A Direct Descending Pathway Informing Locomotor Networks about Tactile Sensor Movement

Abstract

Much like visually impaired humans use a white-cane, nocturnal insects and mammals use antennae or whiskers for near-range orientation. Stick insects, for example, rely heavily on antennal tactile cues to find footholds and detect obstacles. Antennal contacts can even induce aimed reaching movements. Because tactile sensors are essentially one-dimensional, they must be moved to probe the surrounding space. Sensor movement is thus an essential cue for tactile sensing, which needs to be integrated by thoracic networks for generating appropriate adaptive leg movements. Based on single and double recordings, we describe a descending neural pathway comprising three identified ON-and OFF-type neurons that convey complementary, unambiguous, and short-latency information about antennal movement to thoracic networks in the stick insect. The neurons are sensitive to the velocity of antennal movements across the entire range covered by natural movements, regardless of movement direction and joint angle. Intriguingly, none of them originates from the brain. Instead, they descend from the gnathal ganglion and receive input from antennal mechanoreceptors in this lower region of the CNS. From there, they convey information about antennal movement to the thorax. One of the descending neurons, which is additionally sensitive to substrate vibration, feeds this information back to the brain via an ascending branch. We conclude that descending interneurons with complementary tuning characteristics, gains, input and output regions convey detailed information about antennal movement to thoracic networks. This pathway bypasses higher processing centers in the brain and thus constitutes a shortcut between tactile sensors on the head and the thorax.

A Computational Model of a Descending Mechanosensory Pathway Involved in Active Tactile Sensing

“…This suggests that that there are only few individual OFF-type DINs per antenna. This is also supported by the DIN morphology because, so far, only a single morphological type of OFF-type DIN was identified [ 17 ]. Assuming only a single OFF-type DIN on each side of the CNS, the sensitivity of the DIN could either differ between animals, or with dependence on the animal’s state during the recording.…”

“…Therefore, antennal hair fields are involved in the local coordination of antennal joints and the descending control of locomotion. Moreover, afferents from antennal hair fields overlap with DIN dendrites in the brain and gnathal ganglion [ 23 ], where they are likely to provide direct input to at least some DINs [ 17 ]. Therefore, a major objective of our study was to test how much of the DIN response properties could be explained with antennal hair fields providing their only afferent input.…”

“…However, hair field afferents and ON-type velocity-sensitive DINs overlap morphologically in the gnathal ganglion (or suboesophageal ganglion), suggesting they could be directly connected. This is also supported by the short delays of the velocity-sensitive DIN responses, which forward spikes to the thorax within 11 ms after antennal stimulation [ 16 , 17 ]. Nonetheless, it is possible that an interneuron might be interspersed between antennal mechanosensory afferents and DINs.…”

“…The DIN models simulate the multivariate information transfer from an active touch system to a motor control system. For three reasons, we choose the antennal mechanosensitive pathway of the stick insect Carausius morosus as the paragon for our model: i) A behavioural reach-to-grasp paradigm in stick insects [ 5 ] requires fast information transfer of antennal posture and movement; ii) both the antennal tactile system [ 12 , 13 ] and the thoracic leg motor control networks [ 14 , 15 ] are well studied; and iii) a population of spiking DINs has been described that conveys diverse, multivariate information about antennal posture and movement to thoracic neural networks [ 16 ]; [ 17 ]. Our objective was to devise models of several different DIN types, including position- and motion-sensitive DINs, drawing from a small set of computational modules such as linear filters and a noisy spike generator.…”

Spatial Navigation and the Central Complex: Sensory Acquisition, Orientation, and Motor Control

“…In stick insects, gap crossing behavior is initiated when the antennae detect a gap in the substrate they are walking on and are further guided by searching front leg movements (Bläesing and Cruse, 2004). Leg movements associated with turning in the stick insect are also guided by antennal contact (Dürr et al, 2001; Dürr and Ebeling, 2005), through descending pathways from the brain to the thoracic ganglia (Ache et al, 2015). The descending pathways bypass higher processing areas such as the CX.…”