Dynamics of Neuronal and Astrocytic Energy Molecules in Epilepsy
Open accessAbstract
The dynamics of energy molecules in the mouse brain during metabolic challenges induced by epileptic seizures were examined. A transgenic mouse line expressing a fluorescence resonance energy transfer (FRET)‐based adenosine triphosphate (ATP) sensor, selectively expressed in the cytosol of neurons, was used. An optical fiber was inserted into the hippocampus, and changes in cytosolic ATP concentration were estimated using the fiber photometry method. To induce epileptic neuronal hyperactivity, a train of electrical stimuli was delivered to a bipolar electrode placed alongside the optical fiber. Although maintaining a steady cytosolic ATP concentration is crucial for cell survival, a single episode of epileptic neuronal hyperactivity drastically reduced neuronal ATP levels. Interestingly, the magnitude of ATP reduction did not increase with the exacerbation of epilepsy, but rather decreased. This suggests that the primary consumption of ATP during epileptic neuronal hyperactivity may not be solely directed toward restoring the Na + and K + ionic imbalance caused by action potential bursts. Cytosolic ATP concentration reflects the balance between supply and consumption. To investigate the metabolic flux leading to neuronal ATP production, a new FRET‐based pyruvate sensor was developed and selectively expressed in the cytosol of astrocytes in transgenic mice. Upon epileptic neuronal hyperactivity, an increase in astrocytic pyruvate concentration was observed. Changes in the supply of energy molecules, such as glucose and oxygen, due to blood vessel constriction or dilation, as well as metabolic alterations in astrocyte function, may contribute to cytosolic ATP dynamics in neurons. image
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A marked reduction in ATP levels is observed during epileptic seizure activity.
“Consistent with these findings, in vivo studies have demonstrated that neuronal ATP levels remain stable in response to mild sensory stimuli in mice22, while a marked reduction in ATP levels is observed during epileptic seizure activity3.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [3]
Brain energy dynamics are not merely passive reflections of neuronal activity but can diverge from it in a state-dependent manner across behavioral states.
“In this study, we demonstrate that brain energy dynamics are not merely passive reflections of neuronal activity3, but can diverge from it in a state-dependent manner across behavioral states.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [3]
A previous study on epileptic seizures found no clear correlation between seizure duration and the magnitude of ATP reduction.
“Moreover, our previous study on epileptic seizures found no clear correlation between seizure duration (a proxy for total firing) and the magnitude of ATP reduction3, suggesting that firing-driven ATPase activity is unlikely to primarily account for the observed ATP decrease.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [3]
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Energy paradox in REM sleep: balancing supply and consumption in brain metabolism
Takahashi, Y., Ikoma, Y., & Matsui, K. (2026) · Communications Biology · doi:10.1038/s42003-026-10646-6 · Cited by 1 · see citing works
“Moreover, our previous study on epileptic seizures found no clear correlation between seizure duration (a proxy for total fi ring) and the magnitude of ATP reduction 3 , suggesting that fi ring-driven ATPase activity is unlikely to primarily account for the observed ATP decrease.”
InfluentialSelf-citation
- Authors
- Furukawa, K., Ikoma, Y., Niino, Y., Hiraoka, Y., Tanaka, K., Miyawaki, A., Hirrlinger, J., & Matsui, K.
- Affiliations
- Tohoku University (JP)
- RIKEN Center for Brain Science (JP)
- Tokyo Institute of Technology (JP)
- Max Planck Institute for Multidisciplinary Sciences (DE)
- Corresponding author
- Matsui, Ko
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 2025-03
- Volume
- 169
- Issue
- 3
- Pages
- e70044-e70044
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- PMC
- PMC11923518
- OpenAlex
- W4408676381
- Cited by
- 11
- References
- 62
- Citations by year
- 2026: 5 · 2025: 6
- FWCI
- 7.37
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neurochemistry (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- Japan Society for the Promotion of Science (15H05948, 18H05110, 19H03338, 20H05046, 20H05896, 22H02713, 22K15218, 23H04659, 24K18234)
- Japan Agency for Medical Research and Development (Brain/MINDS,JP15dm0207001)
- Uehara Memorial Foundation
- Takeda Science Foundation
- Research Foundation for Opto-Science and Technology
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
- Keywords
- epilepsy, epileptic seizures, neuronal hyperactivity, cytosolic ATP, astrocytes, pyruvate, energy metabolism, hippocampus, transgenic mice, fiber photometry
- MeSH terms
- Adenosine Triphosphate, Animals, Astrocytes, Cytosol, Energy Metabolism, Epilepsy, Hippocampus, Mice, Inbred C57BL, Mice, Transgenic, Neurons, Pyruvic Acid, Fluorescence Resonance Energy Transfer, Mice
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