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

Abstract

The pheromone system of heliothine moths is an optimal model for studying principles underlying higher-order olfactory processing. In Helicoverpa armigera, three male-specific glomeruli receive input about three female-produced signals, the primary pheromone component, serving as an attractant, and two minor constituents, serving a dual function, i.e. attraction versus inhibition of attraction. From the antennal-lobe glomeruli, the information is conveyed to higher olfactory centers, including the lateral protocerebrum, via three main paths – of which the medial tract is the most prominent. In this study, we traced physiologically identified medial-tract projection neurons from each of the three male‑specific glomeruli with the aim of mapping their terminal branches in the lateral protocerebrum. Our data suggest that the neurons’ wide-spread projections are organized according to behavioral significance, including a spatial separation of signals representing attraction versus inhibition – however, with a unique capacity of switching behavioral consequence based on the amount of the minor components.

Organization of the parallel antennal-lobe tracts in the moth

“…[5,7,9,13] In addition, we recently demonstrated segregated processing of distinct social cues conveyed along the medial tract of H. armigera males. Specifically, mALT PNs responding to the primary pheromone component predominantly innervates the superior lateral protocerebrum (SLP) and superior intermediate protocerebrum (SIP), whereas mALT PNs sensitive to interspecific signals and the secondary pheromone component (acting as a behavioral antagonist at high concentration) rather innervate anterior parts of the LH (Kymre et al 2021b). In the silkmoth, Bombyx mori, Seki et al (2005) demonstrated that mALT PNs responding to the major pheromone terminate medially of neurons tuned to the minorpheromone.…”

“…Each of these paths thereby appears to connect with all glomerular clusters in the moth AL. Indeed, individual PNs with omniglomerular innervations are found in both the lateral and mediolateral tracts, while the mainly uniglomerular medial-tract PNs collectively cover all glomerular sub-groups (Chu et al 2020b ; Kymre et al 2021a , b ).…”

“…Example confocal images and 3D reconstructions of distinct PN sub-types are available via the insect brain database ( https://insectbraindb.org/app/neuron/dataset/5fa25351-9cc8-4796-beed-74e13e7dae02 ). In addition, PNs innervating specific sub-sets of glomeruli processing input about pheromones and CO 2 have also received substantial attention lately (Chu et al 2020a , b ; Kymre et al 2021b ). Altogether, the data show that tracts other than the mALT are formed mainly by axons of multiglomerular PNs, except for the dmALT consisting primarily of bilaterally uniglomerular PNs.…”

“…Parentheses indicate projection patterns associated with MGC PNs. Table adapted from Kymre et al ( 2021a ) References: (1) Anton et al ( 1997 ); (2) Chu et al ( 2020b ); (3) Chu et al ( 2020a ); (4) Hansson et al ( 1994 ); (5) Homberg et al ( 1988 ); (6) Ian et al ( 2016b ); (7) Kanzaki et al ( 1989 ); (8) Kanzaki et al ( 2003 ); (9) Kymre et al ( 2021a ); (10) Kymre et al ( 2021b ); (11) Lee et al ( 2019 ); (12) Løfaldli et al ( 2010 ); (13) Namiki and Kanzaki ( 2011 ); (14) Nirazawa et al ( 2017 ); (15) Rø et al ( 2007 ); (16) Sadek et al ( 2002 ); (17) Wu et al ( 1996 ); (18) Zhao and Berg ( 2010 ); (19) Zhao et al ( 2014 ) AC , anterior cell cluster; AL , antennal lobe; ALT , antennal-lobe tract; AMMC , antennal mechanosensory and motor center; BL , bilateral; Ca , calyces; CL , contralateral; Col , column of the superior intermediate protocerebrum; dALT , dorsal ALT; dmALT , dorsomedial ALT; FKA , formerly known as; GCBR , cell-body rind around the gnathal ganglion; INP , inferior neuropil; lALT , lateral ALT; LC , lateral cell cluster; LH , lateral horn; mALT , medial ALT; MC , medial cell cluster; MG , multiglomerular; mlALT , mediolateral ALT; PED , peduncle of the mushroom body; PLP , posteriorlateral protocerebrum; SEZ , subesophageal zone; SLP , superior lateral protocerebrum; SNP , superior neuropil; tALT , transverse ALT; TC , tritocerebrum; UL ., unilateral; UG , uniglomerular; VLP , ventrolateral protocerebrum; VMNP , ventromedial neuropil…”

“…References: (1) Anton et al ( 1997 ); (2) Chu et al ( 2020b ); (3) Chu et al ( 2020a ); (4) Hansson et al ( 1994 ); (5) Homberg et al ( 1988 ); (6) Ian et al ( 2016b ); (7) Kanzaki et al ( 1989 ); (8) Kanzaki et al ( 2003 ); (9) Kymre et al ( 2021a ); (10) Kymre et al ( 2021b ); (11) Lee et al ( 2019 ); (12) Løfaldli et al ( 2010 ); (13) Namiki and Kanzaki ( 2011 ); (14) Nirazawa et al ( 2017 ); (15) Rø et al ( 2007 ); (16) Sadek et al ( 2002 ); (17) Wu et al ( 1996 ); (18) Zhao and Berg ( 2010 ); (19) Zhao et al ( 2014 )…”