Nonspiking local interneurons in insect leg motor control. II. Role of nonspiking local interneurons in the control of leg swing during walking.

1. Nonspiking local interneurons (NSIs) were recorded intracellularly in the mesothoracic ganglion of semi-intact locusts walking on a treadwheel. Interneurons were characterized by their connectivity to motoneurons. Their activity patterns in the step cycle and the effect current injection had on the leg movement were analyzed. We examined interneurons that provided excitatory or inhibitory synaptic drive to a subset of motoneurons active during the swing movement of walking. 2. Interneuron activity was observed to support or oppose the actual leg movement. Both supporting and opposing interneurons were active simultaneously, lending support to the idea that the actual motor output of walking is generated by the adjustment of parallel antagonistic pathways of signal processing. 3. The examined interneurons showed qualitatively the same patterns of activity during forward and backward walking. This indicates that swing movement in both situations may be generated by similar neuronal networks (although the mechanism of movement reversal remains unclear). 4. At least two functional types of NSIs could be distinguished. First, there were interneurons whose depolarization patterns showed distinct variability, often correlated with duration or amplitude of the swing movement. As a rule, current injection had minor, if any, effects on leg movement. Populations of these interneurons appear to be involved in the control of a coordinated swing movement by driving appropriate sets of muscle groups. The second type of NSIs showed more stereotyped activity patterns that varied relatively little with changes in the swing movement. Current injection had strong effects on the leg movement and could, for example, arrest the leg in the stance phase. These interneurons appear to be primarily involved in the trigger mechanism of leg swing.