The role of spiking local interneurons in shaping the receptive fields of intersegmental interneurons in the locust

Abstract

Intracellular recordings were made simultaneously from pairs of spiking local and intersegmental interneurons in the mesothoracic ganglion of the locust Schistocerca gregaria (Forskal). The spiking local interneurons belong to a midline group, and the intersegmental interneurons to a lateral-posterior population that projects ipsilaterally to the metathoracic ganglion. Both respond to mechanosensory inputs from one middle leg. The receptive fields of both types of interneurons were plotted and the contribution of the local interneurons to the shaping of the receptive fields of the intersegmental interneurons was studied. The spiking local interneurons are excited by specific arrays of exteroreceptors and proprioceptors of one leg. They make inhibitory connections with specific intersegmental interneurons which thus have corresponding inhibitory regions to their receptive fields. For example, inhibition from local interneurons with inputs from hairs or campaniform sensilla on the tarsus could sharpen the boundaries of the excitatory receptive field of an intersegmental interneuron by lateral inhibition. Inhibition from local interneurons with inputs from joint proprioceptors suppresses the excitation of an intersegmental interneuron during the antipreferred direction of movement. Rapid alternate movements about one joint can in this way be signaled by an intersegmental interneuron in a phase-locked manner. Certain intersegmental interneurons are excited by exteroreceptive inputs and inhibited by proprioceptive signals, or vice versa. The inhibition could become significant during walking, where the excitatory and inhibitory inputs to an interneuron are likely to be evoked during the different phases of a step cycle. The inhibitory regions of the receptive field of an intersegmental interneuron have never been found to be smaller than the excitatory regions of the receptive field of a presynaptic local interneuron and can result from converging inhibitory inputs from several spiking local interneurons. The inhibitory connections are highly specific: Several local interneurons may be excited by a particular stimulus that also inhibits an intersegmental interneuron, but only a small proportion of the former are the cause of the inhibition in the intersegmental interneuron.