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Metabolic modulation of neuronal gamma-band oscillations

  • Neuroscience
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Abstract

Gamma oscillations (30–100 Hz) represent a physiological fast brain rhythm that occurs in many cortex areas in awake mammals, including humans. They associate with sensory perception, voluntary movement, and memory formation and require precise synaptic transmission between excitatory glutamatergic neurons and inhibitory GABAergic interneurons such as parvalbumin-positive basket cells. Notably, gamma oscillations are exquisitely sensitive to shortage in glucose and oxygen supply (metabolic stress), with devastating consequences for higher cognitive functions. Herein, we explored the robustness of gamma oscillations against changes in the availability of alternative energy substrates and amino acids, which is partially regulated by glial cells such as astrocytes. We used organotypic slice cultures of the rat hippocampus expressing acetylcholine-induced persistent gamma oscillations under normoxic recording conditions (20% oxygen fraction). Our main findings are (1) partial substitution of glucose with pyruvate and the ketone body β-hydroxybutyrate increases the frequency of gamma oscillations, even at different stages of neuronal tissue development. (2) Supplementation with the astrocytic neurotransmitter precursor glutamine has no effect on the properties of gamma oscillations. (3) Supplementation with glycine increases power, frequency, and inner coherence of gamma oscillations in a dose-dependent manner. (4) During these treatments switches to other frequency bands or pathological network states such as neural burst firing or synchronized epileptic activity are absent. Our study indicates that cholinergic gamma oscillations show general robustness against these changes in nutrient and amino acid composition of the cerebrospinal fluid; however, modulation of their properties may impact on cortical information processing under physiological and pathophysiological conditions.

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Acknowledgements

The authors thank Hasan Onur Dikmen for critical reading of the manuscript and helpful discussion.

Funding

This work was supported by the Deutsche Forschungsgemeinschaft within the Collaborative Research Center 1134 (project B02).

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Authors and Affiliations

  1. Institute of Physiology and Pathophysiology, University of Heidelberg, Im Neuenheimer Feld 326, 69120, Heidelberg, Germany

    Wadim Vodovozov, Justus Schneider, Shehabeldin Elzoheiry, Jan-Oliver Hollnagel, Andrea Lewen & Oliver Kann

  2. Interdisciplinary Center for Neurosciences (IZN), University of Heidelberg, 69120, Heidelberg, Germany

    Oliver Kann

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  1. Wadim Vodovozov
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WV, JS, and OK designed the research; WV, JS, SE, JOH, and AL performed the research; WV, JS, SE, JOH, and AL analyzed the data; WV and OK wrote the manuscript. All authors have approved the final version of the manuscript and agree to be accountable for all aspects of the work.

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Correspondence to Oliver Kann.

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Vodovozov, W., Schneider, J., Elzoheiry, S. et al. Metabolic modulation of neuronal gamma-band oscillations. Pflugers Arch - Eur J Physiol 470, 1377–1389 (2018). https://doi.org/10.1007/s00424-018-2156-6

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