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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]
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“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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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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