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      Effects of Metabolic Energy on Synaptic Transmission and Dendritic Integration in Pyramidal Neurons

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          Abstract

          As a sophisticated computing unit, the pyramidal neuron requires sufficient metabolic energy to fuel its powerful computational capabilities. However, the majority of previous works focus on nonlinear integration and energy consumption in individual pyramidal neurons but seldom on the effects of metabolic energy on synaptic transmission and dendritic integration. Here, we developed biologically plausible models to simulate the synaptic transmission and dendritic integration of pyramidal neurons, exploring the relations between synaptic transmission and metabolic energy and between dendritic integration and metabolic energy. We find that synaptic energy not only drives synaptic vesicle cycle, but also participates in the regulation of this cycle. Release probability of synapses adapts to synaptic energy levels by regulating the speed of synaptic vesicle cycle. Besides, we also find that to match neural energy levels, only a part of the synapses receive presynaptic signals during a given period so that neurons have a low action potential frequency. That is, the number of simultaneously active synapses over a period of time should be adapted to neural energy levels.

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          Most cited references36

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          Glutamate exocytosis from astrocytes controls synaptic strength.

          The release of transmitters from glia influences synaptic functions. The modalities and physiological functions of glial release are poorly understood. Here we show that glutamate exocytosis from astrocytes of the rat hippocampal dentate molecular layer enhances synaptic strength at excitatory synapses between perforant path afferents and granule cells. The effect is mediated by ifenprodil-sensitive NMDA ionotropic glutamate receptors and involves an increase of transmitter release at the synapse. Correspondingly, we identify NMDA receptor 2B subunits on the extrasynaptic portion of excitatory nerve terminals. The receptor distribution is spatially related to glutamate-containing synaptic-like microvesicles in the apposed astrocytic processes. This glial regulatory pathway is endogenously activated by neuronal activity-dependent stimulation of purinergic P2Y1 receptors on the astrocytes. Thus, we provide the first combined functional and ultrastructural evidence for a physiological control of synaptic activity via exocytosis of glutamate from astrocytes.
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            Synaptic vesicle pools.

            Communication between cells reaches its highest degree of specialization at chemical synapses. Some synapses talk in a 'whisper'; others 'shout'. The 'louder' the synapse, the more synaptic vesicles are needed to maintain effective transmission, ranging from a few hundred (whisperers) to nearly a million (shouters). These vesicles reside in different 'pools', which have been given a bewildering array of names. In this review, we focus on five tissue preparations in which synaptic vesicle pools have been identified and thoroughly characterized. We argue that, in each preparation, each vesicle can be assigned to one of three distinct pools.
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              Astrocytes potentiate transmitter release at single hippocampal synapses.

              Astrocytes play active roles in brain physiology. They respond to neurotransmitters and modulate neuronal excitability and synaptic function. However, the influence of astrocytes on synaptic transmission and plasticity at the single synapse level is unknown. Ca(2+) elevation in astrocytes transiently increased the probability of transmitter release at hippocampal area CA3-CA1 synapses, without affecting the amplitude of synaptic events. This form of short-term plasticity was due to the release of glutamate from astrocytes, a process that depended on Ca(2+) and soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) protein and that activated metabotropic glutamate receptors (mGluRs). The transient potentiation of transmitter release became persistent when the astrocytic signal was temporally coincident with postsynaptic depolarization. This persistent plasticity was mGluR-mediated but N-methyl-d-aspartate receptor-independent. These results indicate that astrocytes are actively involved in the transfer and storage of synaptic information.
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                Author and article information

                Contributors
                Journal
                Front Comput Neurosci
                Front Comput Neurosci
                Front. Comput. Neurosci.
                Frontiers in Computational Neuroscience
                Frontiers Media S.A.
                1662-5188
                26 September 2018
                2018
                : 12
                : 79
                Affiliations
                [1] 1Department of Automation, Shanghai Jiao Tong University , Shanghai, China
                [2] 2Key Laboratory of System Control and Information Processing, Ministry of Education , Shanghai, China
                Author notes

                Edited by: Yu-Guo Yu, Fudan University, China

                Reviewed by: Claire Cheetham, University of Pittsburgh, United States; Ervin Wolf, University of Debrecen, Hungary; Zhongmin Lu, University of California, San Diego, United States

                *Correspondence: Hong Huo huohong@ 123456sjtu.edu.cn
                Article
                10.3389/fncom.2018.00079
                6168642
                f3bee1df-6cc6-4e1b-a4a3-cbfe9b9fa53f
                Copyright © 2018 Yuan, Huo and Fang.

                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) and the copyright owner(s) 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
                : 28 March 2018
                : 07 September 2018
                Page count
                Figures: 5, Tables: 1, Equations: 14, References: 51, Pages: 13, Words: 9972
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 41571402
                Funded by: Science Fund for Creative Research Groups 10.13039/501100003999
                Award ID: 61221003
                Categories
                Neuroscience
                Original Research

                Neurosciences
                synaptic transmission,dendritic integration,metabolic energy,release probability,connection number,biologically plausible models,synaptic vesicle cycle

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