions and transmits olfactory nerve signals to the excitatory output neurons, mitral/tufted cells (M/TCs). The major glomerular inhibitory interneurons, short axon cells (SACs) and periglomerular cells (PGCs), both provide feedforward and feedback inhibition to M/TCs and have reciprocal inhibitory synapses between each other. Olfactory input is episodically driven by sniffing. We hypothesized that frequency-dependent short-term plasticity within these inhibitory circuits could influence signals sent to higher-order olfactory networks. To assess short-term plasticity in glomerular circuits and MC outputs, we virally delivered channelrhodopsin-2 (ChR2) in glutamic acid decarboxylase-65 promotor (GAD2-cre) or tyrosine hydroxylase promoter (TH-cre) mice and selectively activated one of these two populations while recording from cells of the other population or from MCs. Selective activation of TH-ChR2-expressing SACs inhibited all recorded GAD2-green fluorescent protein(GFP)-expressing presumptive PGC cells, and activation of GAD2-ChR2 cells inhibited TH-GFP-expressing SACs, indicating reciprocal inhibitory connections. SAC synaptic inhibition of GAD2-expressing cells was significantly facilitated at 5–10 Hz activation frequencies. In contrast, GAD2-ChR2 cell inhibition of TH-expressing cells was activation-frequency independent. Both SAC and PGC inhibition of MCs also exhibited short-term plasticity, pronounced in the 5–20 Hz range corresponding to investigative sniffing frequency ranges. In paired SAC and olfactory nerve electrical stimulations, the SAC to MC synapse was able to markedly suppress MC spiking. These data suggest that short-term plasticity across investigative sniffing ranges may differentially regulate intra- and interglomerular inhibitory circuits to dynamically shape glomerular output signals to downstream targets. NEW & NOTEWORTHY Short-term plasticity is a fundamental synaptic property that modulates synaptic strength based on preceding activity of the synapse. In rodent olfaction, sensory input arrives episodically driven by sniffing rates ranging from quiescent respiration (1–2 Hz) through to investigative sniffing (5–10 Hz). Here we show that glomerular inhibitory networks are exquisitely sensitive to input frequencies and exhibit plasticity proportional to investigative sniffing frequencies. This indicates that olfactory glomerular circuits are dynamically modulated by episodic sniffing input.

scholarly journals Functional synapse types via characterization of short-term synaptic plasticity

2019 ◽  
Author(s):  
Jung Hoon Lee ◽  
Luke Campagnola ◽  
Stephanie C. Seeman ◽  
Tim Jarsky ◽  
Stefan Mihalas
Keyword(s):  
Large Scale ◽  
Short Term ◽  
Brain Science ◽  
Short Term Plasticity ◽  
Synaptic Physiology ◽  
History Of ◽  
Experimental Protocols ◽  
Network Simulations ◽  
Underlying Mechanisms

AbstractThe strengths of synaptic connections dynamically change depending on the history of synaptic events, which is referred to as short-term plasticity (STP). While STP’s underlying mechanisms are well researched, its exact functions remain poorly understood. This is in part due to the diverse patterns of STP experimentally reported. Recently, the Allen Institute for Brain Science has launched the synaptic physiology pipeline to characterize the diverse properties of synapses. Since this pipeline generates a large-scale survey of synapses in mouse primary visual cortex using highly standardized experimental protocols, it provides a unique opportunity to study diverse patterns of STP. Here, we develop an end-to-end workflow that can characterize STP from the Allen Institute for Brain Science pipeline data and conduct network simulations to infer STP’s functions. Employing this workflow, we find 1) that diverse patterns of STP exist even in the same synapse classes and 2) that postsynaptic neurons’ responses have distinct characteristics depending on STP.

scholarly journals Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses

2007 ◽  
Vol 104 (24) ◽  
pp. 10258-10263 ◽  
Author(s):  
F. Tecuapetla ◽  
L. Carrillo-Reid ◽  
J. Bargas ◽  
E. Galarraga
Keyword(s):  
Synaptic Plasticity ◽  
Inhibitory Synapses ◽  
Short Term ◽  
Dopaminergic Modulation

Net Interaction Between Different Forms of Short-Term Synaptic Plasticity and Slow-IPSPs in the Hippocampus and Auditory Cortex

1998 ◽  
Vol 80 (4) ◽  
pp. 1765-1774 ◽  
Author(s):  
Dean V. Buonomano ◽  
Michael M. Merzenich
Keyword(s):  
Synaptic Plasticity ◽  
Auditory Cortex ◽  
Hippocampal Neurons ◽  
Time Dependent ◽  
Peak Amplitude ◽  
Short Term ◽  
Paired Pulse ◽  
Postsynaptic Potentials ◽  
Short Term Plasticity ◽  
Cgp 55845

Buonomano, Dean V. and Michael M. Merzenich. Net interaction between different forms of short-term synaptic plasticity and slow-IPSPs in the hippocampus and auditory cortex. J. Neurophysiol. 80: 1765–1774, 1998. Paired-pulse plasticity is typically used to study the mechanisms underlying synaptic transmission and modulation. An important question relates to whether, under physiological conditions in which various opposing synaptic properties are acting in parallel, the net effect is facilitatory or depressive, that is, whether cells further or closer to threshold. For example, does the net sum of paired-pulse facilitation (PPF) of excitatory postsynaptic potentials (EPSPs), paired-pulse depression (PPD) of inhibitory postsynaptic potentials (IPSPs), and the hyperpolarizing slow IPSP result in depression or facilitation? Here we examine how different time-dependent properties act in parallel and examine the contribution of γ-aminobutyric acid-B (GABAB) receptors that mediate two opposing processes, the slow IPSP and PPD of the fast IPSP. Using intracellular recordings from rat CA3 hippocampal neurons and L-II/III auditory cortex neurons, we examined the postsynaptic responses to paired-pulse stimulation (with intervals between 50 and 400 ms) of the Schaffer collaterals and white matter, respectively. Changes in the amplitude, time-to-peak (TTP), and slope of each EPSP were analyzed before and after application of the GABAB antagonist CGP-55845. In both CA3 and L-II/III neurons the peak amplitude of the second EPSP was generally depressed (further from threshold) compared with the first at the longer intervals; however, these EPSPs were generally broader and exhibited a longer TTP that could result in facilitation by enhancing temporal summation. At the short intervals CA3 neurons exhibited facilitation of the peak EPSP amplitude in the absence and presence of CGP-55845. In contrast, on average L-II/III cells did not exhibit facilitation at any interval, in the absence or presence of CGP-55845. CGP-55845 generally “erased” short-term plasticity, equalizing the peak amplitude and TTP of the first and second EPSPs at longer intervals in the hippocampus and auditory cortex. These results show that it is necessary to consider all time-dependent properties to determine whether facilitation or depression will dominate under intact pharmacological conditions. Furthermore our results suggest that GABAB-dependent properties may be the major contributor to short-term plasticity on the time scale of a few hundred milliseconds and are consistent with the hypothesis that the balance of different time-dependent processes can modulate the state of networks in a complex manner and could contribute to the generation of temporally sensitive neural responses.

scholarly journals Self-Tuning of Neural Circuits Through Short-Term Synaptic Plasticity

2007 ◽  
Vol 97 (6) ◽  
pp. 4079-4095 ◽  
Author(s):  
David Sussillo ◽  
Taro Toyoizumi ◽  
Wolfgang Maass
Keyword(s):  
Synaptic Plasticity ◽  
Activity Level ◽  
Cortical Circuits ◽  
Short Term ◽  
Cortical Networks ◽  
Short Term Plasticity ◽  
Numerous Experimental Data ◽  
Self Tuning ◽  
Synaptic Dynamics ◽  
Low Activity

Numerous experimental data show that cortical networks of neurons are not silent in the absence of external inputs, but rather maintain a low spontaneous firing activity. This aspect of cortical networks is likely to be important for their computational function, but is hard to reproduce in models of cortical circuits of neurons because the low-activity regime is inherently unstable. Here we show—through theoretical analysis and extensive computer simulations—that short-term synaptic plasticity endows models of cortical circuits with a remarkable stability in the low-activity regime. This short-term plasticity works as a homeostatic mechanism that stabilizes the overall activity level in spite of drastic changes in external inputs and internal circuit properties, while preserving reliable transient responses to signals. The contribution of synaptic dynamics to this stability can be predicted on the basis of general principles from control theory.

Structural Contributions to Short-Term Synaptic Plasticity

2004 ◽  
Vol 84 (1) ◽  
pp. 69-85 ◽  
Author(s):  
MATTHEW A. XU-FRIEDMAN ◽  
WADE G. REGEHR
Keyword(s):  
Synaptic Plasticity ◽  
Synaptic Transmission ◽  
Synaptic Strength ◽  
Short Term ◽  
Ongoing Activity ◽  
Short Term Plasticity ◽  
Synaptic Ultrastructure

Xu-Friedman, Matthew A., and Wade G. Regehr. Structural Contributions to Short-Term Synaptic Plasticity. Physiol Rev 84: 69–85, 2004; 10.1152/physrev.00016.2003.—Synaptic ultrastructure is critical to many basic hypotheses about synaptic transmission. Various aspects of synaptic ultrastructure have also been implicated in the mechanisms of short-term plasticity. These forms of plasticity can greatly affect synaptic strength during ongoing activity. We review the evidence for how synaptic ultrastructure may contribute to facilitation, depletion, saturation, and desensitization.

scholarly journals Comparing the Seizure-Induced Impairment of Short-Term Plasticity in Dorsal and Ventral Hippocampus in Kindled Mice

2021 ◽  
Author(s):  
Nahid Roohi ◽  
◽  
Mahboubeh Ahmadi ◽  
Yaghoun Fathollahi ◽  
Amir Shojaei ◽  
...  
Keyword(s):  
Synaptic Plasticity ◽  
Dorsal Hippocampus ◽  
Hippocampal Slices ◽  
Ventral Hippocampus ◽  
Control Group ◽  
Short Term ◽  
Paired Pulse ◽  
Short Term Plasticity ◽  
Dorsal Hippocampal ◽  
Fepsp Slope

There are many differences among dorsal and ventral hippocampal neural circuits that affect the synaptic plasticity. In this study we compared the occurrence of short-term plasticity in the field excitatory post synaptic potentials (fEPSP) in dorsal and ventral hippocampal CA1 area following kindled seizures. Animals (male C57 B6/J mice, 12 weeks of age) were kindled by intraperitoneal injections of pentylenetetrazole (PTZ) and fEPSPs were recorded from dorsal and ventral hippocampal slices. Short-term plasticity was evaluated by measuring fEPSP-slope and fEPSP-area following paired-pulse stimulation delivered at three inter-pulse intervals (20, 80 and 160 ms). Obtained results showed that in control slices fEPSP-slope was greater in ventral- compared to dorsal hippocampus, but there was no difference in fEPSP-area among two regions. In hippocampal slices of kindled animals, fEPSP-slope was similar in dorsal and ventral regions, but fEPSP-area was greater in ventral- compared to dorsal hippocampus. In addition, fEPSP-area was greater in kindled compared to control group only in ventral hippocampus. PTZ kindled slices showed impaired short-term facilitation and the paired-pulse index was reduced only at dorsal hippocampal slices. Kindling had no significant effect on paired-pulse ratio in ventral hippocampal slices. Our findings indicated that the seizure occurrence affected the neural activity of hippocampus in a regional dependent manner. Although kindling increased fEPSP-area in ventral hippocampus, kindling-induced changes in short-term synaptic plasticity was significant only in dorsal hippocampal slices compared to control group. The difference in the responses of hippocampal dorsal and ventral poles has to be considered in the future researches.

Memory Stacking in Hierarchical Networks

2016 ◽  
Vol 28 (2) ◽  
pp. 327-353 ◽  
Author(s):  
Johan Westö ◽  
Patrick J. C. May ◽  
Hannu Tiitinen
Keyword(s):  
Synaptic Plasticity ◽  
Auditory Cortex ◽  
Computational Models ◽  
Hierarchical Structures ◽  
Short Term ◽  
Hierarchical Networks ◽  
Local Memory ◽  
Memory Mechanism ◽  
Spectrotemporal Receptive Field ◽  
Temporal Rate

Robust representations of sounds with a complex spectrotemporal structure are thought to emerge in hierarchically organized auditory cortex, but the computational advantage of this hierarchy remains unknown. Here, we used computational models to study how such hierarchical structures affect temporal binding in neural networks. We equipped individual units in different types of feedforward networks with local memory mechanisms storing recent inputs and observed how this affected the ability of the networks to process stimuli context dependently. Our findings illustrate that these local memories stack up in hierarchical structures and hence allow network units to exhibit selectivity to spectral sequences longer than the time spans of the local memories. We also illustrate that short-term synaptic plasticity is a potential local memory mechanism within the auditory cortex, and we show that it can bring robustness to context dependence against variation in the temporal rate of stimuli, while introducing nonlinearities to response profiles that are not well captured by standard linear spectrotemporal receptive field models. The results therefore indicate that short-term synaptic plasticity might provide hierarchically structured auditory cortex with computational capabilities important for robust representations of spectrotemporal patterns.

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