Temporal differences between load and movement signal integration in the sensorimotor network of an insect leg.

Abstract

Nervous systems face a torrent of sensory inputs, including proprioceptive feedback. Signal integration depends on spatially and temporally coinciding signals. It is unclear how relative time delays affect multimodal signal integration from spatially distant sense organs. We measured transmission times and latencies along all processing stages of sensorimotor pathways in the stick insect leg muscle control system, using intra- and extracellular recordings. Transmission times of signals from load-sensing tibial and trochanterofemoral campaniform sensilla (tiCS, tr/fCS) to the premotor network were longer than from the movement-sensing femoral chordotonal organ (fCO). We characterized connectivity patterns from tiCS, tr/fCS, and fCO afferents to identified premotor nonspiking interneurons (NSIs) and motor neurons (MNs) by distinguishing short- and long-latency responses to sensory stimuli. Functional NSI connectivity depended on sensory context. The timeline of multisensory integration in the NSI network showed an early phase of movement signal processing and a delayed phase of load signal integration. The temporal delay of load signals relative to movement feedback persisted into MN activity and muscle force development. We demonstrate differential delays in the processing of two distinct sensory modalities generated by the sensorimotor network and affecting motor output. The reported temporal differences in sensory processing and signal integration improve our understanding of sensory network computation and function in motor control.NEW & NOTEWORTHY Networks integrating multisensory input face the challenge of not only spatial but also temporal integration. In the local network controlling insect leg movements, proprioceptive signal delays differ between sensory modalities. Specifically, signal transmission times to and neuronal connectivity within the sensorimotor network lead to delayed information about leg loading relative to movement signals. Temporal delays persist up to the level of the motor output, demonstrating its relevance for motor control.