Neuroarchitecture of the central complex in the Madeira cockroach Rhyparobia maderae: Pontine and columnar neuronal cell types.
Rhyparobia maderae
central complex
insect brain
neuroanatomy
neuronal cell types
Journal
The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
27
07
2023
received:
15
05
2023
accepted:
03
08
2023
medline:
19
9
2023
pubmed:
23
8
2023
entrez:
23
8
2023
Statut:
ppublish
Résumé
Insects have evolved remarkable abilities to navigate over short distances and during long-range seasonal migrations. The central complex (CX) is a navigation center in the insect brain that controls spatial orientation and directed locomotion. It is composed of the protocerebral bridge (PB), the upper (CBU) and lower (CBL) division of the central body, and a pair of noduli. While most of its functional organization and involvement in head-direction coding has been obtained from work on flies, bees, and locusts that largely rely on vision for navigation, little contribution has been provided by work on nocturnal species. To close this gap, we have investigated the columnar organization of the CX in the cockroach Rhyparobia maderae. Rhyparobia maderae is a highly agile nocturnal insect that relies largely but not exclusively on antennal information for navigation. A particular feature of the cockroach CX is an organization of the CBU and CBL into interleaved series of eight and nine columns. Single-cell tracer injections combined with imaging and 3D analysis revealed five systems of pontine neurons connecting columns along the vertical and horizontal axis and 18 systems of columnar neurons with topographically organized projection patterns. Among these are six types of neurons with no correspondence in other species. Many neurons send processes into the anterior lip, a brain area highly reduced in bees and unknown in flies. While sharing many features with the CX in other species, the cockroach CX shows some unique attributes that may be related to the ecological niche of this insect.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1689-1714Informations de copyright
© 2023 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.
Références
Althaus, V., Jahn, S., Massah, A., Stengl, M., & Homberg, U. (2022). 3D-atlas of the brain of the cockroach Rhyparobia maderae. Journal of Comparative Neurology, 530(18), 3126-3156. https://doi.org/10.1002/cne.25396
Arendt, A., Baz, E.-S., & Stengl, M. (2017). Functions of corazonin and histamine in light entrainment of the circadian pacemaker in the Madeira cockroach, Rhyparobia maderae. Journal of Comparative Neurology, 525(5), 1250-1272. https://doi.org/10.1002/cne.24133
Bender, J. A., Pollack, A. J., & Ritzmann, R. E. (2010). Neural activity in the central complex of the insect brain is linked to locomotor changes. Current Biology, 20(10), 921-926. https://doi.org/10.1016/j.cub.2010.03.054
Burdohan, J. A., & Comer, C. M. (1990). An antennal-derived mechanosensory pathway in the cockroach: Descending interneurons as a substrate for evasive behavior. Brain Research, 535(2), 347-352. https://doi.org/10.1016/0006-8993(90)91623-o
Camhi, J. M., & Tom, W. (1978). The escape behavior of the cockroach Periplaneta americana. Journal of Comparative Physiology A, 128(3), 193-201. https://doi.org/10.1007/BF00656852
Currier, T. A., Matheson, A. M., & Nagel, K. I. (2020). Encoding and control of orientation to airflow by a set of Drosophila fan-shaped body neurons. eLife, 9, e61510. https://doi.org/10.7554/eLife.61510
de Vries, L., Pfeiffer, K., Trebels, B., Adden, A. K., Green, K., Warrant, E., & Heinze, S. (2017). Comparison of navigation-related brain regions in migratory versus non-migratory noctuid moths. Frontiers in Behavioral Neuroscience, 11, 158. https://doi.org/10.3389/fnbeh.2017.00158
Domenici, P., Booth, D., Blagburn, J. M., & Bacon, J. P. (2008). Cockroaches keep predators guessing by using preferred escape trajectories. Current Biology, 18(22), 1792-1796. https://doi.org/10.1016/j.cub.2008.09.062
Durier, V., & Rivault, C. (1999). Path integration in cockroach larvae, Blattella germanica (L.) (insect: Dictyoptera): Direction and distance estimation. Animal Learning & Behavior, 27(1), 108-118. https://doi.org/10.3758/BF03199436
el Jundi, B., Pfeiffer, K., Heinze, S., & Homberg, U. (2014). Integration of polarization and chromatic cues in the insect sky compass. Journal of Comparative Physiology A, 200(6), 575-589. https://doi.org/10.1007/s00359-014-0890-6
el Jundi, B., Warrant, E. J., Byrne, M. J., Khaldy, L., Baird, E., Smolka, J., & Dacke, M. (2015). Neural coding underlying the cue preference for celestial orientation. Proceedings of the National Academy of Sciences of the United States of America, 112(36), 11395-11400. https://doi.org/10.1073/pnas.1501272112
el Jundi, B., Warrant, E. J., Pfeiffer, K., & Dacke, M. (2018). Neuroarchitecture of the dung beetle central complex. Journal of Comparative Neurology, 526(16), 2612-2630. https://doi.org/10.1002/cne.24520
Evers, J. F., Schmitt, S., Sibila, M., & Duch, C. (2005). Progress in functional neuroanatomy: Precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. Journal of Neurophysiology, 93(4), 2331-2342. https://doi.org/10.1152/jn.00761.2004
Green, J., Adachi, A., Shah, K. K., Hirokawa, J. D., Magani, P. S., & Maimon, G. (2017). A neural circuit architecture for angular integration in Drosophila. Nature, 546(7656), 101-106. https://doi.org/10.1038/nature22343
Guo, P., & Ritzmann, R. E. (2013). Neural activity in the central complex of the cockroach brain is linked to turning behaviors. Journal of Experimental Biology, 216(Pt. 6), 992-1002. https://doi.org/10.1242/jeb.080473
Hanesch, U., Fischbach, K.-F., & Heisenberg, M. (1989). Neuronal architecture of the central complex in Drosophila melanogaster. Cell and Tissue Research, 257(2), 343-366. https://doi.org/10.1007/BF00261838
Hardcastle, B. J., Omoto, J. J., Kandimalla, P., Nguyen, B.-C. M., Keleş, M. F., Boyd, N. K., Hartenstein, V., & Frye, M. A. (2021). A visual pathway for skylight polarization processing in Drosophila. eLife, 10, e63225. https://doi.org/10.7554/eLife.63225
Harley, C. M., English, B. A., & Ritzmann, R. E. (2009). Characterization of obstacle negotiation behaviors in the cockroach, Blaberus discoidalis. Journal of Experimental Biology, 212(Pt. 10), 1463-1476. https://doi.org/10.1242/jeb.028381
Harley, C. M., & Ritzmann, R. E. (2010). Electrolytic lesions within central complex neuropils of the cockroach brain affect negotiation of barriers. Journal of Experimental Biology, 213(Pt. 16), 2851-2864. https://doi.org/10.1242/jeb.042499
Heinze, S., el Jundi, B., Berg, B. G., Homberg, U., Menzel, R., Pfeiffer, K., Hensgen, R., Zittrell, F., Dacke, M., Warrant, E., Pfuhl, G., Rybak, J., & Tedore, K. (2021). A unified platform to manage, share, and archive morphological and functional data in insect neuroscience. eLife, 10, e65376. https://doi.org/10.7554/eLife.65376
Heinze, S., Florman, J., Asokaraj, S., el Jundi, B., & Reppert, S. M. (2013). Anatomical basis of sun compass navigation II: The neuronal composition of the central complex of the monarch butterfly. Journal of Comparative Neurology, 521(2), 267-298. https://doi.org/10.1002/cne.23214
Heinze, S., & Homberg, U. (2007). Maplike representation of celestial E-vector orientations in the brain of an insect. Science, 315(5814), 995-997. https://doi.org/10.1126/science.1135531
Heinze, S., & Homberg, U. (2008). Neuroarchitecture of the central complex of the desert locust: Intrinsic and columnar neurons. Journal of Comparative Neurology, 511(4), 454-478. https://doi.org/10.1002/cne.21842
Heinze, S., & Homberg, U. (2009). Linking the input to the output: New sets of neurons complement the polarization vision network in the locust central complex. Journal of Neuroscience, 29(15), 4911-4921. https://doi.org/10.1523/JNEUROSCI.0332-09.2009
Heinze, S., & Reppert, S. M. (2011). Sun compass integration of skylight cues in migratory monarch butterflies. Neuron, 69(2), 345-358. https://doi.org/10.1016/j.neuron.2010.12.025
Heinze, S., & Reppert, S. M. (2012). Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain. Journal of Comparative Neurology, 520(8), 1599-1628. https://doi.org/10.1002/cne.23054
Hensgen, R., Dippel, S., Hümmert, S., Jahn, S., Seyfarth, J., & Homberg, U. (2022). Myoinhibitory peptides in the central complex of the locust Schistocerca gregaria and colocalization with locustatachykinin-related peptides. Journal of Comparative Neurology, 530(15), 2782-2801. https://doi.org/10.1002/cne.25374
Hensgen, R., England, L., Homberg, U., & Pfeiffer, K. (2021). Neuroarchitecture of the central complex in the brain of the honeybee: Neuronal cell types. Journal of Comparative Neurology, 529(1), 159-186. https://doi.org/10.1002/cne.24941
Hensgen, R., Göthe, J., Jahn, S., Hümmert, S., Schneider, K. L., Takahashi, N., Pegel, U., Gotthardt, S., & Homberg, U. (2021). Organization and neural connections of the lateral complex in the brain of the desert locust. Journal of Comparative Neurology, 529(15), 3533-3560. https://doi.org/10.1002/cne.25209
Hofer, S., & Homberg, U. (2006). Orcokinin immunoreactivity in the accessory medulla of the cockroach Leucophaea maderae. Cell and Tissue Research, 325(3), 589-600. https://doi.org/10.1007/s00441-006-0155-y
Homberg, U. (1985). Interneurones of the central complex in the bee brain (Apis mellifera, L.). Journal of Insect Physiology, 31(3), 251-264. https://doi.org/10.1016/0022-1910(85)90127-1
Homberg, U. (1991). Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. Journal of Comparative Neurology, 303(2), 245-254. https://doi.org/10.1002/cne.903030207
Homberg, U., Hensgen, R., Jahn, S., Pegel, U., Takahashi, N., Zittrell, F., & Pfeiffer, K. (2023). The sky compass network in the brain of the desert locust. Journal of Comparative Physiology A, 209, 641-662. https://doi.org/10.1007/s00359-022-01601-x
Homberg, U., Humberg, T.-H., Seyfarth, J., Bode, K., & Quintero Pérez, M. (2018). GABA immunostaining in the central complex of dicondylian insects. Journal of Comparative Neurology, 526(14), 2301-2318. https://doi.org/10.1002/cne.24497
Homberg, U., Reischig, T., & Stengl, M. (2003). Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiology International, 20(4), 577-591. https://doi.org/10.1081/CBI-120022412
Honkanen, A., Adden, A., da Silva Freitas, J., & Heinze, S. (2019). The insect central complex and the neural basis of navigational strategies. Journal of Experimental Biology, 222(1), jeb188854. https://doi.org/10.1242/jeb.188854
Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D., Takemura, S.-Y., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., Hermundstad, A. M., Rubin, G. M., & Jayaraman, V. (2021). A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection. eLife, 10, e66039. https://doi.org/10.7554/eLife.66039
Immonen, E.-V., Dacke, M., Heinze, S., & el Jundi, B. (2017). Anatomical organization of the brain of a diurnal and a nocturnal dung beetle. Journal of Comparative Neurology, 525(8), 1879-1908. https://doi.org/10.1002/cne.24169
Ito, K., Shinomiya, K., Ito, M., Armstrong, J. D., Boyan, G., Hartenstein, V., Harzsch, S., Heisenberg, M., Homberg, U., Jenett, A., Keshishian, H., Restifo, L. L., Rössler, W., Simpson, J. H., Strausfeld, N. J., Strauss, R., & Vosshall, L. B. (2014). A systematic nomenclature for the insect brain. Neuron, 81(4), 755-765. https://doi.org/10.1016/j.neuron.2013.12.017
Kaiser, A., Hensgen, R., Tschirner, K., Beetz, E., Wüstenberg, H., Pfaff, M., Mota, T., & Pfeiffer, K. (2022). A three-dimensional atlas of the honeybee central complex, associated neuropils and peptidergic layers of the central body. Journal of Comparative Neurology, 530(14), 2416-2438. https://doi.org/10.1002/cne.25339
Kathman, N. D., Kesavan, M., & Ritzmann, R. E. (2014). Encoding wide-field motion and direction in the central complex of the cockroach Blaberus discoidalis. Journal of Experimental Biology, 217(Pt. 22), 4079-4090. https://doi.org/10.1242/jeb.112391
Klagges, B. R., Heimbeck, G., Godenschwege, T. A., Hofbauer, A., Pflugfelder, G. O., Reifegerste, R., Reisch, D., Schaupp, M., Buchner, S., & Buchner, E. (1996). Invertebrate synapsins: A single gene codes for several isoforms in Drosophila. Journal of Neuroscience, 16(10), 3154-3165. https://doi.org/10.1523/JNEUROSCI.16-10-03154.1996
Lin, C.-Y., Chuang, C.-C., Hua, T.-E., Chen, C.-C., Dickson, B. J., Greenspan, R. J., & Chiang, A.-S. (2013). A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. Cell Reports, 3(5), 1739-1753. https://doi.org/10.1016/j.celrep.2013.04.022
Lu, J., Behbahani, A. H., Hamburg, L., Westeinde, E. A., Dawson, P. M., Lyu, C., Maimon, G., Dickinson, M. H., Druckmann, S., & Wilson, R. I. (2022). Transforming representations of movement from body- to world-centric space. Nature, 601(7891), 98-104. https://doi.org/10.1038/s41586-021-04191-x
Lyu, C., Abbott, L. F., & Maimon, G. (2022). Building an allocentric travelling direction signal via vector computation. Nature, 601(7891), 92-97. https://doi.org/10.1038/s41586-021-04067-0
Martin, J. P., Guo, P., Mu, L., Harley, C. M., & Ritzmann, R. E. (2015). Central-complex control of movement in the freely walking cockroach. Current Biology, 25(21), 2795-2803. https://doi.org/10.1016/j.cub.2015.09.044
Muren, J. E., Lundquist, C. T., & Nässel, D. R. (1995). Abundant distribution of locustatachykinin-like peptide in the nervous system and intestine of the cockroach Leucophaea maderae. Philosophical Transactions of the Royal Society of London Series B, 348, 423-444. https://doi.org/10.1098/rstb.1995.0079
Müller, M., Homberg, U., & Kühn, A. (1997). Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell and Tissue Research, 288(1), 159-176. https://doi.org/10.1007/s004410050803
Nässel, D. R., Passier, P. C., Elekes, K., Dircksen, H., Vullings, H. G., & Cantera, R. (1995). Evidence that locustatachykinin I is involved in release of adipokinetic hormone from locust corpora cardiaca. Regulatory Peptides, 57(3), 297-310. https://doi.org/10.1016/0167-0115(95)00043-B
Neuser, K., Triphan, T., Mronz, M., Poeck, B., & Strauss, R. (2008). Analysis of a spatial orientation memory in Drosophila. Nature, 453(7199), 1244-1247. https://doi.org/10.1038/nature07003
Pegel, U., Pfeiffer, K., & Homberg, U. (2018). Integration of celestial compass cues in the central complex of the locust brain. Journal of Experimental Biology, 221(Pt. 2), jeb171207. https://doi.org/10.1242/jeb.171207
Pegel, U., Pfeiffer, K., Zittrell, F., Scholtyssek, C., & Homberg, U. (2019). Two compasses in the central complex of the locust brain. Journal of Neuroscience, 39(16), 3070-3080. https://doi.org/10.1523/JNEUROSCI.0940-18.2019
Petri, B., Stengl, M., Würden, S., & Homberg, U. (1995). Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea maderae. Cell and Tissue Research, 282(1), 3-19. https://doi.org/10.1007/BF00319128
Pfeiffer, K. (2023). The neuronal building blocks of the navigational toolkit in the central complex of insects. Current Opinion in Insect Science, 55, 100972. https://doi.org/10.1016/j.cois.2022.100972
Pfeiffer, K., & Homberg, U. (2014). Organization and functional roles of the central complex in the insect brain. Annual Review of Entomology, 59, 165-184. https://doi.org/10.1146/annurev-ento-011613-162031
Predel, R., Rapus, J., & Eckert, M. (2001). Myoinhibitory neuropeptides in the American cockroach. Peptides, 22(2), 199-208. https://doi.org/10.1016/S0196-9781(00)00383-1
Rayshubskiy, A., Holtz, S. L., D'Alessandro, I., Li, A. A., Vanderbeck, Q. X., Haber, I. S., Gibb, P. W., & Wilson, R. I. (2020). Neural circuit mechanisms for steering control in walking Drosophila. bioRxiv. https://doi.org/10.1101/2020.04.04.024703
Ritzmann, R. E. (1984). The cockroach escape response. In R. C. Eaton (Ed.), Neural mechanisms of startle behavior (pp. 93-131). Springer. https://doi.org/10.1007/978-1-4899-2286-1
Ritzmann, R. E., Harley, C. M., Daltorio, K. A., Tietz, B. R., Pollack, A. J., Bender, J. A., Guo, P., Horomanski, A. L., Kathman, N. D., Nieuwoudt, C., Brown, A. E., & Quinn, R. D. (2012). Deciding which way to go. How do insects alter movements to negotiate barriers? Frontiers in Neuroscience, 6, 97. https://doi.org/10.3389/fnins.2012.00097
Ritzmann, R. E., Ridgel, A. L., & Pollack, A. J. (2008). Multi-unit recording of antennal mechano-sensitive units in the central complex of the cockroach, Blaberus discoidalis. Journal of Comparative Physiology A, 194(4), 341-360. https://doi.org/10.1007/s00359-007-0310-2
Rivault, C., & Durier, V. (2004). Homing in German Cockroaches, Blattella germanica (L.) (Insecta: Dictyoptera): Multi-channelled orientation cues. Ethology, 110(10), 761-777. https://doi.org/10.1111/j.1439-0310.2004.01018.x
Sakura, M., Lambrinos, D., & Labhart, T. (2008). Polarized skylight navigation in insects: Model and electrophysiology of e-vector coding by neurons in the central complex. Journal of Neurophysiology, 99(2), 667-682. https://doi.org/10.1152/jn.00784.2007
Sayre, M. E., Templin, R., Chavez, J., Kempenaers, J., & Heinze, S. (2021). A projectome of the bumblebee central complex. eLife, 10, e68911. https://doi.org/10.7554/eLife.68911
Schmitt, S., Evers, J. F., Duch, C., Scholz, M., & Obermayer, K. (2004). New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks. Neuroimage, 23(4), 1283-1298. https://doi.org/10.1016/j.neuroimage.2004.06.047
Schulze, J., Neupert, S., Schmidt, L., Predel, R., Lamkemeyer, T., Homberg, U., & Stengl, M. (2012). Myoinhibitory peptides in the brain of the cockroach Leucophaea maderae and colocalization with pigment-dispersing factor in circadian pacemaker cells. Journal of Comparative Neurology, 520(5), 1078-1097. https://doi.org/10.1002/cne.22785
Seelig, J. D., & Jayaraman, V. (2015). Neural dynamics for landmark orientation and angular path integration. Nature, 521(7551), 186-191. https://doi.org/10.1038/nature14446
Seelinger, G., & Gagel, S. (1985). On the function of sex pheromone components in Periplaneta americana: Improved odour source localization with periplanone-A. Physiological Entomology, 10(2), 221-234. https://doi.org/10.1111/j.1365-3032.1985.tb00038.x
Stengl, M., Werckenthin, A., & Wei, H. (2015). How does the circadian clock tick in the Madeira cockroach? Current Opinion in Insect Science, 12, 38-45. https://doi.org/10.1016/j.cois.2015.09.007
Stierle, I. E., Getman, M., & Comer, C. M. (1994). Multisensory control of escape in the cockroach Periplaneta americana. I. Initial evidence from patterns of wind-evoked behavior. Journal of Comparative Physiology A, 174, 1-11. https://doi.org/10.1007/BF00192001
Stone, T., Webb, B., Adden, A., Weddig, N. B., Honkanen, A., Templin, R., Wcislo, W., Scimeca, L., Warrant, E., & Heinze, S. (2017). An anatomically constrained model for path integration in the bee brain. Current Biology, 27(20), 3069.e11-3085.e11. https://doi.org/10.1016/j.cub.2017.08.052
Strausfeld, N. J. (1999). A brain region in insects that supervises walking. Progress in Brain Research, 123, 273-284. https://doi.org/10.1016/S0079-6123(08)62863-0
Strauss, R. (2002). The central complex and the genetic dissection of locomotor behaviour. Current Opinion in Neurobiology, 12(6), 633-638. https://doi.org/10.1016/S0959-4388(02)00385-9
Timm, J., Scherner, M., Matschke, J., Kern, M., & Homberg, U. (2021). Tyrosine hydroxylase immunostaining in the central complex of dicondylian insects. Journal of Comparative Neurology, 529(12), 3131-3154. https://doi.org/10.1002/cne.25151
Turner-Evans, D., Wegener, S., Rouault, H., Franconville, R., Wolff, T., Seelig, J. D., Druckmann, S., & Jayaraman, V. (2017). Angular velocity integration in a fly heading circuit. eLife, 6, e23496. https://doi.org/10.7554/eLife.23496
Varga, A. G., Kathman, N. D., Martin, J. P., Guo, P., & Ritzmann, R. E. (2017). Spatial navigation and the central complex: Sensory acquisition, orientation, and motor control. Frontiers in Behavioral Neuroscience, 11, 4. https://doi.org/10.3389/fnbeh.2017.00004
Varga, A. G., & Ritzmann, R. E. (2016). Cellular basis of head direction and contextual cues in the insect brain. Current Biology, 26(14), 1816-1828. https://doi.org/10.1016/j.cub.2016.05.037
Veenstra, J. A., & Hagedorn, H. H. (1993). Sensitive enzyme immunoassay for Manduca allatotropin and the existence of an allatotropin-immunoreactive peptide in Periplaneta americana. Archives of Insect Biochemistry and Physiology, 23(3), 99-109. https://doi.org/10.1002/arch.940230302
Veenstra, J. A., Lau, G. W., Agricola, H. J., & Petzel, D. H. (1995). Immunohistological localization of regulatory peptides in the midgut of the female mosquito Aedes aegypti. Histochemistry and Cell Biology, 104(5), 337-347. https://doi.org/10.1007/BF01458127
Vitzthum, H., & Homberg, U. (1998). Immunocytochemical demonstration of locustatachykinin-related peptides in the central complex of the locust brain. Journal of Comparative Neurology, 390(4), 455-469. https://doi.org/10.1002/(SICI)1096-9861(19980126)390:4<455::AID-CNE1>3.0.CO;2-%23
von Hadeln, J., Hensgen, R., Bockhorst, T., Rosner, R., Heidasch, R., Pegel, U., Quintero Pérez, M., & Homberg, U. (2020). Neuroarchitecture of the central complex of the desert locust: Tangential neurons. Journal of Comparative Neurology, 528(6), 906-934. https://doi.org/10.1002/cne.24796
Watson, J. T., Ritzmann, R. E., & Pollack, A. J. (2002). Control of climbing behavior in the cockroach, Blaberus discoidalis. II. Motor activities associated with joint movement. Journal of Comparative Physiology A, 188(1), 55-69. https://doi.org/10.1007/s00359-002-0278-x
Watson, J. T., Ritzmann, R. E., Zill, S. N., & Pollack, A. J. (2002). Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics. Journal of Comparative Physiology A, 188(1), 39-53. https://doi.org/10.1007/s00359-002-0277-y
Wei, H., el Jundi, B., Homberg, U., & Stengl, M. (2010). Implementation of pigment-dispersing factor-immunoreactive neurons in a standardized atlas of the brain of the cockroach Leucophaea maderae. Journal of Comparative Neurology, 518(20), 4113-4133. https://doi.org/10.1002/cne.22471
Willis, M. A., & Avondet, J. L. (2005). Odor-modulated orientation in walking male cockroaches Periplaneta americana, and the effects of odor plumes of different structure. Journal of Experimental Biology, 208(Pt. 4), 721-735. https://doi.org/10.1242/jeb.01418
Wolff, T., Iyer, N. A., & Rubin, G. M. (2015). Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4-based dissection of protocerebral bridge neurons and circuits. Journal of Comparative Neurology, 523(7), 997-1037. https://doi.org/10.1002/cne.23705
Wolff, T., & Rubin, G. M. (2018). Neuroarchitecture of the Drosophila central complex: A catalog of nodulus and asymmetrical body neurons and a revision of the protocerebral bridge catalog. Journal of Comparative Neurology, 526(16), 2585-2611. https://doi.org/10.1002/cne.24512
Zittrell, F., Pabst, K., Carlomagno, E., Rosner, R., Pegel, U., Endres, D. M., & Homberg, U. (2023). Integration of optic flow into the sky compass network in the brain of the desert locust. Frontiers in Neural Circuits, 17, 338. https://doi.org/10.3389/fncir.2023.1111310