Existence of a Long-Range Caudo-Rostral Sensory Influence in Terrestrial Locomotion

Abstract

In multisegmented locomotion, coordination of all appendages is crucial for the generation of a proper motor output. In running for example, leg coordination is mainly based on the central interaction of rhythm generating networks, called central pattern generators (CPGs). In slower forms of locomotion, however, sensory feedback, which originates from sensory organs that detect changes in position, velocity and load of the legs' segments, has been shown to play a more crucial role. How exactly sensory feedback influences the activity of the CPGs to establish functional neuronal connectivity is not yet fully understood. Using the female stick insect Carausius morosus, we show for the first time that a long-range caudo-rostral sensory connection exists and highlight that load as sensory signal is sufficient to entrain rhythmic motoneuron (MN) activity in the most rostral segment. So far, mainly rostro-caudal influencing pathways have been investigated where the strength of activation, expressed by the MN activity in the thoracic ganglia, decreases with the distance from the stepping leg to these ganglia. Here, we activated CPGs, producing rhythmic neuronal activity in the thoracic ganglia by using the muscarinic agonist pilocarpine and enforced the stepping of a single, remaining leg. This enabled us to study sensory influences on the CPGs' oscillatory activity. Using this approach, we show that, in contrast to the distance-dependent activation of the protractor-retractor CPGs in different thoracic ganglia, there is no such dependence for the entrainment of the rhythmic activity of active protractor-retractor CPG networks by individual stepping legs.SIGNIFICANCE STATEMENT We show for the first time that sensory information is transferred not only to the immediate adjacent segmental ganglia but also to those farther away, indicating the existence of a long-range caudo-rostral sensory influence. This influence is dependent on stepping direction but independent of whether the leg is actively or passively moved. We suggest that the sensory information comes from unspecific load signals sensed by cuticle mechanoreceptors (campaniform sensilla) of a leg. Our results provide a neuronal basis for the long-established behavioral rules of insect leg coordination. We thus provide a breakthrough in understanding the neuronal networks underlying multilegged locomotion and open new vistas into the neuronal functional connectivity of multisegmented locomotion systems across the animal kingdom.

Keywords: CPG; entrainment; inter-segmental coordination; locomotion; six-legged walking.