Astrocytes and oligodendrocytes in the thalamus jointly maintain synaptic activity by supplying metabolites
Open accessAbstract
Thalamic astrocytes and oligodendrocytes are coupled via gap junctions and form panglial networks. Here, we show that these networks have a key role in energy supply of neurons. Filling an astrocyte or an oligodendrocyte in acute slices with glucose or lactate is sufficient to rescue the decline of stimulation-induced field post-synaptic potential (fPSP) amplitudes during extracellular glucose deprivation (EGD). In mice lacking oligodendroglial coupling, loading an astrocyte with glucose does not rescue the EGD-mediated loss of fPSPs. Monocarboxylate and glucose transporters are required for rescuing synaptic activity during EGD. In mice deficient in astrocyte coupling, filling of an oligodendrocyte with glucose does not rescue fPSPs during EGD. Our results demonstrate that, in the thalamus, astrocytes and oligodendrocytes are jointly engaged in delivering energy substrates for sustaining neuronal activity and suggest that oligodendrocytes exert their effect mainly by assisting astrocytes in metabolite transfer to the postsynapse.
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Astroglial lactate is preferentially produced at sites of transcellular transport, compatible with a model of astroglial lactate routed through oligodendrocytes to the axonal compartment.
“This suggests that astroglial lactate is preferentially produced at sites of transcellular transport, compatible with a model of astroglial lactate routed through oligodendrocytes to the axonal compartment (Philippot et al., 2021).”
From Downregulated expression of lactate dehydrogenase in adult oligodendrocytes and its implication for the transfer of glycolysis products to axons (2024) · cites this paper as Philippot et al., 2021
The Discussion says thalamic oligodendrocytes mainly assist astrocytes in metabolite transport to postsynapses, “rather than by fueling axons or pre-synaptic structures.” That contradicts the proposed route to the axonal compartment. The Discussion also does not establish that astroglial lactate is preferentially produced at sites of transcellular transport; no page number is available in our copy. (LLM, conf=0.89)
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Cites
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 · see citing works
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 · cited 3× · see citing works
“Indeed, several recent studies, mainly in the optic nerve, but also in spinal cord, have demonstrated that delivery of these substrates by oligodendrocytes is critical for axonal function (Hirrlinger and Nave, 2014; F€ unfschilling et al., 2012; Brown et al., 2003; Lee et al., 2012).”
BackgroundGlycolytic oligodendrocytes maintain myelin and long-term axonal integrity
Fünfschilling, U., Supplie, L. M., Mahad, D., Boretius, S., Saab, A. S., Edgar, J., Brinkmann, B. G., Kassmann, C. M., Tzvetanova, I. D., Möbius, W., et al. (2012) · Nature · doi:10.1038/nature11007 · Cited by 1,523 · see citing works
Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo
Nimmerjahn, A., Kirchhoff, F., Kerr, J. N. D., & Helmchen, F. (2004) · Nature Methods · doi:10.1038/nmeth706 · Cited by 784 · see citing works
Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism
Saab, A. S., Tzvetavona, I. D., Trevisiol, A., Baltan, S., Dibaj, P., Kusch, K., Möbius, W., Goetze, B., Jahn, H. M., Huang, W., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.016 · Cited by 590 · cited 1× · see citing works
“In the optic nerve, axonal activity provokes glucose uptake into oligodendrocytes through incorporation of GLUT1 into the oligodendrocytic membrane, a mechanism not requiring gap junction coupling but NMDA receptors (Saab et al., 2016).”
BackgroundThe slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators
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“Glycogen breakdown also results in lactate production, is released in the extracellular space, and is taken up by neurons to fuel their energy needs (Magistretti et al., 1993; Bélanger et al., 2011).”
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Research works printed but not linked: 3
- Ho ¨ft, S., Griemsmann, S., Seifert, G., and Steinha ¨user, C. (2014). Heterogene- ity in expression of functional ionotropic glutamate and GABA receptors in as- trocytes across brain regions: insights from the thalamus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130602.
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Späte, E., Zhou, B., Sun, T., Kusch, K., Asadollahi, E., Siems, S. B., Depp, C., Werner, H. B., Saher, G., Hirrlinger, J., et al. (2024) · Glia · doi:10.1002/glia.24533 · Cited by 40 · see citing works
- Authors
- Philippot, C., Griemsmann, S., Jabs, R., Seifert, G., Kettenmann, H., & Steinhäuser, C.
- Affiliations
- University of Bonn (DE)
- Max Delbrück Center (DE)
- Corresponding author
- Steinhäuser, Christian
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2021-01
- Volume
- 34
- Issue
- 3
- Pages
- 108642
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W3122179404
- Cited by
- 47
- References
- 7
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 10 · 2023: 7 · 2022: 15 · 2021: 4
- FWCI
- 4.14
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- astrocytes, oligodendrocytes, thalamus, electrical coupling, synaptic activity, energy metabolism, glucose transporters, monocarboxylate transporters, lactate, postsynaptic neurons
- MeSH terms
- Animals, Astrocytes, Oligodendroglia, Thalamus, Chromosome Pairing, Mice
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