The brain has a high energy demand and critically depends on oxidative phosphorylation in mitochondria. However, little is known about energy utilization during different activity states of neuronal networks. We addressed this issue in subfield CA3 of organotypic hippocampal slice cultures under well-defined recording conditions using a 20% O₂ gas mixture. We combined recordings of local field potential (LFP) and interstitial partial oxygen pressure (pO₂) during three different activity states, namely (i) gamma oscillations (30-100 Hz) as induced by cholinergic receptor activation, (ii) spontaneous network activity, and (iii) absence of spiking (action potentials). Oxygen consumption rates were estimated by pO₂ depth profiles with high spatial resolution and a mathematical model that considers convective transport, diffusion and activity-dependent consumption of oxygen. We demonstrate: (1) Relative oxygen consumption during gamma oscillations was 2.2-fold and 5.3-fold higher compared to spontaneous activity and absence of spiking, respectively. (2) Gamma oscillations were associated with a similar large drop in pO₂ as observed previously with a 95% O₂ gas mixture. (3) Sufficient tissue oxygenation during gamma oscillations in vivo is ensured by the calculated critical radius of 30-40 µm around a capillary. We conclude that the structural and biophysical features of brain tissue permit variations in local oxygen consumption by a factor of about five.