Moth pheromone‐selective projection neurons with cell bodies in the antennal lobe lateral cluster exhibit diverse morphological and neurophysiological characteristics

Lee, Seonggyu; Celestino, Christine Fogarty; Stagg, Jeffrey; Kleineidam, Christoph Johannes; Vickers, Neil J.

doi:10.1002/cne.24611

Cited by 14 publications

(24 citation statements)

References 61 publications

(145 reference statements)

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“…Heliothis virescens , Helicoverpa zea , and Helicoverpa assulta (Christensen et al, 1991, Christensen et al, 1995, Vickers et al, 1998, Zhao and Berg, 2010, Zhao et al, 2014), as well as Manduca sexta (Christensen and Hildebrand, 1987, Kanzaki et al, 1989, Hansson et al, 1991), Agrotis ipsilon (Jarriault et al, 2009), and Bombyx mori (Kanzaki et al, 2003, Seki et al, 2005). Only a recent publication on two heliothine species reported individual pheromone neurons passing along ALTs other than the medial (Lee et al, 2019). Thus, our understanding of pheromone processing across parallel pathways in moths is still very limited.…”

Section: Introductionmentioning

confidence: 99%

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

Chu

Heinze

Ian

et al. 2019

Preprint

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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...

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Section: Introductionmentioning

confidence: 99%

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

Chu

Heinze

Ian

et al. 2019

Preprint

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“…More work is needed, however, to test links to behavior and determine whether such changes are common among insects. We also note that some PNs involved in innate olfactory behavior (e.g., a subset of pheromonesensitive PNs in moths; Lee et al 2019) project to novel central targets, outside the lateral horn and mushroom body, that may also be sites of relevant evolutionary change.…”

Section: Changes In the Lateral Hornmentioning

confidence: 90%

“…Multiglomerular PNs are a common feature of the MGC of male moths. These neurons integrate information across OSNs sensitive to different pheromones and often show selective tuning for species-specific pheromone blends (Lee et al 2019). This makes OSN/PN connectivity in the AL a clear potential locus for the evolution of pheromone preference in moths, including in Heliothis.…”

Section: Changes In the Antennal Lobementioning

confidence: 99%

Evolution of olfactory circuits in insects

Zhao

McBride

2020

J Comp Physiol A

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Recent years have seen an explosion of interest in the evolution of neural circuits. Comparison of animals from different families, orders, and phyla reveals fascinating variation in brain morphology, circuit structure, and neural cell types. However, it can be difficult to connect the complex changes that occur across long evolutionary distances to behavior. Luckily, these changes accumulate through processes that should also be observable in recent time, making more tractable comparisons of closely related species relevant and complementary. Here, we review several decades of research on the evolution of insect olfactory circuits across short evolutionary time scales. We describe two well-studied systems, Drosophila sechellia flies and Heliothis moths, in detailed case studies. We then move through key types of circuit evolution, cataloging examples from other insects and looking for general patterns. The literature is dominated by changes in sensory neuron number and tuning at the periphery-often enhancing neural response to odorants with new ecological or social relevance. However, changes in the way olfactory information is processed by central circuits is clearly important in a few cases, and we suspect the development of genetic tools in non-model species will reveal a broad role for central circuit evolution. Moving forward, such tools should also be used to rigorously test causal links between brain evolution and behavior.

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“…Although some of the LPOG PNs stained here, i.e. four neuron subtypes (Pt_a (LPOG) , Pt_d (LPOG) , Pm_e (LPOG) , and Pl_g (LPOG) ), had axonal terminals in the SLP, they targeted a distinct area localized more ventrally and lateral-posteriorly as compared to the MGC PNs 25,35,45 .…”

Section: Discussionmentioning

confidence: 70%

Neuronal architecture of the second-order CO2 pathway in the brain of a noctuid moth

Chu

Ian

et al. 2020

Sci Rep

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Many insects possess the ability to detect fine fluctuations in the environmental CO2 concentration. In herbivorous species, plant-emitted CO2, in combination with other sensory cues, affect many behaviors including foraging and oviposition. In contrast to the comprehensive knowledge obtained on the insect olfactory pathway in recent years, we still know little about the central CO2 system. By utilizing intracellular labeling and mass staining, we report the neuroanatomy of projection neurons connected with the CO2 sensitive antennal-lobe glomerulus, the labial pit organ glomerulus (LPOG), in the noctuid moth, Helicoverpa armigera. We identified 15 individual LPOG projection neurons passing along different tracts. Most of these uniglomerular neurons terminated in the lateral horn, a previously well-described target area of plant-odor projection neurons originating from the numerous ordinary antennal-lobe glomeruli. The other higher-order processing area for odor information, the calyces, on the other hand, was weakly innervated by the LPOG neurons. The overlapping LPOG terminals in the lateral horn, which is considered important for innate behavior in insects, suggests the biological importance of integrating the CO2 input with plant odor information while the weak innervation of the calyces indicates the insignificance of this ubiquitous cue for learning mechanisms.

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Moth pheromone‐selective projection neurons with cell bodies in the antennal lobe lateral cluster exhibit diverse morphological and neurophysiological characteristics

Cited by 14 publications

References 61 publications

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

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

Evolution of olfactory circuits in insects

Neuronal architecture of the second-order CO2 pathway in the brain of a noctuid moth

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