Cellular substrates of action selection: a cluster of higher-order descending neurons shapes body posture and locomotion.

The selection of distinct movements involved in various body postures and locomotion is often dependent on higher-order descending neurons. To study how such cells select different actions, we used a nearly-intact leech preparation (Hirudo sp.) in which cephalic projection interneurons were recorded and stimulated while the leech generated overt behaviors. Two long-distance projecting neurons were identified in the sub-packet of the third neuromere (R3b) of the subesophageal ganglion. These interneurons, named R3b2 and R3b3, produced changes in whole-body posture, crawling and swimming. Cell R3b2 reliably caused the body to become turgid, to hyper-elongate, and to thrash cyclically. Such robust activity resembled struggling behavior exhibited by intact leeches when grasped. The neighboring cell R3b3 elicited body elongation accompanied by a static whole-body bend to the left or right. R3b3 activity was context-dependent, oscillated in phase with crawling, reset the crawl rhythm, and terminated swimming. Both neuronal types responded to multi-modal sensory stimulation delivered to various rostral and caudal regions of the body. Our study illustrates the need to study behavioral selection with a neuroethological approach, and provides a cellular substrate for the motor action-selection cluster proposed for the vertebrate brainstem.