Local oxygen homeostasis during various neuronal network activity states in the mouse hippocampus

• Verfasst von: Schneider, Justus [VerfasserIn]
• Verfasst von: Papageorgiou, Ismini E. [VerfasserIn]
• Verfasst von: Maurer, Jana [VerfasserIn]
• Verfasst von: Both, Martin [VerfasserIn]
• Verfasst von: Draguhn, Andreas [VerfasserIn]
• Verfasst von: Kann, Oliver [VerfasserIn]
• Titel: Local oxygen homeostasis during various neuronal network activity states in the mouse hippocampus
• Verf.angabe: Justus Schneider, Nikolaus Berndt, Ismini E Papageorgiou, Jana Maurer, Sascha Bulik, Martin Both, Andreas Draguhn, Hermann-Georg Holzhütter and Oliver Kann
• Jahr: 2017
• Umfang: 15 S.
• Fussnoten: First published November 3, 2017 ; Gesehen am 26.06.2018
• Titel Quelle: Enthalten in: Journal of cerebral blood flow & metabolism
• Ort Quelle: Thousands Oaks, Calif. : Sage, 1981
• Jahr Quelle: 2019
• Band/Heft Quelle: 39(2019), 5, Seite 859-873
• ISSN Quelle: 1559-7016
• DOI: doi:10.1177/0271678X17740091
• Datenträger: Online-Ressource
• Sprache: eng
• K10plus-PPN: 1576859940

Abstract

Cortical information processing comprises various activity states emerging from timed synaptic excitation and inhibition. However, the underlying energy metabolism is widely unknown. We determined the cerebral metabolic rate of oxygen (CMRO2) along a tissue depth of <0.3 mm in the hippocampal CA3 region during various network activities, including gamma oscillations and sharp wave-ripples that occur during wakefulness and sleep. These physiological states associate with sensory perception and memory formation, and critically depend on perisomatic GABA inhibition. Moreover, we modelled vascular oxygen delivery based on quantitative microvasculature analysis. (1) Local CMRO2 was highest during gamma oscillations (3.4 mM/min), medium during sharp wave-ripples, asynchronous activity and isoflurane application (2.0-1.6 mM/min), and lowest during tetrodotoxin application (1.4 mM/min). (2) Energy expenditure of axonal and synaptic signaling accounted for >50% during gamma oscillations. (3) CMRO2 positively correlated with number and synchronisation of activated synapses, and neural multi-unit activity. (4) The median capillary distance was 44 µm. (5) The vascular oxygen partial pressure of 33 mmHg was needed to sustain oxidative phosphorylation during gamma oscillations. We conclude that gamma oscillations featuring high energetics require a hemodynamic response to match oxygen consumption of respiring mitochondria, and that perisomatic inhibition significantly contributes to the brain energy budget., Cortical information processing comprises various activity states emerging from timed synaptic excitation and inhibition. However, the underlying energy metabolism is widely unknown. We determined the cerebral metabolic rate of oxygen (CMRO2) along a tissue depth of <0.3 mm in the hippocampal CA3 region during various network activities, including gamma oscillations and sharp wave-ripples that occur during wakefulness and sleep. These physiological states associate with sensory perception and memory formation, and critically depend on perisomatic GABA inhibition. Moreover, we modelled vascular oxygen delivery based on quantitative microvasculature analysis. (1) Local CMRO2 was highest during gamma oscillations (3.4 mM/min), medium during sharp wave-ripples, asynchronous activity and isoflurane application (2.0-1.6 mM/min), and lowest during tetrodotoxin application (1.4 mM/min). (2) Energy expenditure of axonal and synaptic signaling accounted for >50% during gamma oscillations. (3) CMRO2 positively correlated with number and synchronisation of activated synapses, and neural multi-unit activity. (4) The median capillary distance was 44 µm. (5) The vascular oxygen partial pressure of 33 mmHg was needed to sustain oxidative phosphorylation during gamma oscillations. We conclude that gamma oscillations featuring high energetics require a hemodynamic response to match oxygen consumption of respiring mitochondria, and that perisomatic inhibition significantly contributes to the brain energy budget.