57
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Lactate Produced by Glycogenolysis in Astrocytes Regulates Memory Processing

      research-article
      1 , 3 , * , 1 , 2 , 3 , 4 , 1 , 2 , 3 , 4 , 5 , 6
      PLoS ONE
      Public Library of Science

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          When administered either systemically or centrally, glucose is a potent enhancer of memory processes. Measures of glucose levels in extracellular fluid in the rat hippocampus during memory tests reveal that these levels are dynamic, decreasing in response to memory tasks and loads; exogenous glucose blocks these decreases and enhances memory. The present experiments test the hypothesis that glucose enhancement of memory is mediated by glycogen storage and then metabolism to lactate in astrocytes, which provide lactate to neurons as an energy substrate. Sensitive bioprobes were used to measure brain glucose and lactate levels in 1-sec samples. Extracellular glucose decreased and lactate increased while rats performed a spatial working memory task. Intrahippocampal infusions of lactate enhanced memory in this task. In addition, pharmacological inhibition of astrocytic glycogenolysis impaired memory and this impairment was reversed by administration of lactate or glucose, both of which can provide lactate to neurons in the absence of glycogenolysis. Pharmacological block of the monocarboxylate transporter responsible for lactate uptake into neurons also impaired memory and this impairment was not reversed by either glucose or lactate. These findings support the view that astrocytes regulate memory formation by controlling the provision of lactate to support neuronal functions.

          Related collections

          Most cited references114

          • Record: found
          • Abstract: found
          • Article: not found

          Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization.

          Glutamate, released at a majority of excitatory synapses in the central nervous system, depolarizes neurons by acting at specific receptors. Its action is terminated by removal from the synaptic cleft mostly via Na(+)-dependent uptake systems located on both neurons and astrocytes. Here we report that glutamate, in addition to its receptor-mediated actions on neuronal excitability, stimulates glycolysis--i.e., glucose utilization and lactate production--in astrocytes. This metabolic action is mediated by activation of a Na(+)-dependent uptake system and not by interaction with receptors. The mechanism involves the Na+/K(+)-ATPase, which is activated by an increase in the intracellular concentration of Na+ cotransported with glutamate by the electrogenic uptake system. Thus, when glutamate is released from active synapses and taken up by astrocytes, the newly identified signaling pathway described here would provide a simple and direct mechanism to tightly couple neuronal activity to glucose utilization. In addition, glutamate-stimulated glycolysis is consistent with data obtained from functional brain imaging studies indicating local nonoxidative glucose utilization during physiological activation.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Cell-cell and intracellular lactate shuttles.

            Once thought to be the consequence of oxygen lack in contracting skeletal muscle, the glycolytic product lactate is formed and utilized continuously in diverse cells under fully aerobic conditions. 'Cell-cell' and 'intracellular lactate shuttle' concepts describe the roles of lactate in delivery of oxidative and gluconeogenic substrates as well as in cell signalling. Examples of the cell-cell shuttles include lactate exchanges between between white-glycolytic and red-oxidative fibres within a working muscle bed, and between working skeletal muscle and heart, brain, liver and kidneys. Examples of intracellular lactate shuttles include lactate uptake by mitochondria and pyruvate for lactate exchange in peroxisomes. Lactate for pyruvate exchanges affect cell redox state, and by itself lactate is a ROS generator. In vivo, lactate is a preferred substrate and high blood lactate levels down-regulate the use of glucose and free fatty acids (FFA). As well, lactate binding may affect metabolic regulation, for instance binding to G-protein receptors in adipocytes inhibiting lipolysis, and thus decreasing plasma FFA availability. In vitro lactate accumulation upregulates expression of MCT1 and genes coding for other components of the mitochondrial reticulum in skeletal muscle. The mitochondrial reticulum in muscle and mitochondrial networks in other aerobic tissues function to establish concentration and proton gradients necessary for cells with high mitochondrial densities to oxidize lactate. The presence of lactate shuttles gives rise to the realization that glycolytic and oxidative pathways should be viewed as linked, as opposed to alternative, processes, because lactate, the product of one pathway, is the substrate for the other.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior.

              The past decade has seen an explosion of research on roles of neuron-astrocyte interactions in the control of brain function. We highlight recent studies performed on the tripartite synapse, the structure consisting of pre- and postsynaptic elements of the synapse and an associated astrocytic process. Astrocytes respond to neuronal activity and neurotransmitters, through the activation of metabotropic receptors, and can release the gliotransmitters ATP, d-serine, and glutamate, which act on neurons. Astrocyte-derived ATP modulates synaptic transmission, either directly or through its metabolic product adenosine. d-serine modulates NMDA receptor function, whereas glia-derived glutamate can play important roles in relapse following withdrawal from drugs of abuse. Cell type-specific molecular genetics has allowed a new level of examination of the function of astrocytes in brain function and has revealed an important role of these glial cells that is mediated by adenosine accumulation in the control of sleep and in cognitive impairments that follow sleep deprivation.
                Bookmark

                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                13 December 2011
                : 6
                : 12
                : e28427
                Affiliations
                [1 ]Neuroscience Program, University of Illinois at Urbana-Champaign, Champaign, Illinois, United States of America
                [2 ]Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Champaign, Illinois, United States of America
                [3 ]Department of Psychology, University of Illinois at Urbana-Champaign, Champaign, Illinois, United States of America
                [4 ]Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Champaign, Illinois, United States of America
                [5 ]Department of Psychiatry, University of Illinois at Urbana-Champaign, Champaign, Illinois, United States of America
                [6 ]Department of Biomedical Engineering, University of Illinois at Urbana-Champaign, Champaign, Illinois, United States of America
                Georgia Health Sciences University, United States of America
                Author notes

                Conceived and designed the experiments: LAN PEG. Performed the experiments: LAN. Analyzed the data: LAN DLK PEG. Contributed reagents/materials/analysis tools: DLK PEG. Wrote the paper: LAN DLK PEG.

                Article
                PONE-D-11-12947
                10.1371/journal.pone.0028427
                3236748
                22180782
                6974e996-1f13-4a5a-bb15-d7a9b95f1f8a
                Newman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 7 July 2011
                : 8 November 2011
                Page count
                Pages: 11
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Physiological Processes
                Energy Metabolism
                Neuroscience
                Behavioral Neuroscience
                Learning and Memory
                Medicine
                Anatomy and Physiology
                Physiological Processes
                Energy Metabolism
                Metabolic Disorders
                Glycogen Storage Diseases
                Neurology
                Dementia
                Alzheimer Disease
                Vascular Dementia
                Neurodegenerative Diseases

                Uncategorized
                Uncategorized

                Comments

                Comment on this article