Tiling of the body wall by multidendritic sensory neurons in Manduca sexta

Abstract

A plexus of multidendritic sensory neurons, the dendritic arborization (da) neurons, innervates the epidermis of soft‐bodied insects. Previous studies have indicated that the plexus may comprise distinct subtypes of da neurons, which utilize diverse cyclic 3′,5′‐guanosine monophosphate signaling pathways and could serve several functions. Here, we identify three distinct classes of da neurons in Manduca, which we term the alpha, beta, and gamma classes. These three classes differ in their sensory responses, branch complexity, peripheral dendritic fields, and axonal projections. The two identified alpha neurons branch over defined regions of the body wall, which in some cases correspond to specific natural folds of the cuticle. These cells project to an intermediate region of the neuropil and appear to function as proprioceptors. Three beta neurons are characterized by long, sinuous dendritic branches and axons that terminate in the ventral neuropil. The function of this group of neurons is unknown. Four neurons belonging to the gamma class have the most complex peripheral dendrites. A representative gamma neuron responds to forceful touch of the cuticle. Although the dendrites of da neurons of different classes may overlap extensively, cells belonging to the same class show minimal dendritic overlap. As a result, the body wall is independently tiled by the beta and gamma da neurons and partially innervated by the alpha neurons. These properties of the da system likely allow insects to discriminate the quality and location of several types of stimuli acting on the cuticle. J. Comp. Neurol. 440:271–283, 2001.