Central projections from Johnston´s Organ in the locust: axogenesis and brain neuroarchitecture

Abstract Johnston´s Organ (JO) acts as an antennal auditory organ across a spectrum of insect species and its axons universally project to the brain. In the locust, this pathway is present at mid-embryogenesis but the process of fasciculation involved in constructing it has not been investigated. Terminal projections into the fine neuropilar organisation of the brain also remain unresolved, information essential for providing insights into the neural circuitry mediating JO-mediated behavior and its evolutionary aspects. In our study here, we employ both neuron-specific and axon-specific labels to show that the pathway to the brain of the locust is built in a stepwise manner during early embryogenesis as processes from JO cell clusters fasciculate first with one another, and then with the two tracts constituting the pioneer axon scaffold of the antenna. A comparison of fasciculation patterns confirms that projections from cell clusters of the JO stereotypically associate with only one axon tract according to their location in the pedicel, consistent with a topographic plan. At the molecular level, all neuronal elements of the JO pathway to the brain express the lipocalin Lazarillo, a cell surface epitope we have shown regulates axogenesis in the primary axon scaffold and may also do so during fasciculation of JO projections to the brain. Central projections from JO first contact the primary axon scaffold of the mid-embryonic brain in the mechanosensory region of the antennal lobe but terminate in the protocerebrum. Examination of the neuroarchitecture of the adult brain reveals these terminals lie among the processes of premotor interneurons known to regulate flight behavior.