Encoding of near-range spatial information by descending interneurons in the stick insect antennal mechanosensory pathway

Abstract

Much like mammals use their whiskers, insects use their antennae for tactile near-range orientation during locomotion. Stick insects rapidly transfer spatial information about antennal touch location to the front legs, allowing for aimed reach-to-grasp movements. This adaptive behavior requires a spatial coordinate transformation from "antennal contact space" to "leg posture space." Therefore, a neural pathway must convey proprioceptive and tactile information about antennal posture and contact site to thoracic motor networks. Here we analyze proprioceptive encoding properties of descending interneurons (DINs) that convey information about antennal posture and movement to the thoracic ganglia. On the basis of response properties of 110 DINs to imposed movement of the distal antennal joint, we distinguish five functional DIN groups according to their sensitivity to three parameters: movement direction, movement velocity, and antennal joint angle. These groups are simple position-sensitive DINs, which signal the antennal joint angle; dynamic position-sensitive DINs, which signal the joint angle with strong dependence on movement; unspecific movement-sensitive DINs, which signal movement but not the velocity, position, or direction of movement; and ON- and OFF-type velocity-sensitive DINs. The activity of the latter two groups is increased/attenuated during antennal movement, with the spike rate increasing/decreasing linearly with antennal joint angle velocity. Some movement-sensitive DINs convey spikes to the thorax within 11 ms, suggesting a rapid, direct pathway from antennal mechanosensory to thoracic motor networks. We discuss how the population of DINs could provide the neural basis for the intersegmental spatial coordinate transfer between a touch sensor of the head and thoracic motor networks.