Synaptic Dynamics Do Not Determine Proper Phase of Activity in a Central Pattern Generator

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Abstract
Rhythmic motor activity often requires neuronal output to the muscles to arrive in a particular sequence. At the pattern-generator level, this requires distinct activity phases in different groups of constituent neurons. The phase differences between rhythmically active neurons in a network are thought to arise from the interplay between their intrinsic properties and the temporal dynamics of synapses among these neurons. In the rhythmically active pyloric network of the lobster Panulirus interruptus, synaptic connections from the pacemaker ensemble to the follower neurons [lateral pyloric (LP) and pyloric constrictor (PY)] are thought to be primarily responsible for the proper phase of activity (pacemaker–LP–PY) across all frequencies (0.5–2 Hz) of the pyloric rhythm. We test this hypothesis by characterizing the synapses from the pacemaker ensemble to the LP and PY neurons. Paired comparisons show that these two synapses are not significantly different in strength or in the extent of short-term depression. To examine the level to which intrinsic properties of the follower neurons determine their relative activity phase, we block all chemical synapses within the network and drive the LP and PY neurons rhythmically using artificial synaptic currents with identical strength and dynamics implemented with the dynamic-clamp technique. In response to these identical synaptic inputs, the LP and PY neurons maintain the proper relative phase of activity. These results strongly indicate that the relative phase of activity among these follower neurons within the pyloric network is not dictated by their synaptic inputs but is solely determined by their distinct intrinsic properties.