Topographic organization of sensory afferents of Johnston's organ in the honeybee brain

Abstract

Johnston's organ (JO) in insects is a multicellular mechanosensory organ stimulated by movement of the distal part of the antenna. In honeybees JO is thought to be a primary sensor detecting air-particle movements caused by the waggling dance of conspecifics. In this study projection patterns of JO afferents within the brain were investigated. About 720 somata, distributed around the periphery of the second segment of the antenna (pedicel), were divided into three subgroups based on their soma location: an anterior group, a ventral group, and a dorsal group. These groups sent axons to different branches (N2 to N4) diverged from the antennal nerve. Dye injection into individual nerve branches revealed that all three groups of afferents, having fine collaterals in the dorsal lobe, sent axons broadly through tracts T6I, T6II, and T6III to terminate ipsilaterally in the medial posterior protocerebral lobe, the dorsal region of the subesophageal ganglion, and the central posterior protocerebral lobe, respectively. Within these termination fields only axon terminals running in T6I were characterized by thick processes with large varicosities. Differential staining using fluorescent dyes revealed that the axon terminals of the three groups were spatially segregated, especially in T6I, showing some degree of somatotopy. This spatial segregation was not observed in axon terminals running in other tracts. Our results show that projection patterns of JO afferents in the honeybee brain fundamentally resemble those in the dipteran brain. The possible roles of extensive termination fields of JO afferents in parallel processings of mechanosensory signals are discussed.