Central Projections of Antennal and Labial Palp Sensory Neurons in the Migratory Armyworm Mythimna separata

Abstract

The oriental armyworm, Mythimna separata (Walker), is a polyphagous, migratory pest relying on olfactory cues to find mates, locate nectar, and guide long-distance flight behavior. In the present study, a combination of neuroanatomical techniques were utilized on this species, including backfills, confocal microscopy, and three-dimensional reconstructions, to trace the central projections of sensory neurons from the antenna and the labial pit organ, respectively. As previously shown, the axons of the labial sensory neurons project via the ipsilateral labial nerve and terminate in three main areas of the central nervous system: (1) the labial-palp pit organ glomerulus of each antennal lobe, (2) the gnathal ganglion, and (3) the prothoracic ganglion of the ventral nerve cord. Similarly, the antennal sensory axons project to multiple areas of the central nervous system. The ipsilateral antennal nerve targets mainly the antennal lobe, the antennal mechanosensory and motor center, and the prothoracic and mesothoracic ganglia. Specific staining experiments including dye application to each of the three antennal segments indicate that the antennal lobe receives input from flagellar olfactory neurons exclusively, while the antennal mechanosensory and motor center is innervated by mechanosensory neurons from the whole antenna, comprising the flagellum, pedicle, and scape. The terminals in the mechanosensory and motor center are organized in segregated zones relating to the origin of neurons. The flagellar mechanosensory axons target anterior zones, while the pedicular and scapal axons terminate in posterior zones. In the ventral nerve cord, the processes from the antennal sensory neurons terminate in the motor area of the thoracic ganglia, suggesting a close connection with motor neurons. Taken together, the numerous neuropils innervated by axons both from the antenna and labial palp indicate the multiple roles these sensory organs serve in insect behavior.

Revisiting the Labial Pit Organ Pathway in the Noctuid Moth, Helicoverpa armigera

“…Distinct staining of sensilla located on the outer palp surface, as performed here, revealed that the projections originating from this site terminate in the two additional areas -the GNG and the ventral nerve cord. "Merging" the staining patterns obtained from the two labeling techniques utilized in the present study ( Figures 1B,C), forms a pattern that is very similar to that previously reported by several researchers using the classic mass staining technique ( Figure 1D; Kent et al, 1986;Lee and Altner, 1986;Zhao et al, 2013;Ma et al, 2017). This confirms the suggestion made by Kent et al (1986) that the axon projections to the LPOGs originated from sensory neurons housed inside the pit and that the branches seen in the GNG were parts of other sensory neuron types.…”

“…In all these studies, dye was applied to the truncated part of the peripheral labial-palp segment. Whereas the two last-mentioned reports insisted that all labeled axons were CO 2 -sensitive neurons projecting from the LPO (Zhao et al, 2013;Ma et al, 2017), the original paper suggested that the stained processes in the GNG arose from other sensory neurons on the labial palp (Kent et al, 1986). Thus, even though all previous studies have reported about LPO projections passing bilaterally to the LPOG in each antennal lobe, the total staining pattern including additional axon terminals in other central regions has been interpreted in various ways by the different investigations.…”

“…An unresolved issue, however, is whether sensory axons from the LPO also have projections in central areas other than the antennal lobes. In the classical paper about the "accessory olfactory pathway, " (Kent et al, 1986) found additional innervations in the gnathal ganglion (GNG), and consecutive studies of other moths have reported additional terminal branches in the ventral nerve cord (Lee and Altner, 1986;Zhao et al, 2013;Ma et al, 2017). In all these studies, dye was applied to the truncated part of the peripheral labial-palp segment.…”

“…Another relevant issue concerns the projection pattern of individual neurons. Although several studies have characterized the LPO sensory neurons, both structurally and functionally (Kent et al, 1986;Stange, 1992Stange, , 1997Stange et al, 1995;Sage, 2002;Guerenstein et al, 2004;Zhao et al, 2013;Ma et al, 2017), we still know little about projection patterns of single axons and how the sampled CO 2 input is integrated in the central nervous system.…”

Brain Organization of Apolygus lucorum: A Hemipteran Species With Prominent Antennal Lobes

“…It receives axonal terminals originating mainly from the neurons of Böhm bristles and Johnston’s organ. Different sensory neurons project to distinct regions of the AMMC in many different insect species (Ma et al, 2017). In Drosophila , the AMMC is subdivided into five zones, while in the desert locust, it is subdivided into four regions (Kamikouchi et al, 2009; von Hadeln et al, 2018).…”