Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Abstract

Dorsal Excitor motor neuron DE-3 in the medicinal leech plays three very different dynamical roles in three different behaviors. In swimming, it oscillates at a relatively rapid 2 Hz in antiphase to its Ventral Excitor counterpart (VE-4) and controls the local dorsal flexion phase of the swim rhythm. In crawling, it is active in phase with VE-4 and controls the contraction phase of the crawl rhythm. In "local bending" it operates in tight concert with its contralateral homolog as well as VE-4 to precisely deform the local body wall away from a mechanical stimulus. Without rewiring its anatomical connectivity, how can a motor neuron dynamically switch roles to play its appropriate role in various behaviors? We used voltage-sensitive dye imaging to record from DE-3 and most other neurons in the segmental ganglion of the leech during fictive versions of the three behaviors. Then we re-imaged the same ganglion using serial blockface electron microscopy and traced all of DE-3's processes. Further, we traced back the processes of all of DE-3's presynaptic partners to their respective somata. This allowed us to analyze the relationship between circuit anatomy and the activity patterns it sustains. We found that input synapses important for all of the behaviors were widely distributed over DE-3's branches, yet that functional clusters were different during (fictive) swimming vs. crawling.