Insect-like organization of the stomatopod central complex: Functional and phylogenetic implications

Frontiers in Behavioral Neuroscience

Volumn 11, Issue , 2017, Pages

  Thoen, Hanne H ^a   Marshall, Justin ^a   Wolff, Gabriella H ^b   Strausfeld, Nicholas J ^c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Central complex; Crustaceans; Evolution; Eye movements; Insects; Stomatopod

Indexed keywords

AXON; EYE MOVEMENT; INSECT; LOCOMOTION; NEUROPIL; NONHUMAN; PHOTORECEPTOR CELL; SHRIMP; SWIMMING;

EID: 85012044298     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2017.00012     Document Type: Article

References (105)

1. Andrew, D. R., Brown, S. M., and Strausfeld, N. J. (2012). The minute brain of the copepod Tigriopus californicus supports a complex ancestral ground pattern of the tetraconate cerebral nervous systems. J. Comp. Neurol. 520, 3446–3470. doi: 10.1002/cne.23099
2. Bausenwein, B., Wolf, R., and Heisenberg, M. (1986). Genetic dissection of optomotor behavior in Drosophila melanogaster studies on wild-type and the mutant optomotor-blind H31. J. Neurogenet. 3, 87–109. doi: 10.3109/01677068609106897
3. Bender, J. A., Pollack, A. J., and Ritzmann, R. E. (2010). Neural activity in the central complex of the insect brain is linked to locomotor changes. Curr. Biol. 20, 921–926. doi: 10.1016/j.cub.2010.03.054
4. Bodian, D. (1936). A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat. Rec. 65, 89–97. doi: 10.1002/ar.10906 50110
5. Bok, M. J. (2012). Available online at: https://www.youtube.com/watch?v=ZhlAYDvAeFk
6. Boyan, G., Williams, L., and Liu, Y. (2015). Conserved patterns of axogenesis in the panarthropod brain. Arthropod Struct. Dev. 44, 101–112. doi: 10.1016/j.asd.2014.11.003
7. Buchanan, S. M., Kain, J. S., and de Bivort, B. L. (2015). Neuronal control of locomotor handedness in Drosophila. Proc. Natl. Acad. Sci. U S A 112, 6700–6705. doi: 10.1073/pnas.1500804112
8. Chiou, T. H., Kleinlogel, S., Cronin, T., Caldwell, R., Loeffler, B., Siddiqi, A., et al. (2008). Circular polarization vision in a stomatopod crustacean. Curr. Biol. 18, 429–434. doi: 10.1016/j.cub.2008.02.066
9. Cronin, T. W., and Marshall, N. J. (1989a). Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. J. Comp. Physiol. A 166, 261–275. doi: 10.1007/bf00193471
10. Cronin, T. W., and Marshall, N. J. (1989b). A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature 339, 137–140. doi: 10.1038/339137a0
11. Cronin, T. W., Marshall, N. J., and Land, M. F. (1991). Optokinesis in gonodactyloid mantis shrimps (Crustacea; Stomatopoda; Gonodactylidae). J. Comp. Physiol. A 168, 233–240. doi: 10.1007/bf00218415
12. Cronin, T. W., Marshall, N. J., Quinn, C. A., and King, C. A. (1994). Ultraviolet photoreception in mantis shrimp. Vision Res. 34, 1443–1452. doi: 10.1016/0042-6989(94)90145-7
13. Cronin, T. W., Nair, J. N., Doyle, R. D., and Caldwell, R. L. (1988). Ocular tracking of rapidly moving visual targets by stomatopod crustaceans. J. Exp. Biol. 138, 155–179.
14. Daly, I. M., How, M. J., Partridge, J. C., Temple, S. E., Marshall, N. J., Cronin, T. W., et al. (2016). Dynamic polarization vision in mantis shrimps. Nat. Commun. 7:12140. doi: 10.1038/ncomms12140
15. Derby, C. D., Fortier, J. K., Harrison, P. J. H., and Cate, H. S. (2003). The peripheral and central antennular pathway of the Caribbean stomatopod crustacean Neogonodactylus oerstedii. Arthropod Struct. Dev. 32, 175–188. doi: 10.1016/s1467-8039(03)00048-3
16. Ehmer, B., and Gronenberg, W. (2002). Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J. Comp. Neurol. 451, 362–373. doi: 10.1002/cne.10355
17. Fanenbruck, M., Harzsch, S., and Wägele, J. W. (2004). The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc. Natl. Acad. Sci. U S A 101, 3868–3873. doi: 10.1073/pnas.03062 12101
18. Fiore, V. G., Dolan, R. J., Strausfeld, N. J., and Hirth, F. (2015). Evolutionarily conserved mechanisms for the selection and maintenance of behavioural activity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370:20150053. doi: 10.1098/rstb. 2015.0053
19. Fritsches, K. A., and Marshall, J. (1999). A new category of eye movements in a small fish. Curr. Biol. 9, R272–R273. doi: 10.1016/s0960-9822(99) 80176-6
20. Gagnon, Y. L., Templin, R. M., How, M. J., and Marshall, N. J. (2015). Circularly polarized light as a communication signal in mantis shrimps. Curr. Biol. 25, 3074–3078. doi: 10.1016/j.cub.2015.10.047
21. Guo, P. Y., and Ritzmann, R. E. (2013). Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J. Exp. Biol. 216, 992–1002. doi: 10.1242/jeb.080473
22. Hanesch, U., Fischbach, K.-F., and Heisenberg, M. (1989). Neuronal architecture of the central complex in Drosophila Melanogaster. Cell Tissue Res. 257, 343–366. doi: 10.1007/Bf00261838
23. Harzsch, S., and Hansson, B. S. (2008). Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell. BMC Neurosci. 9:58. doi: 10.1186/1471-2202-9-58
24. Heinze, S., and Homberg, U. (2007). Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315, 995–997. doi: 10.1126/science.1135531
25. Heinze, S., and Homberg, U. (2008). Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J. Comp. Neurol. 511, 454–478. doi: 10.1002/cne.21842
26. Heinze, S., and Reppert, S. M. (2011). Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345–358. doi: 10.1016/j.neuron. 2010.12.025
27. Held, M., Berz, A., Hensgen, R., Muenz, T. S., Scholl, C., Rössler, W., et al. (2016). Microglomerular synaptic complexes in the sky-compass network of the honeybee connect parallel pathways from the anterior optic tubercle to the central complex. Front. Behav. Neurosci. 10:186. doi: 10.3389/fnbeh.2016. 00186
28. Herbert, Z., Rauser, S., Williams, L., Kapan, N., Güntner, M., Walch, A., et al. (2010). Developmental expression of neuromodulators in the central complex of the grasshopper Schistocerca gregaria. J. Morphol. 271, 1509–1526. doi: 10.1002/jmor.10895
29. Heuer, C. M., Müller, C. H., Todt, C., and Loesel, R. (2010). Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida. Front. Zool. 7:13. doi: 10.1186/1742-9994-7-13
30. Homberg, U. (1985). Interneurones of the central complex in the bee brain (Apis-Mellifera, L). J. Insect Physiol. 31, 251–264. doi: 10.1016/0022-1910(85) 90127-1
31. Homberg, U. (2008). Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct. Dev. 37, 347–362. doi: 10.1016/j. asd.2008.01.008
32. Homberg, U., Heinze, S., Pfeiffer, K., Kinoshita, M., and el Jundi, B. (2011). Central neural coding of sky polarization in insects. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 680–687. doi: 10.1098/rstb.2010.0199
33. Honegger, H. W., and Schürmann, F. W. (1975). Cobalt sulphide staining of optic fibres in the brain of the cricket, Gryllus campestris. Cell Tissue Res. 159, 213–225. doi: 10.1007/bf00219157
34. Huber, F. (1959). Auslösung von Bewegungsmustern durch elektrische Reizung des Oberschlundganglions bei Orthopteren (Saltatoriab: Gryllidae, Acridiidae). Verh. Dtsch. Zool. Ges. 1959, 248–269.
35. Huber, F. (1960). Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirnes bei der Fortbewegung und der Lauterzeugung der Grillen. Vergl. Physiol. 44, 60–132. doi: 10.1007/BF002 97863
36. Ilius, M., Wolf, R., and Heisenberg, M. (2007). The central complex of Drosophila melanogaster is involved in flight control: studies on mutants and mosaics of the gene ellipsoid body open. J. Neurogenet. 21, 321–338. doi: 10.1080/01677060701693503
37. Ito, K., Shinomiya, K., Ito, M., Armstrong, J. D., Boyan, G., Hartenstein, V., et al. (2014). A systematic nomenclature for the insect brain. Neuron 81, 755–765. doi: 10.1016/j.neuron.2013.12.017
38. Iwano, M., Hill, E. S., Mori, A., Mishima, T., Mishima, T., Ito, K., et al. (2010). Neurons associated with the flip-flop activity in the lateral accessory lobe and ventral protocerebrum of the silkworm moth brain. J. Comp. Neurol. 518, 366–388. doi: 10.1002/cne.22224
39. Jones, J. (1994). Architecture and composition of the muscles that drive stomatopod eye-movements. J. Exp. Biol. 188, 317–331.
40. Kahsai, L., Martin, J. R., and Winther, Å. M. E. (2010). Neuropeptides in the Drosophila central complex in modulation of locomotor behavior. J. Exp. Biol. 213, 2256–2265. doi: 10.1242/jeb.043190
41. Kahsai, L., and Winther, Å. M. E. (2011). Chemical neuroanatomy of the Drosophila central complex: distribution of multiple neuropeptides in relation to neurotransmitters. J. Comp. Neurol. 519, 290–315. doi: 10.1002/cne. 22520
42. Kenning, M., Müller, C., Wirkner, C. S., and Harzsch, S. (2013). The Malacostraca (Crustacea) from a neurophylogenetic perspective: new insights from brain architecture in Nebalia herbstii Leach, 1814 (Leptostraca, Phyllocarida). Zool. Anz. 252, 319–336. doi: 10.1016/j.jcz.2012.09.003
43. Klagges, B. R. E., Heimbeck, G., Godenschwege, T. A., Hofbauer, A., Pflugfelder, G. O., Reifegerste, R., et al. (1996). Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J. Neurosci. 16, 3154–3165.
44. Kleinlogel, S., and Marshall, N. J. (2006). Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean Gonodactylus chiragra. J. Exp. Biol. 209, 4262–4272. doi: 10.1242/jeb. 02499
45. Kral, K., Vernik, M., and Devetak, D. (2000). The visually controlled prey-capture behaviour of the European mantispid Mantispa styriaca. J. Exp. Biol. 203, 2117–2123.
46. Kumar, J. P., and Moses, K. (2001). EGF receptor and notch signaling act upstream of Eyeless/Pax6 to control eye specification. Cell 104, 687–697. doi: 10.1016/s0092-8674(01)00265-3
47. Kunst, M., Pförtner, R., Aschenbrenner, K., and Heinrich, R. (2011). Neurochemical architecture of the central complex related to its function in the control of grasshopper acoustic communication. PLoS One 6:e25613. doi: 10.1371/journal.pone.0025613
48. Labandeira, C. C., Beall, B. S., and Hueber, F. M. (1988). Early insect diversification–evidence from a lower devonian bristletail from Quebec. Science 242, 913–916. doi: 10.1126/science.242.4880.913
49. Land, M. F., Marshall, J. N., Brownless, D., and Cronin, T. W. (1990). The eye-movements of the mantis shrimp Odontodactylus-Scyllarus (Crustacea, Stomatopoda). J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 167, 155–166. doi: 10.1007/bf00188107
50. Li, Y., and Strausfeld, N. J. (1997). Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J. Comp. Neurol. 387, 631–650. doi: 10.1002/(SICI)1096-9861(19971103)387:4<631::AID-CNE9>3.3.CO;2-Z
51. Li, Y., and Strausfeld, N. J. (1999). Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. J. Comp. Neurol. 409, 647–663. doi: 10.1002/(SICI)1096-9861(19990712)409:4<647::AID-CNE9>3.0. CO;2-3
52. Lin, C. Y., Chuang, C. C., Hua, T. E., Chen, C. C., Dickson, B. J., Greenspan, R. J., et al. (2013). A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. Cell Rep. 3, 1739–1753. doi: 10.1016/j.celrep.2013.04.022
53. Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., et al. (2006). Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551–556. doi: 10.1038/nature04381
54. Loesel, R., Nässel, D. R., and Strausfeld, N. J. (2002). Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct. Dev. 31, 77–91. doi: 10.1016/s1467-8039(02)00017-8
55. Ma, X., Hou, X., Edgecombe, G. D., and Strausfeld, N. J. (2012). Complex brain and optic lobes in an early Cambrian arthropod. Nature 490, 258–261. doi: 10.1038/nature11495
56. Marshall, N. J. (1988). A unique colour and polarization vision system in mantis shrimps. Nature 333, 557–560. doi: 10.1038/333557a0
57. Marshall, J., Cronin, T. W., and Kleinlogel, S. (2007). Stomatopod eye structure and function: a review. Arthropod Struct. Dev. 36, 420–448. doi: 10.1016/j.asd. 2007.01.006
58. Marshall, J., Cronin, T. W., Shashar, N., and Land, M. (1999). Behavioural evidence for polarisation vision in stomatopods reveals a potential channel for communication. Curr. Biol. 9, 755–758. doi: 10.1016/s0960-9822(99) 80336-4
59. Marshall, N. J., and Diebel, C. (1995). ‘Deep-sea spiders’ that walk through the water. J. Exp. Biol. 198, 1371–1379.
60. Marshall, N. J., Jones, J. P., and Cronin, T. W. (1996). Behavioural evidence for colour vision in stomatopod crustaceans. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 179, 473–481. doi: 10.1007/bf00192314
61. Marshall, N. J., and Land, M. F. (1993). Some optical-features of the eyes of stomatopods. 2. ommatidial design, sensitivity and habitat. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 173, 583–594. doi: 10.1007/bf00197766
62. Marshall, N. J., Land, M. F., and Cronin, T. W. (2014). Shrimps that pay attention: saccadic eye movements in stomatopod crustaceans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369:20130042. doi: 10.1098/rstb.2013.0042
63. Marshall, N. J., Land, M. F., King, C. A., and Cronin, T. W. (1991a). The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarized light. Philos. Trans. R. Soc. Lond. B Biol. Sci. 334, 33–56. doi: 10.1098/rstb.1991.0096
64. Marshall, N. J., Land, M. F., King, C. A., and Cronin, T. W. (1991b). The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Philos. Trans. R. Soc. Lond. B Biol. Sci. 334, 57–84. doi: 10.1098/rstb.1991.0097
65. Martin, J. P., Guo, P., Mu, L., Harley, C. M., and Ritzmann, R. E. (2015). Central complex control of movement in the freely walking cockroach. Curr. Biol. 25, 2795–2803. doi: 10.1016/j.cub.2015.09.044
66. Mellon, D. (1977). Anatomy and motor-nerve distribution of eye-muscles in crayfish. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 121, 349–366. doi: 10.1007/bf00613014
67. Milne-Edwards, A. (1864). Sur un cas de transformation du pedoncle oculaire en une antenne, observe chez une Langouste. Comptes Rendus Academie Sci. 59, 710–712.
68. Mobbs, P. G. (1985). ‘‘Brain structure,’’ in Comprehensive Insect Physiology Biochemistry and Pharmacology, Nervous System: Structure and Motor Function, (Vol. 5) eds G. A. Kerkut and L. I. Gilbert (Oxford: Pergamon), 299–370.
69. Namiki, S., and Kanzaki, R. (2016). Comparative neuroanatomy of the lateral accessory lobe in the insect brain. Front. Physiol. 7:244. doi: 10.3389/fphys.2016. 00244
70. Neuser, K., Triphan, T., Mronz, M., Poeck, B., and Strauss, R. (2008). Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244–1247. doi: 10.1038/nature07003
71. Oakley, T. H., Wolfe, J. M., Lindgren, A. R., and Zaharoff, A. K. (2012). Phylotranscriptomics to bring the understudied into the fold: monophyletic ostracoda, fossil placement and pancrustacean phylogeny. Mol. Biol. Evol. 30, 215–233. doi: 10.1093/molbev/mss216
72. Ofstad, T. A., Zuker, C. S., and Reiser, M. B. (2011). Visual place learning in Drosophila melanogaster. Nature 474, 204–207. doi: 10.1038/nature10131
73. Pfeiffer, K., and Homberg, U. (2015). Organization and functional roles of the central complex in the insect brain. Ann. Rev. Entomol. 59, 165–184. doi: 10.1146/annurev-ento-011613-162031
74. Phillips-Portillo, J. (2012). The central complex of the flesh fly, Neobellieria bullata: recordings and morphologies of protocerebral inputs and small-field neurons. J. Comp. Neurol. 520, 3088–3104. doi: 10.1002/cne.23134
75. Phillips-Portillo, J., and Strausfeld, N. J. (2012). Representation of the brain’s superior protocerebrum of the flesh fly, Neobellieria bullata, in the central body. J. Comp. Neurol. 520, 3070–3087. doi: 10.1002/cne.23094
76. Power, M. E. (1943). The brain of Drosophila melanogaster. J. Morphol. 72, 517–559. doi: 10.1002/jmor.1050720306
77. Ridgel, A. L., Alexander, B. E., and Ritzmann, R. E. (2007). Descending control of turning behavior in the cockroach, Blaberus discoidalis. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 193, 385–402. doi: 10.1007/s00359-006-0193-7
78. Ritzmann, R. E., Harley, C. M., Daltorio, K. A., Tietz, B. R., Pollack, A. J., Bender, J. A., et al. (2012). Deciding which way to go: how do insects alter movements to negotiate barriers? Front. Neurosci. 6:97. doi: 10.3389/fnins. 2012.00097
79. Ritzmann, R. E., Ridgel, A. L., and Pollack, A. J. (2008). Multi-unit recording of antennal mechano-sensitive units in the central complex of the cockroach, Blaberus discoidalis. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 194, 341–360. doi: 10.1007/s00359-007-0310-2
80. Sandeman, D. C., Sandeman, R. E., and Aitken, A. R. (1988). Atlas of serotonincontaining neurons in the optic lobes and brain of the crayfish, Cherax destructor. J. Comp. Neurol. 269, 465–478. doi: 10.1002/cne.902690402
81. Sandeman, D., Sandeman, R., Derby, C., and Schmidt, M. (1992). Morphology of the brain of crayfish, crabs and spiny lobsters–a common nomenclature for homologous structures. Biol. Bull. 183, 304–326. doi: 10.2307/1542217
82. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682. doi: 10.1038/nmeth.2019
83. Schram, F. R. (1969). Polyphyly in the eumalacostraca? Crustaceana 16, 243–250. doi: 10.1163/156854069x00286
84. Seelig, J. D., and Jayaraman, V. (2013). Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262–266. doi: 10.1038/nature12601
85. Seelig, J. D., and Jayaraman, V. (2015). Neural dynamics for landmark orientation and angular path integration. Nature 521, 186–191. doi: 10.1038/nature 14446
86. Shaw, S. R., and Varney, L. P. (1999). Primitive, crustacean-like state of bloodbrain barrier in the eye of the apterygote insect Petrobius (Archaeognatha) determined from uptake of fluorescent tracers. J. Neurobiol. 41, 452–470. doi: 10.1002/(SICI)1097-4695(199912)41:4<452::AID-NEU2>3.3.CO;2-X
87. Stegner, M. E., and Richter, S. (2011). Morphology of the brain in Hutchinsoniella macracantha (Cephalocarida, Crustacea). Arthropod Struct. Dev. 40, 221–243. doi: 10.1016/j.asd.2011.04.001
88. Strausfeld, N. J. (1976). Atlas of An Insect Brain. Heidelberg, New York, NY: Springer-Verlag Berlin.
89. Strausfeld, N. J. (1998). Crustacean–Insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav. Evol. 52, 186–206. doi: 10.1159/000006563
90. Strausfeld, N. J. (1999). A brain region in insects that supervises walking. Prog. Brain Res. 123, 273–284. doi: 10.1016/s0079-6123(08)62863-0
91. Strausfeld, N. J. (2012). Arthropod Brains: Evolution, Functional Elegance and Historical Significance. Cambridge, MA: Belknap Press of Harvard University Press.
92. Strausfeld, N. J., and Hirth, F. (2013). Deep homology of arthropod central complex and vertebrate basal ganglia. Science 340, 157–161. doi: 10.1126/science.1231828
93. Strausfeld, N. J., Ma, X., and Edgecombe, G. D. (2016). Fossils and the evolution of the arthropod brain. Curr. Biol. 26, R989–R1000. doi: 10.1016/j.cub.2016. 09.012
94. Strauss, R., and Heisenberg, M. (1993). A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13, 1852–1861.
95. Sullivan, J. M., and Beltz, B. S. (2004). Evolutionary changes in the olfactory projection neuron pathways of eumalacostracan crustaceans. J. Comp. Neurol. 470, 25–38. doi: 10.1002/cne.11026
96. Tauber, E. S., and Atkin, A. (1967). Disconjugate eye movement patterns during optokinetic stimulation of the African chameleon, Chameleo melleri. Nature 214, 1008–1010. doi: 10.1038/2141008b0
97. Thoen, H. H., How, M. J., Chiou, T. H., and Marshall, J. (2014). A different form of color vision in mantis shrimp. Science 343, 411–413. doi: 10.1126/science. 1245824
98. Triphan, T., Poeck, B., Neuser, K., and Strauss, R. (2010). Visual targeting of motor actions in climbing Drosophila. Curr. Biol. 20, 663–668. doi: 10.1016/j.cub.2010. 02.055
99. Utting, M., Agricola, H. J., Sandeman, R., and Sandeman, D. (2000). Central complex in the brain of crayfish and its possible homology with that of insects. J. Comp. Neurol. 416, 245–261. doi: 10.1002/(SICI)1096-9861(20000110)416:2<245::AID-CNE9>3.3.CO;2-1
100. Webb, B., and Wystrach, A. (2016). Neural mechanisms of insect navigation. Curr. Opin. Insect Sci. 15, 27–39. doi: 10.1016/j.cois.2016.02.011
101. Williams, J. (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. 176, 67–86. doi: 10.1111/j. 1469-7998.1975.tb03188.x
102. Wolff, G., Harzsch, S., Hansson, B. S., Brown, S., and Strausfeld, N. (2012). Neuronal organization of the hemiellipsoid body of the land hermit crab, Coenobita clypeatus: correspondence with the mushroom body ground pattern. J. Comp. Neurol. 520, 2824–2846. doi: 10.1002/cne. 23059
103. Wolff, G. H., and Strausfeld, N. J. (2015). Genealogical correspondence of mushroom bodies across invertebrate phyla. Curr. Biol. 25, 38–44. doi: 10.1016/j.cub.2014.10.049
104. Wolff, G. H., and Strausfeld, N. (2016). ‘‘The insect brain: a commentated primer,’’ in Structure and Evolution of Invertebrate Nervous Systems, eds A. SchmidtRhaesa, S. Harzsch and G. Purschke (Oxford: Oxford University Press), 597–639.
105. Zaidi, Q., Marshall, J., Thoen, H., and Conway, B. R. (2014). Evolution of neural computations: mantis shrimp and human color decoding. Iperception 5, 492–496. doi: 10.1068/i0662sas