Impaired mitochondrial function abolishes gamma oscillations in the hippocampus through an effect on fast-spiking interneurons
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Sir, Synchronous neuronal oscillations in the gamma frequency band (30–80 Hz) are implicated in a wide range of cognitive processes, including memory formation (Varela et al., 2001) and sensory processing (Singer, 1993; Gray, 1994). This rapid, temporally co-ordinated activity in spatially distributed areas of cortex is highly energy dependent, producing large changes in blood-oxygen level dependent signals in vivo and showing exquisite sensitivity to hypoxia in vitro (Huchzermeyer, 2008). Gamma oscillations are generated by reciprocal excitation and inhibition in networks of electrically coupled pyramidal cells and GABAergic interneurons (Fisahn et al., 1998; Cunningham et al., 2003; Hájos et al., 2004). Synchronous firing of networks of basket-cell interneurons at gamma frequency produces phasic inhibition of pyramidal cells, the periods when this inhibition is minimal, providing temporal windows for pyramidal cell firing. Pyramidal cell firing in turn provides reciprocal tonic excitation onto interneurons, allowing the cycle to continue (Traub et al., 1996). The research article by Kann et al. (2011) demonstrates the critical dependence of gamma oscillations upon mitochondrial function. However, little is known about the relative energetic requirements of the different cellular components of this network. We have addressed this issue with intracellular recordings of pyramidal cells and interneurons undergoing gamma oscillations under conditions of metabolic stress in vitro. Rat hippocampal slices (450 μm horizontal sections) were maintained in a recording chamber at the interface between 95% oxygen/5% CO2 and artificial CSF (in mM: 10 glucose, 126 NaCl, 3 KCl, 24 NaHCO3, 1.25 NaH2PO4, 2 MgSO4 and 2 CaCl2). Stable gamma oscillation was induced by adding low dose (100 nM) kainic acid to the perfusate. Local field potential recordings were made from the stratum pyramidale layer in CA3 region of the hippocampus using glass microelectrodes (10–300 Hz band-pass filtered, digitized at 10 kHz). We also performed simultaneous intracellular recordings from CA3 pyramidal cells using sharp microelectrodes (70–130 MΩ) containing 2 M potassium acetate. Cells were recorded in current clamp mode, and identified electrophysiologically on the basis of their low resting firing rate, accommodating response to sustained depolarization and gamma frequency phasic inhibitory post-synaptic potentials. Excitatory post-synaptic potentials (EPSPs) and inhibitory post-synaptic potentials (IPSPs) were recorded at −70 and −20 mV, respectively. We then measured the effect on gamma oscillation power and corresponding intracellular activity using a variety of mitochondrial respiratory chain inhibitors. Potassium cyanide (KCN; 100 μM), an inhibitor of cytochrome oxidase in complex IV of the mitochondrial respiratory chain, caused a 72.1% reduction in gamma power (1221.3 ± 207.8 μV2 control versus 340.8 ± 70.5 μV2 KCN, n = 9, P < 0.05; Fig. 1A(i)) within 15 min. There was no significant change in the resting membrane potential (−57.9 ± 1.29 mV versus −60.6 ± 2.05 mV KCN, P > 0.05; Fig. 1A(ii)) of pyramidal cells. Despite this, there was a marked reduction in pyramidal cell firing rate during the concurrently recorded gamma frequency oscillation (3.02 ± 0.70 Hz versus 1.43 ± 0.64 Hz KCN, n = 9, P < 0.05). We therefore examined the synaptic inputs to pyramidal cells. There was no significant change in excitatory input (mean EPSP amplitude 3.18 ± 0.70 mV control versus 2.43 ± 0.72 mV KCN, P > 0.05; mean EPSP frequency 12.4 ± 2.6 Hz control versus 11.9 ± 1.9 Hz KCN, P > 0.05). The mean IPSP amplitude was reduced, (6.80 ± 1.66 mV control versus 5.21 ± 0.74 mV KCN, P < 0.05); however, the most striking finding was a marked reduction in the frequency of IPSPs impinging on the pyramidal cells (32.4 ± 2.6 Hz control versus 26.2 ± 3.9 Hz KCN, P < 0.05; Fig. 1A(iv)). We found similar effects on pyramidal cell firing and synaptic inputs using 1 μM Rotenone, an inhibitor of complex I, and 1 μM FCCP, a protonophore that discharges the mitochondrial membrane electrochemical gradient. With all three inhibitors, gamma power and pyramidal cell function returned to control levels on washing out of the inhibitors. (A) (i) Local field potential recording, CA3 region of hippocampus. Low dose (100 μM) KCN significantly reduces gamma oscillation power. Scale bar: horizontal 100 ms, vertical 200 μV. (ii) Simultaneous intracellular recording, CA3 stratum pyramidale pyramidal cell. KCN causes reduced resting firing rate with no significant change in resting membrane potential. (iii) Inhibitory post-synaptic potentials recorded at −20 mV. Scale bar: horizontal 50 ms, vertical 2 mV. (iv) Inter-event intervals of IPSPs impinging on pyramidal neuron. Mean frequency of IPSPs declines significantly. (B) (i) CA3 stratum pyramidale interneurons show rapid resting firing rates, (ii) show little accommodation to sustained depolarization, (iii) fire in phase with gamma field p
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The energy demands of PV-INs make them highly susceptible to loss of mitochondrial membrane potential and to metabolic and oxidative stress that accompanies disease states.
“The energy requirements of PV-INs make them highly susceptible to the loss of mitochondrial membrane potential (a component of, and a proxy for, a decrease in mitochondrial function), and to metabolic and oxidative stress that accompanies disease states [81,91].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [91]
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In vitro modelling of the neuropathophysiological features of mitochondrial epilepsy
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- Authors
- Whittaker, R. G., Turnbull, D. M., Whittington, M. A., & Cunningham, M. O.
- Affiliations
- Newcastle University (GB)
- Corresponding author
- Cunningham, M. O.
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-03-04
- Volume
- 134
- Issue
- 7
- Pages
- e180-e180
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3708717
- OpenAlex
- W2133255336
- Cited by
- 74
- References
- 16
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 7 · 2023: 9 · 2022: 5 · 2021: 5 · 2020: 5 · 2019: 6 · 2018: 5 · 2017: 2 · 2016: 4 · 2015: 5 · 2014: 3 · 2013: 3 · 2012: 1
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Brain (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- National Institute for Health and Care Research (NF-SI-0510-10187)
- European Commission
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- gamma oscillations, mitochondrial function, fast-spiking interneurons, hippocampus, CA3 pyramidal cells, metabolic stress, energy metabolism, kainic acid, local field potentials, intracellular recording, GABAergic interneurons, hypoxia, rat hippocampal slices
- MeSH terms
- Action Potentials, Animals, Hippocampus, Interneurons, Mitochondrial Diseases, Brain Waves
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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