The DOI matches its Crossref record; 63 of the 65 references it cites were found in a registry or an index.
Astrocyte-Neuron Lactate Transport Is Required for Long-Term Memory Formation
Open accessAbstract
We report that, in the rat hippocampus, learning leads to a significant increase in extracellular lactate levels that derive from glycogen, an energy reserve selectively localized in astrocytes. Astrocytic glycogen breakdown and lactate release are essential for long-term but not short-term memory formation, and for the maintenance of long-term potentiation (LTP) of synaptic strength elicited in vivo. Disrupting the expression of the astrocytic lactate transporters monocarboxylate transporter 4 (MCT4) or MCT1 causes amnesia, which, like LTP impairment, is rescued by L-lactate but not equicaloric glucose. Disrupting the expression of the neuronal lactate transporter MCT2 also leads to amnesia that is unaffected by either L-lactate or glucose, suggesting that lactate import into neurons is necessary for long-term memory. Glycogenolysis and astrocytic lactate transporters are also critical for the induction of molecular changes required for memory formation, including the induction of phospho-CREB, Arc, and phospho-cofilin. We conclude that astrocyte-neuron lactate transport is required for long-term memory formation.
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“Increased levels of lactate have also been shown to be correlated with neuronal network activity, as the astrocyte-neuron lactate shuttle is known to regulate neuronal activity.31”
From ApoE4-dependent lysosomal cholesterol accumulation impairs mitochondrial homeostasis and oxidative phosphorylation in human astrocytes (2023) · cites this paper as [31]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Increased levels of lactate have also been shown to be correlated with neuronal network activity, as the astrocyte-neuron lactate shuttle is known to regulate neuronal activity.31”
From ApoE4-dependent lysosomal cholesterol accumulation impairs mitochondrial homeostasis and oxidative phosphorylation in human astrocytes (2023) · cites this paper as [31]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Conversely, metabolic state may, in turn, influence the properties of neuronal computation19, suggesting a bidirectional interaction between energy metabolism and information processing.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [19]
In the citing paper
“Another astrocyte-derived molecule, L-lactate, plays a key role in LTP at hippocampal CA1 synapses 37 .”
From Astrocyte function from information processing to cognition and cognitive impairment (2019) · cites this paper as [37]
In the citing paper
“A first study identified a necessary role for L-lactate in long-term episodic memory by pharmacological inhibition of its production in astrocytes 37 .”
From Astrocyte function from information processing to cognition and cognitive impairment (2019) · cites this paper as [37]
In the citing paper
“The fact that L-lactate cannot be substituted in this function by equicaloric glucose 37 hints, however, at additional non-metabolic functions for this molecule.”
From Astrocyte function from information processing to cognition and cognitive impairment (2019) · cites this paper as [37]
In the citing paper
“blocking neuronal oxidative utilization of lactate affects neuronal survival and even memory formation (Suzuki et al., 2011; Lee et al., 2012).”
From Metabolic reprogramming during neuronal differentiation from aerobic glycolysis to neuronal oxidative phosphorylation (2016) · cites this paper as Suzuki et al., 2011
In the citing paper
“If an ANLS operates at rest, it could also explain why chronic disruption of MCT, LDH, or glycogenolysis in astrocytes can affect neuronal function (Suzuki et al., 2011; Zhang et al., 2016; Mazuel et al., 2017); these and similar results showing that MCT and lactate transport contribute to neuronal health and function provide evidence for some critical biological role for lactate uptake, but do”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Suzuki et al., 2011
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Citations
Cites
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917
Pellerin, L., & Magistretti, P. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10625 · Cited by 2,927 · cited 1×
“…Fédérale de Lausanne (EPFL) and Center for Psychiatric Neuroscience, University of Lausanne-CHUV, Lausanne, Switzerland 6These authors contributed equally to this work *Correspondence: cristina.alberini@mssm.edu (C.M.A.), pierre.magistretti@epfl.ch (P.J.M.) DOI 10.1016/j.cell.2011.02.018”
InfluentialSelf-citationTranscriptional regulation by the phosphorylation-dependent factor CREB
Mayr, B., & Montminy, M. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35085068 · Cited by 2,587
Learning induces long-term potentiation in the hippocampus
Whitlock, J. R., Heynen, A. J., Shuler, M. G., & Bear, M. F. (2006) · Science · doi:10.1126/science.1128134 · Cited by 1,913
Tripartite synapses: astrocytes process and control synaptic information
Perea, G., Navarrete, M., & Araque, A. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.05.001 · Cited by 1,820
The Neurobiology of Consolidations, Or, How Stable is the Engram?
Dudai, Y. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.142050 · Cited by 1,671
Long-term potentiation depends on release of d-serine from astrocytes
Henneberger, C., Papouin, T., Oliet, S. H. R., & Rusakov, D. A. (2010) · Nature · doi:10.1038/nature08673 · Cited by 1,389
Magistretti, P. J., Pellerin, L., Rothman, D. L., & Shulman, R. G. (1999) · Science · doi:10.1126/science.283.5401.496 · Cited by 1,170
Self-citationMetabolic coupling between glia and neurons
Tsacopoulos, M., & Magistretti, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-03-00877.1996 · Cited by 1,006
Self-citationTranscription Factors in Long-Term Memory and Synaptic Plasticity
Alberini, C. M. (2009) · Physiological Reviews · doi:10.1152/physrev.00017.2008 · Cited by 991
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Brain energy metabolism: focus on Astrocyte-neuron metabolic cooperation
Bélanger, M., Allaman, I., & Magistretti, P. J. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.08.016 · Cited by 2,313
Self-citationSynaptic Energy Use and Supply
Harris, J. J., Jolivet, R., & Attwell, D. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.019 · Cited by 1,747
Oligodendroglia metabolically support axons and contribute to neurodegeneration
Lee, Y., Morrison, B. M., Li, Y., Lengacher, S., Farah, M. H., Hoffman, P. N., Liu, Y., Tsingalia, A., Jin, L., Zhang, P.-W., et al. (2012) · Nature · doi:10.1038/nature11314 · Cited by 1,664
Self-citationVerkhratsky, A., & Nedergaard, M. (2018) · Physiological Reviews · doi:10.1152/physrev.00042.2016 · Cited by 1,678
Sugar for the brain: the role of glucose in physiological and pathological brain function
Mergenthaler, P., Lindauer, U., Dienel, G. A., & Meisel, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.07.001 · Cited by 1,612
Metadata
- Authors
- Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., & Alberini, C. M.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- James J. Peters VA Medical Center (US)
- Centre Hospitalier Universitaire Vaudois (CH)
- Corresponding author
- Magistretti, Pierre J.
- Alberini, Cristina M.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2011-03
- Volume
- 144
- Issue
- 5
- Pages
- 810-823
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3073831
- OpenAlex
- W2001725826
- Cited by
- 1,711
- References
- 65
- Citations by year
- 2026: 157 · 2025: 138 · 2024: 142 · 2023: 145 · 2022: 118 · 2021: 123 · 2020: 119 · 2019: 109 · 2018: 111 · 2017: 88 · 2016: 95 · 2015: 100 · 2014: 78 · 2013: 70 · 2012: 76
- FWCI
- 42.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 905 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- IRIS (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- SERVAL (Université de Lausanne) (submittedVersion, other-oa)
- Funders
- U.S. Department of Veterans Affairs
- École Polytechnique Fédérale de Lausanne
- National Institutes of Health
- National Institute of Mental Health (R01MH074736, R01MH065635, T32MH087004)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- long-term memory, hippocampus, extracellular lactate, MCT4, MCT1, MCT2, long-term potentiation, amnesia, L-lactate, synaptic plasticity, CREB, Arc, cofilin, learning
- MeSH terms
- Monocarboxylate Transport Protein 1, Animals, Arabinose, Astrocytes, Glycogen, Hippocampus, Muscle Proteins, Neurons, Sugar Alcohols, Lactic Acid, Monocarboxylic Acid Transporters, Symporters, Imino Furanoses, Rats, Memory, Long-Term
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