Male silkmoths, Bombyx mori, exhibit a characteristic zigzagging behavior consisting of straight-line walking, zigzagging turns, and looping. The timing for shifting the turning direction is synchronized to the sideways head movements controlled by neck motor neurons (NMNs) including a cervical ventral NMN (cv1-NMN). It has been suggested that this programmed behavior is instructed by two types of activity patterns descending from the brain and the thoracic ganglion: one is a phasic excitation and the other is a state-dependent activity similar to the flipflop in electric memory circuits. These activities are shown by certain descending interneurons contained in two subsets of DNs, Group-I and -II DNs. However, it is not yet well understood which DNs are directly related to instructing this behavior. In order to understand neural control mechanisms of this programmed behavior, we investigated the morphological relationship between these DNs and the cv1-NMN, which is an index of this programmed behavior. We applied a double-labeling technique combining backfilling of the cv1-NMN and intracellular staining of single DNs. 3D confocal images revealed overlapping regions between the Group-I, -II DNs and the cv1-NMN. Group-IIA and -IID, which showed typical flipflop activities, Group-IIC DNs, which showed phasic excitation, and Group-IB DNs, which showed long-lasting inhibition had many overlapping regions on the cv1-NMNs. Our results indicate that the programmed behavior is instructed by these types of DNs.

A population of descending neurons connect the brain and thoracic motor center, playing a critical role in controlling behavior. We examined the anatomical organization of descending neurons (DNs) in the brain of the silkmoth Bombyx mori. Moth pheromone orientation is a good model to investigate neuronal mechanisms of behavior. Based on mass staining and single-cell staining, we evaluated the anatomical organization of neurite distribution by DNs in the brain. Dense innervation was observed in the posterior–ventral part of the brain called the posterior slope (PS). We analyzed the morphology of DNs innervating the lateral accessory lobe (LAL), which is considered important for moth olfactory behavior. We observed that all LAL DNs also innervate the PS, suggesting the integration of signals from the LAL and PS. We also identified a set of DNs innervating the PS but not the LAL. These DNs were sensitive to the sex pheromone, suggesting a role of the PS in motor control for pheromone processing. Here we discuss the organization of descending pathways for pheromone orientation.