scholarly journals Temporal filters in response to presynaptic spike trains: Interplay of cellular, synaptic and short-term plasticity time scales

2021 ◽  
Author(s):  
Yugarshi Mondal ◽  
Rodrigo F. O. Pena ◽  
Horacio G. Rotstein

Temporal filters, the ability of postsynaptic neurons to preferentially select certain presynaptic input patterns, have been shown to be associated with the notion of information filtering and coding of sensory inputs. Their properties can be dynamically characterized as the transient responses to periodic presynaptic inputs. Short-term plasticity (STP) has been proposed to be an important player in the generation of temporal filters, but the response of postsynaptic neurons to presynaptic inputs depends on a collection of time scales in addition to STP's, which conspire to create temporal filters: the postsynaptic time scales generated by the cellular intrinsic currents and the presynaptic time scales captured by the ISI distribution patterns. The mechanisms by which these time scales and the processes giving rise to them interact to produce temporal filters in response to presynaptic input spike trains are not well understood. We carry out a systematic modeling and computational analysis to understand how the postsynaptic low-, high- and band-pass temporal filters are generated in response to periodic presynaptic spike trains in the presence STP, and how the dynamic properties of these filters depend on the interplay of a hierarchy of processes: arrival of the presynaptic spikes, the activation of STP and its effect on the synaptic connection efficacy, and the response of the postsynaptic cell. The time scales associated with each of these processes operate at the short-term, single-event level (they are activated at the arrival of each presynaptic spike) and collectively produce the long-term time scales that determine the shape and properties of the filters. We develop a series of mathematical tools to address these issues for a relatively simple model where depression and facilitation interact only at the level of the synaptic efficacy change as time progresses and we extend our results and tools to account for more complex models that involve interactions at the STP level and multiple STP time scales. We use these tools to understand the mechanisms of generation of temporal filters in the postsynaptic cells in terms of the properties and dynamics of the interacting building blocks.

2000 ◽  
Vol 83 (5) ◽  
pp. 3031-3041 ◽  
Author(s):  
Chris M. Hempel ◽  
Kenichi H. Hartman ◽  
X.-J. Wang ◽  
Gina G. Turrigiano ◽  
Sacha B. Nelson

Short-term synaptic plasticity, in particular short-term depression and facilitation, strongly influences neuronal activity in cerebral cortical circuits. We investigated short-term plasticity at excitatory synapses onto layer V pyramidal cells in the rat medial prefrontal cortex, a region whose synaptic dynamic properties have not been systematically examined. Using intracellular and extracellular recordings of synaptic responses evoked by stimulation in layers II/III in vitro, we found that short-term depression and short-term facilitation are similar to those described previously in other regions of the cortex. In additition, synapses in the prefrontal cortex prominently express augmentation, a longer lasting form of short-term synaptic enhancement. This consists of a 40–60% enhancement of synaptic transmission which lasts seconds to minutes and which can be induced by stimulus trains of moderate duration and frequency. Synapses onto layer III neurons in the primary visual cortex express substantially less augmentation, indicating that this is a synapse-specific property. Intracellular recordings from connected pairs of layer V pyramidal cells in the prefrontal cortex suggest that augmentation is a property of individual synapses that does not require activation of multiple synaptic inputs or neuromodulatory fibers. We propose that synaptic augmentation could function to enhance the ability of a neuronal circuit to sustain persistent activity after a transient stimulus. This idea is explored using a computer simulation of a simplified recurrent cortical network.


2004 ◽  
Vol 91 (2) ◽  
pp. 1064-1070 ◽  
Author(s):  
John E. Lewis ◽  
Leonard Maler

Synaptic dynamics comprise a variety of interacting processes acting on a wide range of time scales. This enables a synapse to perform a large array of computations, from temporal and spatial filtering to associative learning. In this study, we describe how changing synaptic gain via long-term plasticity can act to shape the temporal filtering of a synapse through modulation of short-term plasticity. In the weakly electric fish, parallel fibers from cerebellar granule cells provide massive feedback inputs to the pyramidal neurons of the electrosensory lateral line lobe. We demonstrate a long-term synaptic enhancement (LTE) of these synapses that is biochemically similar to the presynaptic long-term potentiation expressed by parallel fibers in the mammalian cerebellum. Using a novel stimulation protocol and a simple modeling paradigm, we then quantify the changes in short-term plasticity during the induction of LTE and show that these changes can be explained by gradual changes in only one model parameter, that which is associated with the baseline probability of transmitter release. These changes lead to a shift in the spike frequency preference of the synapse, suggesting that long-term plasticity is not only involved in controlling the gain of the parallel fiber synapse, but also provides a means of controlling synaptic filtering over multiple time scales.


Author(s):  
Mohammad Z. Awad ◽  
Ryan J. Vaden ◽  
Zachary T. Irwin ◽  
Christopher L. Gonzalez ◽  
Sarah Black ◽  
...  

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Nishant Singh ◽  
Thomas Bartol ◽  
Herbert Levine ◽  
Terrence Sejnowski ◽  
Suhita Nadkarni

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Atefeh Pooryasin ◽  
Marta Maglione ◽  
Marco Schubert ◽  
Tanja Matkovic-Rachid ◽  
Sayed-mohammad Hasheminasab ◽  
...  

AbstractThe physical distance between presynaptic Ca2+ channels and the Ca2+ sensors triggering the release of neurotransmitter-containing vesicles regulates short-term plasticity (STP). While STP is highly diversified across synapse types, the computational and behavioral relevance of this diversity remains unclear. In the Drosophila brain, at nanoscale level, we can distinguish distinct coupling distances between Ca2+ channels and the (m)unc13 family priming factors, Unc13A and Unc13B. Importantly, coupling distance defines release components with distinct STP characteristics. Here, we show that while Unc13A and Unc13B both contribute to synaptic signalling, they play distinct roles in neural decoding of olfactory information at excitatory projection neuron (ePN) output synapses. Unc13A clusters closer to Ca2+ channels than Unc13B, specifically promoting fast phasic signal transfer. Reduction of Unc13A in ePNs attenuates responses to both aversive and appetitive stimuli, while reduction of Unc13B provokes a general shift towards appetitive values. Collectively, we provide direct genetic evidence that release components of distinct nanoscopic coupling distances differentially control STP to play distinct roles in neural decoding of sensory information.


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