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      Long-term plasticity determines the postsynaptic response to correlated afferents with multivesicular short-term synaptic depression

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          Abstract

          Synchrony in a presynaptic population leads to correlations in vesicle occupancy at the active sites for neurotransmitter release. The number of independent release sites per presynaptic neuron, a synaptic parameter recently shown to be modified during long-term plasticity, will modulate these correlations and therefore have a significant effect on the firing rate of the postsynaptic neuron. To understand how correlations from synaptic dynamics and from presynaptic synchrony shape the postsynaptic response, we study a model of multiple release site short-term plasticity and derive exact results for the crosscorrelation function of vesicle occupancy and neurotransmitter release, as well as the postsynaptic voltage variance. Using approximate forms for the postsynaptic firing rate in the limits of low and high correlations, we demonstrate that short-term depression leads to a maximum response for an intermediate number of presynaptic release sites, and that this leads to a tuning-curve response peaked at an optimal presynaptic synchrony set by the number of neurotransmitter release sites per presynaptic neuron. These effects arise because, above a certain level of correlation, activity in the presynaptic population is overly strong resulting in wastage of the pool of releasable neurotransmitter. As the nervous system operates under constraints of efficient metabolism it is likely that this phenomenon provides an activity-dependent constraint on network architecture.

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          Most cited references42

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          Short-term synaptic plasticity.

          Synaptic transmission is a dynamic process. Postsynaptic responses wax and wane as presynaptic activity evolves. This prominent characteristic of chemical synaptic transmission is a crucial determinant of the response properties of synapses and, in turn, of the stimulus properties selected by neural networks and of the patterns of activity generated by those networks. This review focuses on synaptic changes that result from prior activity in the synapse under study, and is restricted to short-term effects that last for at most a few minutes. Forms of synaptic enhancement, such as facilitation, augmentation, and post-tetanic potentiation, are usually attributed to effects of a residual elevation in presynaptic [Ca(2+)]i, acting on one or more molecular targets that appear to be distinct from the secretory trigger responsible for fast exocytosis and phasic release of transmitter to single action potentials. We discuss the evidence for this hypothesis, and the origins of the different kinetic phases of synaptic enhancement, as well as the interpretation of statistical changes in transmitter release and roles played by other factors such as alterations in presynaptic Ca(2+) influx or postsynaptic levels of [Ca(2+)]i. Synaptic depression dominates enhancement at many synapses. Depression is usually attributed to depletion of some pool of readily releasable vesicles, and various forms of the depletion model are discussed. Depression can also arise from feedback activation of presynaptic receptors and from postsynaptic processes such as receptor desensitization. In addition, glial-neuronal interactions can contribute to short-term synaptic plasticity. Finally, we summarize the recent literature on putative molecular players in synaptic plasticity and the effects of genetic manipulations and other modulatory influences.
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            Neural correlations, population coding and computation.

            How the brain encodes information in population activity, and how it combines and manipulates that activity as it carries out computations, are questions that lie at the heart of systems neuroscience. During the past decade, with the advent of multi-electrode recording and improved theoretical models, these questions have begun to yield answers. However, a complete understanding of neuronal variability, and, in particular, how it affects population codes, is missing. This is because variability in the brain is typically correlated, and although the exact effects of these correlations are not known, it is known that they can be large. Here, we review studies that address the interaction between neuronal noise and population codes, and discuss their implications for population coding in general.
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              Synaptic computation.

              Neurons are often considered to be the computational engines of the brain, with synapses acting solely as conveyers of information. But the diverse types of synaptic plasticity and the range of timescales over which they operate suggest that synapses have a more active role in information processing. Long-term changes in the transmission properties of synapses provide a physiological substrate for learning and memory, whereas short-term changes support a variety of computations. By expressing several forms of synaptic plasticity, a single neuron can convey an array of different signals to the neural circuit in which it operates.
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                Author and article information

                Journal
                Front Comput Neurosci
                Front Comput Neurosci
                Front. Comput. Neurosci.
                Frontiers in Computational Neuroscience
                Frontiers Media S.A.
                1662-5188
                30 January 2014
                2014
                : 8
                : 2
                Affiliations
                [1] 1Warwick Systems Biology Centre, University of Warwick Coventry, UK
                [2] 2Warwick Systems Biology Doctoral Training Centre, University of Warwick Coventry, UK
                [3] 3School of Life Sciences, University of Warwick Coventry, UK
                Author notes

                Edited by: Tatjana Tchumatchenko, Max Planck Institute for Brain Research, Germany

                Reviewed by: Jean-Pascal Pfister, Cambridge University, UK (in collaboration with Simone Surace); Michael Graupner, New York University, USA

                *Correspondence: Alex D. Bird, Warwick Systems Biology Centre, Senate House, University of Warwick, CV4 7AL, Coventry, UK e-mail: a.d.bird@ 123456warwick.ac.uk

                This article was submitted to the journal Frontiers in Computational Neuroscience.

                Article
                10.3389/fncom.2014.00002
                3906582
                24523691
                5b65c3f2-7432-49e5-9b53-1982e52b17ef
                Copyright © 2014 Bird and Richardson.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 06 August 2013
                : 07 January 2014
                Page count
                Figures: 8, Tables: 1, Equations: 25, References: 47, Pages: 11, Words: 8242
                Categories
                Neuroscience
                Original Research Article

                Neurosciences
                short-term plasticity,voltage fluctuations,correlations and synchrony,synaptic depression,long-term plasticity

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