Gamma oscillations in the hippocampus require high complex I gene expression and strong functional performance of mitochondria
Abstract
Fast neuronal network oscillations in the gamma range (~30-90 Hz) have been implicated in complex brain functions such as sensory processing, memory formation and, perhaps, consciousness, and appear to be exceptionally vulnerable to various pathologies. However, both energy demand and mitochondrial performance underlying gamma oscillations are unknown. We investigated the fundamental relationship between acetylcholine-induced gamma oscillations, mitochondrial gene expression and oxidative metabolism in hippocampal slice preparations of mouse and rat by applying electrophysiology, in situ hybridization, quantitative polymerase chain reaction, oxygen sensor microelectrode (interstitial partial oxygen pressure) and imaging of mitochondrial redox state [nicotinamide adenine dinucleotide (phosphate) and flavin adenine dinucleotide fluorescence]. We show that (i) gamma oscillation power, oxygen consumption and expression of complex I (nicotinamide adenine dinucleotide:ubiquinone oxidoreductase) subunits are higher in hippocampal subfield CA3 than in CA1 and dentate gyrus; (ii) the amount of oxygen consumption of gamma oscillations reaches that of seizure-like events; (iii) gamma oscillations are exquisitely sensitive to pharmacological complex I inhibition; and (iv) gamma oscillations utilize mitochondrial oxidative capacity near limit. These data suggest that gamma oscillations are especially energy demanding and require both high complex I expression and strong functional performance of mitochondria. Our study helps to explain the exceptional vulnerability of complex brain functions in ischaemia as well as in neurodegenerative and psychiatric disorders that are associated with mitochondrial dysfunction.
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The large amounts of ATP needed to sustain gamma oscillations are supplied by a high density of mitochondria.
“The large amounts of ATP needed to sustain gamma oscillations are supplied by a high density of mitochondria [81][82][83].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [83]
The rate of oxygen consumption during hippocampal gamma oscillations can equal the rate during a seizure.
“Studies have shown that the rate of oxygen consumption during hippocampal gamma oscillations can be equivalent to the rate of oxygen spent during a seizure [83,84].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [83]
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- Authors
- Kann, O., Huchzermeyer, C., Kovács, R., Wirtz, S., & Schuelke, M.
- Affiliations
- Heidelberg University (DE)
- Charité – Universitätsmedizin Berlin (DE)
- Stiftung Charité (DE)
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-12-22
- Volume
- 134
- Issue
- 2
- Pages
- 345-358
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2100518016
- Cited by
- 189
- References
- 67
- Citations by year
- 2026: 10 · 2025: 10 · 2024: 8 · 2023: 13 · 2022: 15 · 2021: 13 · 2020: 14 · 2019: 15 · 2018: 10 · 2017: 9 · 2016: 15 · 2015: 14 · 2014: 14 · 2013: 7 · 2012: 11
- FWCI
- 5.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- gamma oscillations, hippocampus, complex I, mitochondrial gene expression, mitochondrial oxidative metabolism, oxygen consumption, acetylcholine, CA3, mitochondrial redox state, mitochondrial complex I inhibition, energy demand, seizure-like events, mitochondrial dysfunction
- MeSH terms
- Acetylcholine, Animals, Hippocampus, Mice, Inbred C57BL, Mitochondria, Oxidation-Reduction, Oxygen Consumption, Gene Expression, Rats, Wistar, Electron Transport Complex I, Mice, Rats, Brain Waves, In Vitro Techniques
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