Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. II. Oscillatory properties of pyloric neurons

In three preceding papers in this series (6, 33, 45), the functional roles, intrinsic cellular properties, and synaptic connections of identified neurons in the lobster stomatogastric ganglion were investigated using the dye-sensitized photoinactivation technique. In this paper, we investigate the network properties of the pyloric system. 2. The relative strengths of the synaptic interactions between all possible motor neuron pairs were measured from the neuronal cell bodies. 3. Experiments were performed to determine the minimal subset of the pyloric neurons that could generate rhythmic activity due to network interactions alone. With the endogenously bursting anterior burster (AB) cell excluded from consideration, the minimum number of elements was found to be two. These two elements behaved as a classical "half-center" oscillator when their overall activity levels were appropriately adjusted. 4. Two cells in the commissural ganglia supply the pyloric system with rhythmic excitatory input phase locked to ongoing pyloric activity. The rhythmicity of that input is shown to be functionally irrelevant. The inputs can exert their effects on pyloric system activity through tonic firing. 5. A qualitative explanation of three important aspects of the pyloric motor pattern is presented, based on the intrinsic properties of pyloric neurons and the systematic properties of the network they form. The existence of the pattern results from oscillatory membrane properties of the individual neurons in combination with the multiple reciprocally inhibitory interactions within the network. The phase relationships derive from the synaptic connectivity and depend on relative synaptic strengths, postinhibitory rebound, rebound delay, and the kinetics of the plateau and bursting pacemaker-potential generation mechanisms. The overall pattern frequency is determined by the AB interneuron via its intrinsic oscillatory behavior and strong synapses with the rest of the pyloric neurons.