Local brain environment changes associated with epileptogenesis
Abstract
Plastic change of the neuronal system has traditionally been assumed to be governed primarily by the long-term potentiation/depression mechanisms of synaptic transmission. However, a rather simple shift in the ambient ion, transmitter and metabolite concentrations could have a pivotal role in generating plasticity upon the physiological process of learning and memory. Local brain environment and metabolic changes could also be the cause and consequences of the pathogenesis leading to epilepsy. Governing of the local brain environment is the primal function of astrocytes. The metabolic state of the entire brain is strongly linked to the activity of the lateral hypothalamus. In this study, plastic change of astrocyte reactions in the lateral hypothalamus was examined using epileptogenesis as an extreme form of plasticity. Fluorescent sensors for calcium or pH expressed in astrocytes were examined for up to one week by in vivo fibre photometry in freely moving transgenic male mice. Optical fluctuations on a timescale of seconds is difficult to assess because these signals are heavily influenced by local brain blood volume changes and pH changes. Using a newly devised method for the analysis of the optical signals, changes in Ca2+ and pH in astrocytes and changes in local brain blood volume associated with hippocampal-stimulated epileptic seizures were extracted. Following a transient alkaline shift in the astrocyte triggered by neuronal hyperactivity, a prominent acidic shift appeared in response to intensified seizure which developed with kindling. The acidic shift was unexpected as transient increase in local brain blood volume was observed in response to intensified seizures, which should lead to efficient extrusion of the acidic CO2. The acidic shift could be a result of glutamate transporter activity and/or due to the increased metabolic load of astrocytes leading to increased CO2 and lactate production. This acidic shift may trigger additional gliotransmitter release from astrocytes leading to the exacerbation of epilepsy. As all cellular enzymic reactions are influenced by Ca2+ and pH, changes in these parameters could also have an impact on the neuronal circuit activity. Thus, controlling the astrocyte pH and/or Ca2+ could be a new therapeutic target for treatment of epilepsy or prevention of undesired plasticity associated with epileptogenesis.
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Fluorescence emitted from parenchymal cells is attenuated by overlying blood vessels, which appear as shadows in wide-field images.
“Our earlier studies showed that fluorescence emitted from parenchymal cells is attenuated by overlying blood vessels, which therefore appear as shadows in wide-field images2,4,36.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [36]
Violet to yellow excitation and emission light are well absorbed by blood within the vasculature, so blood vessels lacking fluorescent proteins appear as dark shadows when fluorescent proteins are diffusely expressed in brain cells.
“Violet to yellow excitation and emission light are well absorbed by the blood within the vasculature. Therefore, when fluorescent proteins are diffusely expressed in brain cells, blood vessels that lack these proteins appear as dark shadows36,37.”
From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [36]
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Self-citationReviewer #1 (Public Review): Plastic vasomotion entrainment
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Reviewer #3 (Public Review): Plastic vasomotion entrainment
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Author Response: Plastic vasomotion entrainment
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Wang, L., Liu, Y., Ding, W., Yang, M., Liu, Q., & Xu, F. (2025) · CNS Neuroscience & Therapeutics · doi:10.1002/cns.70686
Maity, S., & Remya, P. N. (2026) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2026.108543
Vagal nerve stimulation induces vascular oscillations and enhances long-term learning
Chen, J. U., Ikoma, Y., & Matsui, K. (2026) · iScience · doi:10.1016/j.isci.2026.117413
Self-citation
- Authors
- Ikoma, Y., Sasaki, D., & Matsui, K.
- Affiliations
- Tohoku University (JP)
- Corresponding author
- Matsui, Ko
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2022-11-25
- Volume
- 146
- Issue
- 2
- Pages
- 576-586
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W4310055704
- Cited by
- 26
- References
- 68
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 12 · 2023: 5
- FWCI
- 3.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Grant-in-Aid for Transformative Research Areas (20H05896, 20H05046, 22H02713, 22K15218)
- Research Foundation for Opto-Science and Technology
- NOVARTIS Foundation
- Promotion of Science
- Takeda Science Foundation
- 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 › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- epileptogenesis, astrocytes, lateral hypothalamus, kindling, epileptic seizures, glutamate transporters, gliotransmitter release, lactic acid production, epilepsy treatment
- MeSH terms
- Animals, Astrocytes, Brain, Calcium, Carbon Dioxide, Epilepsy, Male, Seizures, Mice
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