{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,11]],"date-time":"2026-04-11T02:30:52Z","timestamp":1775874652310,"version":"3.50.1"},"reference-count":75,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,5,1]],"date-time":"2024-05-01T00:00:00Z","timestamp":1714521600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,5,1]],"date-time":"2024-05-01T00:00:00Z","timestamp":1714521600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Graduate School of Systemic Neuroscience, Ludwig-Maximilians-Universit\u00e4t, M\u00fcnchen"},{"DOI":"10.13039\/501100005722","name":"Ludwig-Maximilians-Universit\u00e4t M\u00fcnchen","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100005722","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Dev Genes Evol"],"published-print":{"date-parts":[[2024,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    The antennal flagellum of the locust\n                    <jats:italic>S. gregaria<\/jats:italic>\n                    is an articulated structure bearing a spectrum of sensilla that responds to sensory stimuli. In this study, we focus on the basiconic-type bristles as a model for sensory system development in the antenna. At the end of embryogenesis, these bristles are found at fixed locations and then on only the most distal six articulations of the antenna. They are innervated by a dendrite from a sensory cell cluster in the underlying epithelium, with each cluster directing fused axons topographically to an antennal tract running to the brain. We employ confocal imaging and immunolabeling to (a) identify mitotically active sense organ precursors for sensory cell clusters in the most distal annuli of the early embryonic antenna; (b) observe the subsequent spatial appearance of their neuronal progeny; and (c) map the spatial and temporal organization of axon projections from such clusters into the antennal tracts. We show that early in embryogenesis, proliferative precursors are localized circumferentially within discrete epithelial domains of the flagellum. Progeny first appear distally at the antennal tip and then sequentially in a proximal direction so that sensory neuron populations are distributed in an age-dependent manner along the antenna. Autotracing reveals that axon fasciculation with a tract is also sequential and reflects the location and age of the cell cluster along the most distal annuli. Cell cluster location and bristle location are therefore represented topographically and temporally within the axon profile of the tract and its projection to the brain.\n                  <\/jats:p>","DOI":"10.1007\/s00427-024-00716-2","type":"journal-article","created":{"date-parts":[[2024,5,1]],"date-time":"2024-05-01T08:52:52Z","timestamp":1714553572000},"page":"33-44","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["From bristle to brain: embryonic development of topographic projections from basiconic sensilla in the antennal nervous system of the locust Schistocerca gregaria"],"prefix":"10.1007","volume":"234","author":[{"given":"George","family":"Boyan","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Erica","family":"Ehrhardt","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,5,1]]},"reference":[{"key":"716_CR1","doi-asserted-by":"publisher","first-page":"865","DOI":"10.1083\/jcb.153.4.865","volume":"153","author":"RR Adams","year":"2001","unstructured":"Adams RR, Maiato H, Earnshaw W, Carmena M (2001) Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome Segregation. J Cell Biol 153:865\u2013879","journal-title":"J Cell Biol"},{"key":"716_CR2","doi-asserted-by":"publisher","first-page":"1030","DOI":"10.1002\/cne.21341","volume":"502","author":"H Ai","year":"2007","unstructured":"Ai H, Nishino H, Itoh T (2007) Topographic organization of sensory afferents of Johnston\u2019s organ in the honeybee brain. J Comp Neurol 502:1030\u20131046","journal-title":"J Comp Neurol"},{"key":"716_CR3","first-page":"47","volume":"54","author":"D Bentley","year":"1979","unstructured":"Bentley D, Keshishian H, Shankland M, Torian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47\u201374","journal-title":"J Embryol Exp Morphol"},{"key":"716_CR4","doi-asserted-by":"publisher","first-page":"22628","DOI":"10.1038\/s41598-022-27199-3","volume":"12","author":"A Boronat-Garcia","year":"2022","unstructured":"Boronat-Garcia A, Iben J, Dominguez-Martin E, Stopfer M (2022) Identification and analysis of odorant receptors expressed in the two main olfactory organs, antennae and palps, of Schistocerca americana. Sci Rep 12:22628","journal-title":"Sci Rep"},{"key":"716_CR5","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/s00427-016-0565-0","volume":"227","author":"G Boyan","year":"2017","unstructured":"Boyan G, Ehrhardt E (2017) Ontogeny of pioneer neurons in the antennal nervous system of the grasshopper Schistocerca gregaria. Dev Genes Evol 227:11\u201323","journal-title":"Dev Genes Evol"},{"key":"716_CR6","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1007\/s10158-020-0240-z","volume":"20","author":"G Boyan","year":"2020","unstructured":"Boyan G, Ehrhardt E (2020) Epithelial domains and the primordial antennal nervous system of the embryonic grasshopper Schistocerca gregaria. Inv Neurosci 20:6","journal-title":"Inv Neurosci"},{"key":"716_CR7","doi-asserted-by":"publisher","first-page":"167","DOI":"10.3389\/fnbeh.2016.00167","volume":"10","author":"G Boyan","year":"2016","unstructured":"Boyan G, Liu Y (2016) Development of the neurochemical architecture of the central complex. Front Behav Neurosci 10:167","journal-title":"Front Behav Neurosci"},{"key":"716_CR8","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1007\/s00427-010-0348-y","volume":"220","author":"G Boyan","year":"2011","unstructured":"Boyan G, Niederleitner B (2011) Patterns of dye coupling involving serotonergic neurons provide insights into the cellular organization of a central complex lineage of the embryonic grasshopper Schistocerca gregaria. Dev Genes Evol 220:297\u2013313","journal-title":"Dev Genes Evol"},{"key":"716_CR9","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/j.asd.2004.03.001","volume":"33","author":"GS Boyan","year":"2004","unstructured":"Boyan GS, Williams JLD (2004) Embryonic development of the sensory innervation of the antenna of the grasshopper Schistocerca gregaria. Arthr Struct Dev 33:381\u2013397","journal-title":"Arthr Struct Dev"},{"key":"716_CR10","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1016\/j.asd.2007.01.005","volume":"36","author":"GS Boyan","year":"2007","unstructured":"Boyan GS, Williams JLD (2007) Embryonic development of a peripheral nervous system: nerve tract associated cells and pioneer neurons in the antenna of the grasshopper Schistocerca gregaria. Arthr Struct Dev 36:336\u2013350","journal-title":"Arthr Struct Dev"},{"key":"716_CR11","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/j.asd.2014.11.003","volume":"44","author":"G Boyan","year":"2015","unstructured":"Boyan G, Williams L, Liu Y (2015) Conserved patterns of axogenesis in the panarthropod brain. Arthr Struct Devel 44:101\u2013112","journal-title":"Arthr Struct Devel"},{"key":"716_CR12","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1007\/s00427-017-0587-2","volume":"227","author":"G Boyan","year":"2017","unstructured":"Boyan G, Liu Y, Khalsa S, Hartenstein V (2017) A conserved plan for wiring up the fan-shaped body in the grasshopper and Drosophila. Dev Genes Evol 227:253\u2013269","journal-title":"Dev Genes Evol"},{"key":"716_CR13","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1007\/s00427-023-00710-0","volume":"233","author":"G Boyan","year":"2023","unstructured":"Boyan G, Williams L, Ehrhardt E (2023) Central projections from Johnston\u2019s organ in the locust: axogenesis and brain neuroarchitecture. Dev Genes Evol 233:147\u2013159","journal-title":"Dev Genes Evol"},{"key":"716_CR14","first-page":"188","volume":"16","author":"N Bray","year":"2015","unstructured":"Bray N (2015) Whiskers of a good friend. Nat Rev Neurosci 16:188","journal-title":"Nat Rev Neurosci"},{"key":"716_CR15","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/j.cub.2003.12.052","volume":"14","author":"PA Brennan","year":"2004","unstructured":"Brennan PA, Keverne EB (2004) Something in the air? New insights into mammalian pheromones. Curr Biol 14:81\u201389","journal-title":"Curr Biol"},{"key":"716_CR16","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1159\/000102974","volume":"70","author":"A Brockmann","year":"2007","unstructured":"Brockmann A, Robinson GE (2007) Central projections of sensory systems involved in honey bee dance language communication. Brain Behav Evol 70:125\u2013136","journal-title":"Brain Behav Evol"},{"key":"716_CR17","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1111\/j.1469-185X.1960.tb01462.x","volume":"35","author":"FH Butt","year":"1960","unstructured":"Butt FH (1960) Head development in the arthropods. Biological Rev 35:43\u201391","journal-title":"Biological Rev"},{"key":"716_CR18","doi-asserted-by":"publisher","first-page":"7528","DOI":"10.1523\/JNEUROSCI.0186-10.2010","volume":"30","author":"A Cardona","year":"2010","unstructured":"Cardona A, Saalfeld S, Arganda I, Pereanu W, Schindelin J, Hartenstein V (2010) Identifying neuronal lineages of Drosophila by sequence analysis of axon tracts. J Neurosci 30:7528\u20137553","journal-title":"J Neurosci"},{"key":"716_CR19","doi-asserted-by":"publisher","first-page":"100053","DOI":"10.1016\/j.cris.2023.100053","volume":"3","author":"S Cassau","year":"2023","unstructured":"Cassau S, Degen A, Kr\u00fcger S, Krieger J (2023) The specific expression patterns of sensory neuron membrane proteins are retained throughout the development of the desert locust Schistocerca gregaria. Curr Res Insect Sci 3:100053","journal-title":"Curr Res Insect Sci"},{"key":"716_CR20","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1016\/0012-1606(86)90010-2","volume":"118","author":"M Caudy","year":"1986","unstructured":"Caudy M, Bentley D (1986) Epithelial cell specialization at a limb segment boundary in the grasshopper embryo. Dev Biol 118:399\u2013402","journal-title":"Dev Biol"},{"key":"716_CR21","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1002\/jmor.10026","volume":"254","author":"RF Chapman","year":"2002","unstructured":"Chapman RF (2002) Development of phenotypic differences in sensillum populations on the antennae of a grasshopper, Schistocerca americana. J Morphol 254:186\u2013194","journal-title":"J Morphol"},{"key":"716_CR22","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/0020-7322(86)90009-7","volume":"15","author":"RF Chapman","year":"1986","unstructured":"Chapman RF, Greenwood M (1986) Changes in distribution and abundance of antennal sensilla during growth of Locusta migratoria L. (Orthoptera: Acrididae). Int J Insect Morphol Embryol 15:83\u201396","journal-title":"Int J Insect Morphol Embryol"},{"key":"716_CR23","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1093\/chemse\/16.6.607","volume":"16","author":"RF Chapman","year":"1991","unstructured":"Chapman RF, Lee JC (1991) Environmental effects on numbers of peripheral chemoreceptors on the antenna of a grasshopper. Chem Senses 16:607\u2013616","journal-title":"Chem Senses"},{"key":"716_CR24","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1007\/BF02708435","volume":"28","author":"H-H Chen","year":"2003","unstructured":"Chen H-H, Zhao Y-X, Kang L (2003) Antennal sensilla of grasshoppers (Orthoptera: Acrididae) in relation to food preferences and habits. J Biosci 28:743\u2013752","journal-title":"J Biosci"},{"key":"716_CR25","doi-asserted-by":"publisher","first-page":"7272","DOI":"10.1523\/JNEUROSCI.14-12-07272.1994","volume":"14","author":"CJ Desai","year":"1994","unstructured":"Desai CJ, Popova E, Zinn K (1994) A Drosophila receptor tyrosine phosphatase expressed in the embryonic CNS and larval optic lobes is a member of a set of proteins bearing the \u201cHRP\u201d carbohydrate epitope. J Neurosci 14:7272\u20137283","journal-title":"J Neurosci"},{"key":"716_CR26","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1007\/s00427-014-0485-9","volume":"225","author":"E Ehrhardt","year":"2015","unstructured":"Ehrhardt E, Liu Y, Boyan GS (2015) Axogenesis in the antennal nervous system of the grasshopper Schistocerca gregaria revisited: the base pioneers. Dev Genes Evol 225:39\u201345","journal-title":"Dev Genes Evol"},{"key":"716_CR27","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.asd.2015.11.001","volume":"45","author":"EE Ehrhardt","year":"2016","unstructured":"Ehrhardt EE, Graf P, Kleele T, Liu Y, Boyan GS (2016) Fates of identified pioneer cells in the developing antennal nervous system of the grasshopper Schistocerca gregaria. Arthr Struct Dev 45:23\u201330","journal-title":"Arthr Struct Dev"},{"key":"716_CR28","doi-asserted-by":"publisher","first-page":"1548","DOI":"10.1016\/j.cub.2005.07.066","volume":"15","author":"E Fishilevich","year":"2005","unstructured":"Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548\u20131553","journal-title":"Curr Biol"},{"key":"716_CR29","doi-asserted-by":"publisher","first-page":"1263","DOI":"10.1038\/2251263a0","volume":"225","author":"M Gewecke","year":"1970","unstructured":"Gewecke M (1970) Antennae: another wind-sensitive receptor in locusts. Nature 225:1263\u20131264","journal-title":"Nature"},{"key":"716_CR30","doi-asserted-by":"publisher","first-page":"908","DOI":"10.1038\/35082144","volume":"411","author":"M G\u00f6pfert","year":"2001","unstructured":"G\u00f6pfert M, Robert D (2001a) Turning the key on Drosophila audition. Nature 411:908","journal-title":"Nature"},{"key":"716_CR31","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1098\/rspb.2000.1376","volume":"268","author":"M G\u00f6pfert","year":"2001","unstructured":"G\u00f6pfert M, Robert D (2001b) Active auditory mechanics in mosquitoes. Proc R Soc Lond B 268:333\u2013339","journal-title":"Proc R Soc Lond B"},{"key":"716_CR32","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1016\/0020-7322(84)90004-7","volume":"13","author":"M Greenwood","year":"1984","unstructured":"Greenwood M, Chapman RF (1984) Differences in numbers of sensilla on the antennae of solitarious and gregarious Locusta migratoria L (Orthoptera: Acrididae). Int J Insect Morphol Embryol 13:295\u2013301","journal-title":"Int J Insect Morphol Embryol"},{"key":"716_CR33","doi-asserted-by":"publisher","first-page":"2138","DOI":"10.1002\/cne.25077","volume":"529","author":"R Grob","year":"2021","unstructured":"Grob R, Tritscher C, Gr\u00fcbel K, Stigloher C, Groh C, Fleischmann PN, R\u00f6ssler W (2021) Johnston\u2019s organ and its central projections in Cataglyphis desert ants. J Comp Neurol 529:2138\u20132155","journal-title":"J Comp Neurol"},{"key":"716_CR34","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1007\/BF00222783","volume":"179","author":"BS Hansson","year":"1996","unstructured":"Hansson BS, Ochieng SA, Grosmaitre X, Anton S, Njagi PGN (1996) Physiological responses and central nervous projections of antennal olfactory neurones in the adult desert locust, Schistocerca gregaria (Orthoptera: Acrididae). J Comp Physiol A 179:157\u2013167","journal-title":"J Comp Physiol A"},{"key":"716_CR35","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1007\/s004120050256","volume":"106","author":"M Hendzel","year":"1997","unstructured":"Hendzel M, Wie Y, Mancini MA, Van Hooser A, Ranali T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348\u2013360","journal-title":"Chromosoma"},{"key":"716_CR36","unstructured":"Henley C (2021) Foundations of neuroscience. Michigan State University Libraries"},{"key":"716_CR37","doi-asserted-by":"publisher","first-page":"3197","DOI":"10.1002\/stem.2123","volume":"33","author":"Y-C Hsu","year":"2015","unstructured":"Hsu Y-C (2015) The theory and practice of lineage tracing. Stem Cells 33:3197\u20133204","journal-title":"Stem Cells"},{"key":"716_CR38","doi-asserted-by":"publisher","first-page":"761","DOI":"10.1242\/dev.124.4.761","volume":"124","author":"K Ito","year":"1997","unstructured":"Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761\u2013771","journal-title":"Development"},{"key":"716_CR39","doi-asserted-by":"publisher","first-page":"644","DOI":"10.1016\/j.cub.2013.03.015","volume":"23","author":"M Ito","year":"2013","unstructured":"Ito M, Masuda N, Shinomiya K, Endo K, Ito K (2013) Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr Biol 23:644\u2013655","journal-title":"Curr Biol"},{"key":"716_CR40","doi-asserted-by":"publisher","first-page":"2700","DOI":"10.1073\/pnas.79.8.2700","volume":"79","author":"LY Jan","year":"1982","unstructured":"Jan LY, Jan YN (1982) Antibodies to horseradish-peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc Natl Acad Sci USA 79:2700\u20132704","journal-title":"Proc Natl Acad Sci USA"},{"key":"716_CR41","doi-asserted-by":"crossref","unstructured":"Jarman AP (2014) Development of the auditory organ (Johnston\u2019s organ) in Drosophila. In: Development of auditory and vestibular systems. Romand R, Varela-Nieto I (eds), Academic Press, pp 31\u201363","DOI":"10.1016\/B978-0-12-408088-1.00002-6"},{"key":"716_CR42","doi-asserted-by":"publisher","first-page":"417","DOI":"10.3389\/fphys.2018.00417","volume":"9","author":"X Jiang","year":"2018","unstructured":"Jiang X, Ryl M, Krieger J, Breer H, Pregitzer P (2018) Odorant Binding Proteins of the desert locust Schistocerca gregaria (Orthoptera, Acrididae): Topographic expression patterns in the antennae. Front Physiol 9:417. https:\/\/doi.org\/10.3389\/fphys.2018.00417","journal-title":"Front Physiol"},{"key":"716_CR43","doi-asserted-by":"publisher","first-page":"317","DOI":"10.1002\/cne.21075","volume":"499","author":"A Kamikouchi","year":"2006","unstructured":"Kamikouchi A, Shimada T, Ito K (2006) Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 499:317\u2013356","journal-title":"J Comp Neurol"},{"key":"716_CR44","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1007\/s00359-023-01616-y","volume":"209","author":"P Kandimalla","year":"2023","unstructured":"Kandimalla P, Omoto JJ, Hong EJ, Hartenstein V (2023) Lineages to circuits: the developmental and evolutionary architecture of information channels into the central complex. J Comp Physiol A 209:679\u2013720","journal-title":"J Comp Physiol A"},{"key":"716_CR45","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1242\/dev.118.2.509","volume":"118","author":"RO Karlstrom","year":"1993","unstructured":"Karlstrom RO, Wilder LP, Bastiani MJ (1993) Lachesin: an immunoglobulin superfamily protein whose expression correlates with neurogenesis in grasshopper embryos. Development 118:509\u2013522","journal-title":"Development"},{"key":"716_CR46","doi-asserted-by":"publisher","first-page":"104212","DOI":"10.1016\/j.isci.2022.104212","volume":"25","author":"IW Keesey","year":"2022","unstructured":"Keesey IW, Zhang J, Depetris-Chauvin A, Obiero GF, Gupta A, Gupta N, Vogel H, Knaden M, Hansson BS (2022) Functional olfactory evolution in Drosophila suzukii and the subgenus Sophophora. Iscience 25:104212","journal-title":"Iscience"},{"key":"716_CR47","doi-asserted-by":"crossref","unstructured":"Keesey IW, Hansson BS (2021) The neuroethology of labeled lines in insect olfactory systems. In: Insect Pheromone Biochemistry and Molecular Biology (2nd ed). Academic Press, pp 285\u2013327","DOI":"10.1016\/B978-0-12-819628-1.00010-9"},{"key":"716_CR48","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1038\/311151a0","volume":"311","author":"KJ Kotrla","year":"1984","unstructured":"Kotrla KJ, Goodman CS (1984) Transient expression of a surface antigen on a small subset of neurones during embryonic development. Nature 311:151\u2013153","journal-title":"Nature"},{"key":"716_CR49","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1016\/0012-1606(85)90069-7","volume":"110","author":"JY Kuwada","year":"1985","unstructured":"Kuwada JY, Goodman CS (1985) Neuronal determination during embryonic development of the grasshopper nervous system. Dev Biol 110:114\u2013126","journal-title":"Dev Biol"},{"key":"716_CR50","doi-asserted-by":"publisher","first-page":"733","DOI":"10.1038\/293733a0","volume":"293","author":"M Locke","year":"1981","unstructured":"Locke M, Huie P (1981) Epidermal feet in insect morphogenesis. Nature 293:733\u2013735","journal-title":"Nature"},{"key":"716_CR51","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1016\/j.conb.2004.07.001","volume":"14","author":"M Luo","year":"2004","unstructured":"Luo M, Katz LC (2004) Encoding pheromonal signals in the mammalian vomeronasal system. Curr Opinion Neurobiol 14:428\u2013434","journal-title":"Curr Opinion Neurobiol"},{"key":"716_CR52","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1152\/physrev.1990.70.1.199","volume":"70","author":"C Masson","year":"1990","unstructured":"Masson C, Mustaparta H (1990) Chemical information processing in the olfactory systems of insects. Physiol Rev 70:199\u2013245","journal-title":"Physiol Rev"},{"key":"716_CR53","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1016\/0003-2697(80)90550-3","volume":"106","author":"P Naimski","year":"1980","unstructured":"Naimski P, Bierzyimageski A, Fikus M (1980) Quantitative fluorescent analysis of different conformational forms of DNA bound to the dye 4\u2019,6-diamidine-2-phenylindole, and separated by gel electrophoresis. Anal Biochem 106:471\u2013475","journal-title":"Anal Biochem"},{"key":"716_CR54","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1007\/s10886-021-01333-3","volume":"48","author":"M Nakano","year":"2022","unstructured":"Nakano M, Morgan-Richards M, Trewick SA, Clavijo-McCormick A (2022) Chemical ecology and olfaction in short-horned grasshoppers (Orthoptera: Acrididae). J Chem Ecol 48:121\u2013140","journal-title":"J Chem Ecol"},{"key":"716_CR55","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.neulet.2015.04.006","volume":"595","author":"H Nishino","year":"2015","unstructured":"Nishino H, Watanabe H, Kamimura I, Yokohari F, Mizunami M (2015) Coarse topographic organization of pheromone-sesnitive afferents from different antennal surfaces in the American cockroach. Neurosci Lett 595:35\u201340","journal-title":"Neurosci Lett"},{"key":"716_CR56","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1046\/j.1365-3032.1999.00107.x","volume":"24","author":"SA Ochieng","year":"1999","unstructured":"Ochieng SA, Hansson BS (1999) Responses of olfactory receptor neurones to behaviourally important odours in gregarious and solitarious desert locust, Schistocerca gregaria. Physiol Entomol 24:28\u201336","journal-title":"Physiol Entomol"},{"key":"716_CR57","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1007\/s004410051022","volume":"291","author":"S Ochieng","year":"1998","unstructured":"Ochieng S, Hallberg E, Hansson B (1998) Fine structure and distribution of antennal sensilla of the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). Cell Tissue Res 291:525\u2013536","journal-title":"Cell Tissue Res"},{"key":"716_CR58","doi-asserted-by":"publisher","first-page":"218032","DOI":"10.1242\/jeb.218032","volume":"223","author":"M Paoli","year":"2020","unstructured":"Paoli M, Nishino H, Couzin-Fuchs E, Galizia CG (2020) Coding of odour and space in the hemimetabolous insect Periplaneta americana. J Exp Biol 223:218032","journal-title":"J Exp Biol"},{"key":"716_CR59","doi-asserted-by":"publisher","first-page":"1189","DOI":"10.1016\/j.cub.2018.02.074","volume":"28","author":"P Patella","year":"2018","unstructured":"Patella P, Wilson RI (2018) Functional maps of mechanosensory features in the Drosophila brain. Current Biol 28:1189\u20131203","journal-title":"Current Biol"},{"key":"716_CR60","doi-asserted-by":"publisher","first-page":"853","DOI":"10.1016\/j.mehy.2011.07.054","volume":"77","author":"JC Pereira Jr","year":"2011","unstructured":"Pereira JC Jr, Alves RC (2011) The labelled-lines principle of the somatosensory physiology might explain the phantom limb phenomenon. Med Hypotheses 77:853\u2013856","journal-title":"Med Hypotheses"},{"key":"716_CR61","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/j.neuron.2007.09.017","volume":"56","author":"CCH Petersen","year":"2017","unstructured":"Petersen CCH (2017) The functional organization of the barrel cortex. Neuron 56:339\u2013355","journal-title":"Neuron"},{"key":"716_CR62","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1002\/jmor.1051010207","volume":"101","author":"EH Slifer","year":"1957","unstructured":"Slifer EH, Prestage JJ, Beams HW (1957) The fine structure of the long basiconic sensory pegs of the grasshopper (Orthoptera, Acrididae) with special reference to those on the antenna. J Morph 101:359\u2013396","journal-title":"J Morph"},{"key":"716_CR63","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1002\/jmor.1051050106","volume":"105","author":"EH Slifer","year":"1959","unstructured":"Slifer EH, Prestage JJ, Beams HW (1959) The chemoreceptors and other sense organs on the antennal flagellum of the grasshopper (Orthoptera; Acrididae). J Morph 105:145\u2013191","journal-title":"J Morph"},{"key":"716_CR64","volume-title":"Principles of insect morphology","author":"RE Snodgrass","year":"1935","unstructured":"Snodgrass RE (1935) Principles of insect morphology. McGraw-Hill, New York"},{"key":"716_CR65","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1038\/nature09867","volume":"471","author":"R Sousa-Nunes","year":"2011","unstructured":"Sousa-Nunes R, Yee LL, Gould AP (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471:508\u2013513","journal-title":"Nature"},{"key":"716_CR66","doi-asserted-by":"publisher","first-page":"1929","DOI":"10.1098\/rspb.2008.1471","volume":"276","author":"NJ Strausfeld","year":"2009","unstructured":"Strausfeld NJ (2009) Brain organization and the origin of insects: an assessment. Proc R Soc B 276:1929\u20131937","journal-title":"Proc R Soc B"},{"key":"716_CR67","doi-asserted-by":"publisher","DOI":"10.2307\/j.ctv1dp0v2h","volume-title":"Arthropod Brains","author":"NJ Strausfeld","year":"2012","unstructured":"Strausfeld NJ (2012) Arthropod Brains. Harvard Univ. Press, Cambridge"},{"key":"716_CR68","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1111\/j.1440-169X.2011.01325.x","volume":"54","author":"A Takagi","year":"2012","unstructured":"Takagi A, Kurita K, Terasawa T, Nakamura T, Bando T, Moriyama Y, Mito T, Noji S, Ohuchi H (2012) Functional analysis of the role of eye absent and sine oculis in the developing eye of the cricket Gryllus bimaculatus. Develop Growth Differ 54:227\u2013240","journal-title":"Develop Growth Differ"},{"key":"716_CR69","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1002\/jemt.20053","volume":"63","author":"SV Todi","year":"2004","unstructured":"Todi SV, Sharma Y, Eberl DF (2004) Anatomical and molecular design of the Drosophila antenna as a flagellar auditory organ. Microsc Res Tech 63:388\u2013399","journal-title":"Microsc Res Tech"},{"key":"716_CR70","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1016\/S0092-8674(00)80582-6","volume":"96","author":"LB Vosshall","year":"1999","unstructured":"Vosshall LB, Amrein H, Rzhetsky MPS, A, Axel R, (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725\u2013736","journal-title":"Cell"},{"key":"716_CR71","doi-asserted-by":"publisher","first-page":"2683","DOI":"10.1002\/cne.24524","volume":"526","author":"H Watanabe","year":"2018","unstructured":"Watanabe H, Koike Y, Tateishi K, Domae M, Nishino H, Yokohari F (2018) Two types of sensory proliferation patterns underlie the formation of spatially tuned olfactory receptive fields in the cockroach Periplaneta americana. J Comp Neurol 526:2683\u20132705","journal-title":"J Comp Neurol"},{"key":"716_CR72","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1111\/j.1469-7998.1975.tb03188.x","volume":"176","author":"JLD Williams","year":"1975","unstructured":"Williams JLD (1975) Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool Lond 176:67\u201386","journal-title":"J Zool Lond"},{"key":"716_CR73","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.asd.2007.05.005","volume":"37","author":"JLD Williams","year":"2008","unstructured":"Williams JLD, Boyan GS (2008) Building the central complex of the grasshopper Schistocerca gregaria: axons pioneering the w, x, y, z tracts project onto the primary commissural fascicle of the brain. Arthr Struct Devel 37:129\u2013140","journal-title":"Arthr Struct Devel"},{"key":"716_CR74","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/j.asd.2004.11.001","volume":"34","author":"JLD Williams","year":"2005","unstructured":"Williams JLD, Guentner M, Boyan GS (2005) Building the central complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w, x, y, z tracts. Arthr Struct Devel 34:97\u2013110","journal-title":"Arthr Struct Devel"},{"key":"716_CR75","first-page":"1525","volume":"518","author":"JM Young","year":"2010","unstructured":"Young JM, Armstrong JD (2010) Building the central complex in Drosophila: the generation and development of distinct neural subsets. J Comp Physiol 518:1525\u20131541","journal-title":"J Comp Physiol"}],"container-title":["Development Genes and Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00427-024-00716-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00427-024-00716-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00427-024-00716-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,5]],"date-time":"2024-07-05T05:16:47Z","timestamp":1720156607000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00427-024-00716-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,1]]},"references-count":75,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,6]]}},"alternative-id":["716"],"URL":"https:\/\/doi.org\/10.1007\/s00427-024-00716-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-3936625\/v1","asserted-by":"object"}]},"ISSN":["0949-944X","1432-041X"],"issn-type":[{"value":"0949-944X","type":"print"},{"value":"1432-041X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,1]]},"assertion":[{"value":"7 February 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"26 April 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 May 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"All experiments strictly followed the guidelines for animal welfare as laid down by the Deutsche Forschungsgemeinschaft (DFG). Accordingly, nymphal and adult locusts were routinely anesthetized by either cold or CO<sub>2<\/sub> prior to experimentation.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Permission has been obtained from the copyright holder to reproduce Fig.\u00a0\n                      \n                      from Slifer et al.\n                      \n                      in modified form. This permission can be provided on request.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Third-party permissions"}}]}}