Modulation of a Neural Network by Physiological Levels of Oxygen in Lobster Stomatogastric Ganglion

Abstract

Although a large body of literature has been devoted to the role of O2 in the CNS, how neural networks function during long-term exposures to low but physiological O2 partial pressure (PO2) has never been studied. We addressed this issue in crustaceans, where arterial blood PO2 is set in the 1-3 kPa range, a level that is similar to the most frequently measured tissue PO2 in the vertebrate CNS. We demonstrate that over its physiological range, O2 can reversibly modify the activity of the pyloric network in the lobster Homarus gammarus. This network is composed of 12 identified neurons that spontaneously generate a triphasic rhythmic motor output in vitro as well as in vivo. When PO2 decreased from 20 to 1 kPa, the pyloric cycle period increased by 30-40%, and the neuronal pattern was modified. These effects were all dose- and state-dependent. Specifically, we found that the single lateral pyloric (LP) neuron was responsible for the O2-mediated changes. At low PO2, the LP burst duration increased without change in its intraburst firing frequency. Because LP inhibits the pyloric pacemaker neurons, the increased LP burst duration delayed the onset of each rhythmic pacemaker burst, thereby reducing significantly the cycling frequency. When we deleted LP, the network was no longer O2-sensitive. In conclusion, we propose that (1) O2 has specific neuromodulator-like actions in the CNS and that (2) the physiological role of this reduction of activity and energy expenditure could be a key adaptation for tolerating low but physiological PO2 in sensitive neural networks.