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

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          Abstract

          Even though insects have comparably small brains, they achieve astoundingly complex behaviors. One example is flying moths tracking minute amounts of pheromones using olfactory circuits. The tracking distance can be up to 1 km, which makes it essential that male moths respond efficiently and reliably to very few pheromone molecules. The male-specific macroglomerular complex (MGC) in the moth antennal lobe contains circuitry dedicated to pheromone processing. Output neurons from this region project along three parallel pathways, the medial, mediolateral, and lateral tracts. The MGC-neurons of the lateral tract are least described and their functional significance is mainly unknown. We used mass staining, calcium imaging, and intracellular recording/staining to characterize the morphological and physiological properties of these neurons in the noctuid moth, Helicoverpa armigera. All lateral-tract MGC neurons targeted the column, a small region within the superior intermediate neuropil. We identified this region as a unique converging site for MGC lateral-tract neurons responsive to pheromones, as well as a dense congregating site for plant odor information since a substantial number of lateral-tract neurons from ordinary glomeruli (OG) also terminates in this region. The lateral-tract MGC-neurons responded with a shorter peak latency than the well-described neurons in the medial tract. Different from the medial-tract MGC neurons encoding odor quality important for species-specific signal identification, those in the lateral tract convey a more robust and rapid signal—potentially important for fast control of hard-wired behavior.

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          Most cited references52

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          The Ecology of Heliothis Species in Relation to Agroecosystems

          G Fitt (1989)
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            Central neural coding of sky polarization in insects.

            Many animals rely on a sun compass for spatial orientation and long-range navigation. In addition to the Sun, insects also exploit the polarization pattern and chromatic gradient of the sky for estimating navigational directions. Analysis of polarization-vision pathways in locusts and crickets has shed first light on brain areas involved in sky compass orientation. Detection of sky polarization relies on specialized photoreceptor cells in a small dorsal rim area of the compound eye. Brain areas involved in polarization processing include parts of the lamina, medulla and lobula of the optic lobe and, in the central brain, the anterior optic tubercle, the lateral accessory lobe and the central complex. In the optic lobe, polarization sensitivity and contrast are enhanced through convergence and opponency. In the anterior optic tubercle, polarized-light signals are integrated with information on the chromatic contrast of the sky. Tubercle neurons combine responses to the UV/green contrast and e-vector orientation of the sky and compensate for diurnal changes of the celestial polarization pattern associated with changes in solar elevation. In the central complex, a topographic representation of e-vector tunings underlies the columnar organization and suggests that this brain area serves as an internal compass coding for spatial directions.
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              Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths.

              We characterized single upwind surges of flying male Heliothis virescens moths in response to individual strands of pheromone generated experimentally in a wind tunnel. We then showed how this surge functions in this species as a basic 13.4-cm, 0.38-sec-long building block that is strung together repeatedly during typical male upwind flight in a normal pheromone plume. The template for a single iteration, complete with crosswind casting both before and after the straighter upwind surging portion, was exhibited by males flying upwind to pheromone and experiencing filament contacts just frequently enough to produce successful upwind flight to the source, as hypothesized by an earlier model. Also as predicted, with more frequent filament contact by males, only the straightest upwind portions of the surges were reiterated, producing direct upwind flight with little crosswind casting. Electroantennogram recordings made from males in free flight upwind in a normal point source pheromone plume further support the idea that a high frequency of filaments encountered under the usual pheromone plume conditions promotes only these repeated straight surges. In-flight electroantennogram recordings also showed that when filament contacts cease, the casting, counterturning program begins to be expressed after a latency period of 0.30 sec. Together these results provide a plausible explanation for how male and female moths, and maybe other insects, fly successfully upwind in an odor plume and locate the source of odor, using a surging-casting, phasic-tonic response to the onset and disappearance of each odor strand.
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                Author and article information

                Contributors
                Journal
                Front Cell Neurosci
                Front Cell Neurosci
                Front. Cell. Neurosci.
                Frontiers in Cellular Neuroscience
                Frontiers Media S.A.
                1662-5102
                08 June 2020
                2020
                : 14
                : 147
                Affiliations
                [1] 1Chemosensory Laboratory, Department of Psychology, Norwegian University of Science and Technology , Trondheim, Norway
                [2] 2Lund Vision Group, Department of Biology, Lund University , Lund, Sweden
                Author notes

                Edited by: Julian P. Meeks, University of Texas Southwestern Medical Center, United States

                Reviewed by: Monika Stengl, University of Kassel, Germany; Nicolás Pírez, Molecular Biology and Neurosciences (IFIBYNE), Argentina

                *Correspondence: Xi Chu xi.chu@ 123456ntnu.no

                Specialty section: This article was submitted to Cellular Neurophysiology, a section of the journal Frontiers in Cellular Neuroscience

                Article
                10.3389/fncel.2020.00147
                7294775
                d2f3f727-a682-4482-bd5f-e5b16501b58a
                Copyright © 2020 Chu, Heinze, Ian and Berg.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 March 2020
                : 04 May 2020
                Page count
                Figures: 8, Tables: 0, Equations: 4, References: 59, Pages: 20, Words: 13191
                Funding
                Funded by: Norges Forskningsråd 10.13039/501100005416
                Award ID: 287052
                Funded by: Vetenskapsrådet 10.13039/501100004359
                Award ID: 621-2012-2213
                Funded by: European Research Council 10.13039/501100000781
                Award ID: 714599
                Categories
                Cellular Neuroscience
                Original Research

                Neurosciences
                pheromone system,insect olfaction,parallel processing,intracellular recording/staining,calcium imaging

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