Heterogeneous properties of segmentally homologous interneurons in the ventral nerve cord of locusts

Abstract

The G, B1, and B2 neurons are three prominent interneurons located in adjacent segmental ganglia in the central nervous system of locusts. Previous studies on the adult nervous system have shown that each of these cells has its own distinctive morphology and responsiveness to auditory input. Previous studies on the embryonic nervous system have described the lineage and development of one of these cells, the G neuron, in the mesothoracic (T2) segment. In this paper it is shown that the G, B1, and B2 neurons are segmental homologues in that they arise from equivalent lineages during embryogenesis in the T2, T3, and A1 segments, respectively. Each cell arises (along with its identified sibling neuron) from the division of the second ganglion mother cell of neuroblast 7-4. The segment-specific morphology of the G homologues was determined in the T3 and A1 segments between 60-70% of embryonic development, and their identity was established as the adult B1 and B2 neurons by comparing the distinctive cell-specific features of their morphology between embryo and adult. Although all three neurons display striking morphological differences, they all share certain structural features in common, including the location of their primary axons and neurites in specific tracts in the neuropil. By recording intracellularly from the main neurites of the G, B1, and B2 neurons, clear differences were found in the synaptic inputs each of the neurons receives and the synaptic outputs each makes. For example, G and B2, but not B1, receive direct monosynaptic input from the descending contralateral movement detector (DCMD) interneurons and from auditory afferents; B1, but not B2, connects directly to G; and B2, but not B1 or G, connects directly to flight motoneurons. The main conclusion from these observations is that lineally equivalent neurons in different segments can develop similar primary structures but quite different secondary morphologies and synaptic connections. How these segment-specific differences arise during embryogenesis remains unknown.