Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system

Abstract

The regulation of motor patterns by higher-order neuronal centers ensures appropriate motor function and behavior, but only a few studies have characterized this regulation at the cellular level. Here, we address motor pattern regulation in the stomatogastric nervous system (STNS) of the crab Cancer pagurus. This easily accessible model system is an extension of the central nervous system and contains the motor circuits that generate the rhythmic motor patterns for ingestion (esophageal rhythm) and processing of food (gastric mill and pyloric rhythms). We have documented the actions of two identified neurons located in the brain on the STNS motor circuits. We show that these neurons provide exteroceptive chemosensory information to the motor circuits and we outline their axonal projection patterns, their firing activity and their effects on three motor patterns. Backfill stainings and activity measurements in vivo and in vitro show that two neurons located in cluster 17 of the brain project via the inferior ventricular (IV) nerve to the STNS. These IV neurons started to burst rhythmically when chemosensory stimuli were applied to the first antennae. When rhythmically activated in vitro, gastric mill rhythms were elicited or, if already active, entrained by the IV neuron activity. In addition, IV neuron stimulation excited the esophageal motor neuron and inhibited several pyloric neurons such that the timing of the IV neuron activity was imposed on all motor rhythms. The IV neurons were thus capable of synchronizing the activities of different motor circuits, which demonstrates the regulation of motor patterns by higher-order neuronal centers.