A novel major output target for pheromone-sensitive projection neurons in male moths

Abstract

10The male-specific macroglomerular complex (MGC) in the moth antennal lobe contains 11 circuitry dedicated to pheromone processing. Output neurons from this region project along 12 three parallel pathways, the medial, mediolateral, and lateral tracts. The MGC-neurons of the 13 lateral tract are least described and their functional significance is unknown. We used 14 mass-staining, calcium imaging, and intracellular recording/staining to characterize the 15 morphological and physiological properties of these neurons in Helicoverpa armigera. All 16 lateral-tract MGC neurons targeted the column, a small region within the superior intermediate 17 neuropil. We identified this region as the major converging site for lateral-tract neurons 18 responsive to pheromones and plant-odors. The lateral-tract MGC-neurons consistently 19 responded with a faster onset than the well-described medial-tract neurons. Different from the 20 medial-tract MGC neurons encoding odor quality important for signal identification, those in 21 the lateral tract seem to convey a robust and rapid, but fixed signalpotentially important for 22 fast control of hard-wired behavior. 23 24 25In the antennal lobe, all sensory axons make synaptic contacts with local interneurons 51 and projection neurons. The latter cells carry odor information to higher integration centers in 52 the protocerebrum via several parallel antennal-lobe tracts (ALTs). The three main ALTs, the 53 medial ALT, the mediolateral ALT, and the lateral ALT, connect the antennal lobe with the 54 calyces of the mushroom bodies (MB) and the lateral protocerebrum (mostly lateral horn), 55 which constitute the two most prominent higher-order olfactory projection areas across insects 56 (Homberg et al., 1988, Seki et al., 2005, Rø et al., 2007, Ito et al., 2014. A third area is targeted 57 by a significant proportion of lateral-tract projection neurons and is embedded in the superior 58 intermediate protocerebrum (SIP, see Ito et al., 2014), occupying the space in between the 59 anterior optic tubercle (AOTU) and the MB vertical lobe. Although it was discovered in the 60 hawk moth Manduca sexta (Homberg et al., 1988), its prominence as a major projection region 61 was pointed out in the heliothine moth, where it was termed the column (Ian et al., 2016). 62 Similar to insects, an arrangement of parallel olfactory tracts and projection areas is also 63 found in vertebrates, such as fish (Hamdani and Døving, 2007) and mammals (Mori, 2016, 64 Kauer, 1991. In fish, each of three tracts carries a different category of olfactory information, 65 i.e. social cues, pheromones, and food odors (Hamdani and Døving, 2007). Contrary, in insects, 66 particularly in moths, each of the three main ALTs is formed by axons of projection neurons 67 originating from both the MGC and the ordinary glomeruli (Homberg et al., 1988, Zhao et al., 68 2014, Kanzaki et al., 2003. Thus, different categories of olfactory cues are processed in all 69 ALTs. Rather than encoding different stimulus categor...

Antennal‐lobe neurons in the moth Helicoverpa armigera: Morphological features of projection neurons, local interneurons, and centrifugal neurons

“…The Pl_a sub‐type targeting the column of the SIP is not represented here. All stained PNs of this sub‐type innervated the MGC, and they were recently reported in Chu et al (2020). The almost exclusively multiglomerular mlALT PNs all innervate the SLP (Figure 4), and most also target the LH.…”

“…To compensate for refraction indexes, the z‐axis dimension of the brain was multiplied by a factor of 1.16 for the water objective and 1.54 for the air lens. Reconstructed neurons were manually transformed into the 3D representative brain of H. armigera (Chu et al, 2020) in accordance with their original projection pattern.…”

“…The staining procedure was performed as previously described (Chu et al, 2020; Ian, Zhao, et al, 2016; KC et al, 2020). Electrodes were pulled from borosilicate capillaries (OD: 1 mm, ID: 0.5 mm, with hollow filament 0.13 mm; Hilgenberg GmbH, Germany) using a horizontal P‐97 Flaming/Brown Pipette Puller (Sutter Instruments Inc.).…”

“… Note : Innervations in bold are most frequent. References: 1) Anton, Löfstedt, and Hansson (1997); 2) Chu, Heinze, Ian, & Berg, (2020); 3) Hansson, Anton, and Christensen (1994); 4) Homberg et al (1988); 5) Ian, Zhao, et al (2016); 6) Kanzaki, Arbas, Strausfeld, and Hildebrand (1989); 7) Kanzaki, Soo, Seki, and Wada (2003); 8) Lee, Celestino, Stagg, Kleineidam, and Vickers (2019); 9) Løfaldli, Kvello, and Mustaparta (2010); 10) Namiki and Kanzaki (2011); 11) Nirazawa et al (2017); 12) Rø, Müller, and Mustaparta (2007); 13) Sadek, Hansson, Rospars, and Anton (2002); 14) Wu, Anton, Löfstedt, and Hansson (1996); 15) Zhao and Berg (2010); 16) Zhao et al (2014). …”

A Novel Major Output Target for Pheromone-Sensitive Projection Neurons in Male Moths

“…We thank Jonas H. Kymre (NTNU), Christoffer Nerland Berge (NTNU), and Pramod KC (NTNU) for assistance with data collection. This article has been released as a pre-print at bioRxiv (Chu et al, 2019).…”