Locust Embryo Study Reveals How Antenna Bristles Map Line by Line to the Brain

In the desert locust Schistocerca gregaria, a small patch of bristle-shaped sense organs on the antenna appears to keep its identity all the way from the insect’s outer cuticle to its brain. A new open-access study published in Development Genes and Evolution on 1 May 2024 shows that during embryonic development, the sensory cells associated with these basiconic-type bristles arise in a strict distal-to-proximal sequence, and that their axons join the antennal nerve tracts in that same order, building a topographic and temporal map within the tract itself.

The research, carried out by George Boyan and Erica Ehrhardt, focused on the basiconic-type bristles of the antennal flagellum. On hatching, these bristles are found only at fixed locations on the six most distal annuli, or segments, of the antenna, a pattern previously documented by Chapman and colleagues. Each bristle is innervated by a dendrite from a cluster of sensory cells in the underlying epidermis, and each cluster sends fused axons toward the brain along one of two antennal tracts. Because the bristle positions are fixed, the authors asked whether that spatial order is preserved in the wiring.

To trace the origins of these sensory cells, the team used confocal imaging and immunolabeling on embryonic antennae, drawing on more than 140 preparations. The S-phase label EdU marked proliferating cells, the nuclear stain DAPI outlined cell bodies, and antibodies against Lachesin, horseradish peroxidase (HRP), and phospho-histone 3 flagged differentiating neuroepithelial cells, neurons, and mitotically active precursors respectively. Sense organ precursors, or SOPs, were first detected at 30 percent of embryogenesis, localized in defined bands of the epithelium corresponding to individual annuli.

By 31 percent of embryogenesis, individual SOPs were seen at the tips of columns of EdU-positive epithelial cells, which the authors interpret as lineages. Double labeling for Lachesin and phospho-histone 3 at 33 percent showed that mitotically active SOPs were distributed circumferentially within the Lach-positive epithelial domains of the distal annuli. The precursors are connected to the cuticle by an epithelial foot, and at 38 percent a representative SOP in annulus A2 was associated with three Lach- and HRP-positive progeny. By 48 percent, a dividing SOP had detached from the epithelium and was accompanied by at least six such progeny, and by 55 percent each mitotically active SOP sat beside a cluster of HRP-positive cells that had already extended axons onto an antennal tract.

The appearance of the sensory cell clusters followed a clear temporal gradient. At 45 percent of embryogenesis, HRP-labeled clusters were numerous only in the most distal annulus A1, with a single unilateral cluster in A4. At 53 percent, clusters had increased in A1, A2, and A4, and isolated clusters appeared in A6 and A8. At 56 percent, A3 was populated as well, while the more proximal annuli A5 through A8 had advanced little. By 65 percent, labeled clusters filled the epithelia of A1 through A8, and proliferative precursors were no longer detected in these distal annuli afterward, suggesting that embryonic generation of the clusters was complete. The oldest neuronal populations therefore sit near the antennal tip, with progressively younger populations toward the base.

The wiring side of the story emerged from tracking axons. At 43 percent of embryogenesis, clusters in A1 had already generated axons projecting onto the primary tract system, which consists of a ventral and a dorsal tract running along the border between the lumen and the epithelium toward the antennal base. By 48 percent, clusters were clearly associated with either the ventral or the dorsal tract, and dendrites extended toward the cuticle even though bristles were not yet evident. Even at 70 percent, target basiconic bristles had not formed; only at 85 percent did cuticular bristles appear, innervated by fused HRP-positive dendrites from the sensory cell clusters. Depth-collaged confocal montages confirmed that clusters in A1 and A2 project axons onto their respective ventral or dorsal tracts in symmetrical patterns.

The most striking result came from computer-based autotracings of axons from six representative HRP-positive sensory cell clusters in annuli A5 and A6 at the first instar stage. The axons joined the ventral tract in strict sequence according to the position of their cell cluster along the antenna: axons from distal clusters lie medially in the tract, and axons from progressively more proximal clusters add laterally, producing a layered topographic profile the authors compare to tree rings. Because the clusters themselves appeared developmentally from distal to proximal, the tract also carries a temporal topology, with axons from older neurons lying medially and those from younger neurons laterally.

The authors propose that this organization could allow spatially and temporally encoded information from the basiconic cell clusters of the distal six annuli to travel unmixed from bristle to brain, an anatomical implementation of the labeled-line principle in which sensory structures and their central targets form point-to-point communication channels. They note, however, that their evidence is limited to the distal six annuli, where cell clusters and initial axon projections can be imaged simultaneously. Testing whether the order is maintained further downstream would require differential labeling of clusters and axons, for example through genetic labeling techniques not yet available in the locust.

The findings connect to a broader literature on topographic mapping in sensory systems. In the cockroach, another orthopteroid insect, pheromone-sensing neurons project to different layers of the macroglomerulus, mapping both spatial location and birth date, and antennal lobe responses vary with the position of olfactory sensilla along the antenna. In Drosophila, spatial maps of sensillum subtypes match ordered odorant receptor expression and translate into an odorant map in the antennal lobe, while in the locust itself, terminals from odorant-sensitive afferents are distributed discretely in the olfactory lobe. The authors also point out that SNMP1 and SNMP2 sensory neuron membrane proteins expressed in locust basiconic sensilla are already distributed topographically by the first instar, meaning the pattern must have developed embryonically and is retained to maturity.

Ecologically, the picture is more dynamic than the wiring itself. The distribution of sensilla on more proximal antennal segments changes during postembryonic development, is influenced by environmental conditions and diet, and differs between solitarious and gregarious locusts, while odorant receptor expression varies by sex. Yet as studies in Drosophila suggest, the underlying neuronal wiring can remain conserved even when the ligand spectrum shifts. Within that molecularly flexible system, the layered, age-ordered axon profile described in the locust antenna offers a concrete anatomical substrate for how a growing insect preserves a point-to-point sensory map from the very first bristle to the brain.

Subject of Research: Embryonic development of topographic sensory projections from basiconic sensilla in the locust antennal nervous system

Article Title: From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria

Article References: Boyan, G., & Ehrhardt, E. (2024). From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria. Development Genes and Evolution, 234(1), 33-44. https://doi.org/10.1007/s00427-024-00716-2

Image Credits: AI Generated

DOI: 10.1007/s00427-024-00716-2

Keywords: locust, Schistocerca gregaria, antennal nervous system, basiconic sensilla, embryonic development, topographic mapping, sensory neurons, labeled lines, axon tracts, immunolabeling, confocal imaging, neurodevelopment