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

Abstract

The relatively large primary olfactory center of the insect brain, the antennal lobe (AL), contains several heterogeneous neuronal types. These include projection neurons (PNs), providing olfactory information to higher-order neuropils via parallel pathways, and local interneurons (LNs), which provide lateral processing within the AL. In addition, various types of centrifugal neurons (CNs) offer top-down modulation onto the other AL neurons. By performing iontophoretic intracellular staining, we collected a large number of AL neurons in the moth, Helicoverpa armigera, to examine the distinct morphological features of PNs, LNs, and CNs. We characterize 190 AL neurons. These were allocated to 25 distinct neuronal types or sub-types, which were reconstructed and placed into a reference brain. In addition to six PN types comprising 15 sub-types, three LN and seven CN types were identified. High-resolution confocal images allowed us to analyze AL innervations of the various reported neurons, which demonstrated that all PNs innervating ventroposterior glomeruli contact a protocerebral neuropil rarely targeted by other PNs, that is the posteriorlateral protocerebrum. We also discuss the functional roles of the distinct CNs, which included several previously uncharacterized types, likely involved in computations spanning from multisensory processing to olfactory feedback signalization into the AL.

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

“…2K). In contrast to most non-MGC mlALT PNs, innervating dorsal neuropils such as the SLP (Kymre et al, 2020), both PNs projected solely to ventral neuropils, mainly the VLP. Similar neurons were previously reported in another heliothine species (Lee et al, 2019).…”

“…The multiglomerular mediolateral-tract PNs (dashed green lines) target primarily the VLP, whereas the uniglomerular lateral-tract PNs innervating the cumulus runs directly to the column in the anterior SIP (Chu et al, 2020a). In the right hemisphere, a plethora of different PN-types arborizing in the ordinary glomeruli (OG) innervate several lateral protocerebral neuropils (Ian et al, 2016;Kymre et al, 2020). (B) Projection scheme of MGC PNs versus OG PNs in the higher brain regions.…”

“…By applying a calcium-sensitive dye (Fura 2) into the calyces (Fig. 1A), we label primarily the population of medial-tract uniglomerular neurons (Ian et al, 2016;Kymre et al, 2020). In the species used here, H. armigera, the MGC comprises three units (Skiri et al, 2005;Zhao et al, 2016) receiving input from three OSN categories: (1) the cumulus from OSNs tuned to the primary component, Z11-16:Al, (2) the dorsomedial posterior (dmp) unit from OSNs tuned mainly to the secondary component, and (3) the dorsomedial anterior (dma) unit from OSNs tuned to the behavioral antagonist/enhancer, Z9-14:AL (Wu et al, 2015).…”

“…(Chu et al, 2020a). In the right hemisphere, a plethora of different PN-types arborizing in the ordinary glomeruli (OG) innervate several lateral protocerebral neuropils (Ian et al, 2016;Kymre et al, 2020). (B) Projection scheme of MGC PNs versus OG PNs in the higher brain regions.…”

Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

“…To measure the output signals from the same three MGC glomeruli, we performed calcium imaging measurements of odor-evoked responses in a group of PNs exclusively. By applying a calcium-sensitive dye (Fura-2) into the calyces ( Figure 2A ), we label primarily the population of medial-tract uniglomerular neurons ( Ian et al, 2016 ; Kymre et al, 2021 ). In the species used here, H. armigera , the MGC comprises three units ( Skiri et al, 2005 ; Zhao et al, 2016 ) receiving input from three OSN categories: (1) the cumulus from OSNs tuned to the primary component, Z11-16:Al, (2) the dorsomedial posterior (dmp) unit from OSNs tuned mainly to the secondary component, Z9-16:Al, and (3) the dorsomedial anterior (dma) unit from OSNs tuned to the behavioral antagonist/enhancer, Z9-14:AL ( Wu et al, 2015 ).…”