Insect Brains: Minute Structures Controlling Complex Behaviors

Part of the Diversity and Commonality in Animals book series (DCA)


Insects are the largest taxon of arthropods, characterized by a segmented body plan. They comprise the most abundant and diverse group of animals. Many insects show highly complex adaptive behaviors, including learning abilities, social interactions, and spatial orientation skills that, in simplified version, are reminiscent of the abilities of vertebrates and even humans. In contrast to their sophisticated behavior, their brain, however, is minute and simple compared to that of humans. Because of these features, many insects have become models for studies of the neuronal basis underlying specific behaviors.

The insect body is divided into three parts: the head, the thorax with wings and legs, and the abdomen. In most species, each part contains relatively autonomously operating neural circuits, which have functions in local sensing and motor control. The head contains the antennae, the compound eyes, the ocelli, various sense organs on the mouth parts, and, as part of the nervous system, the brain. The brain processes this multitude of sensory input and provides multisensory integration. In addition, it controls movements of the antennae and mouth parts and induces suitable behaviors by modifying the activity of the thoracic and abdominal nervous systems, which, likewise, provide sensory input and feedback to the brain. This chapter introduces the organization of the insect brain and then focuses on neural circuits underlying five aspects of insect behavior that are relatively well understood.


Sensory systems Insect brain Motion vision Circadian clock Learning and memory Orientation Courtship 


  1. Alerstam T, Gudmundsson GA, Green M, Hedenstrom A (2001) Migration along orthodromic sun compass routes by arctic birds. Science 291:300–303PubMedCrossRefGoogle Scholar
  2. Arendt D, Nübler-Jung K (1996) Common ground plans in early brain development in mice and flies. Bioessays 18:255–259PubMedCrossRefGoogle Scholar
  3. Aso Y, Herb A, Ogueta M, Siwanowicz I, Templier T, Friedrich AB, Ito K, Scholz H, Tanimoto H (2012) Three dopamine pathways induce aversive odor memories with different stability. PLoS Genet 8, e1002768PubMedPubMedCentralCrossRefGoogle Scholar
  4. Azevedo FA, Carvalho LR, Grinberg LT, Farfel JM, Ferretti RE, Leite RE, Jacob Filho W, Lent R, Herculano-Houzel S (2009) Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol 513:532–541PubMedCrossRefGoogle Scholar
  5. Barlow HB, Hill RM (1963) Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139:412–414PubMedCrossRefGoogle Scholar
  6. Behnia R, Clark DA, Carter AG, Clandinin TR, Desplan C (2014) Processing properties of ON and OFF pathways for Drosophila motion detection. Nature 512:427–430PubMedPubMedCentralCrossRefGoogle Scholar
  7. Biro D, Freeman R, Meade J, Roberts S, Guilford T (2007) Pigeons combine compass and landmark guidance in familiar route navigation. Proc Natl Acad Sci USA 104:7471–7476PubMedPubMedCentralCrossRefGoogle Scholar
  8. Borst A, Euler T (2011) Seeing things in motion: models, circuits, and mechanisms. Neuron 71:974–994PubMedCrossRefGoogle Scholar
  9. Borst A, Haag J (2002) Neural networks in the cockpit of the fly. J Comp Physiol A 188:419–437CrossRefGoogle Scholar
  10. Borst A, Helmstaedter M (2015) Common circuit design in fly and mammalian motion vision. Nature Neurosci 18:1067–1076PubMedCrossRefGoogle Scholar
  11. Borst A, Haag J, Reiff DF (2010) Fly motion vision. Annu Rev Neurosci 33:49–70PubMedCrossRefGoogle Scholar
  12. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege HC, Menzel R (2005) Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492:1–19PubMedCrossRefGoogle Scholar
  13. Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ, Das G, Gohl D, Silies M, Certel S, Waddell S (2012) Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492:433–437PubMedPubMedCentralCrossRefGoogle Scholar
  14. Busch S, Selcho M, Ito K, Tanimoto H (2009) A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513:643–667PubMedCrossRefGoogle Scholar
  15. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS (2010) Sexual dimorphism in the fly brain. Curr Biol 20:1589–1601PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19:R995–R1008PubMedCrossRefGoogle Scholar
  17. Coemans MA, Vos Hzn JJ, Nuboer JF (1994) The relation between celestial colour gradients and the position of the sun, with regard to the sun compass. Vision Res 34:1461–1470PubMedCrossRefGoogle Scholar
  18. Dacke M, Nilsson DE, Scholtz CH, Byrne M, Warrant EJ (2003) Animal behaviour: insect orientation to polarized moonlight. Nature 424:33PubMedCrossRefGoogle Scholar
  19. Dickson BJ (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322:904–909PubMedCrossRefGoogle Scholar
  20. Dreyer D, Vitt H, Dippel S, Goetz B, el Jundi B, Kollmann M, Huetteroth W, Schachtner J (2010) 3D standard brain of the red flour beetle Tribolium castaneum: a tool to study metamorphic development and adult plasticity. Front Syst Neurosci 4:3PubMedPubMedCentralGoogle Scholar
  21. Dunbier JR, Wiederman SD, Shoemaker PA, O’Carroll DC (2012) Facilitation of dragonfly target-detecting neurons by slow moving features on continuous paths. Front Neural Circuits 6:79PubMedPubMedCentralCrossRefGoogle Scholar
  22. Ehmer B, Gronenberg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451:362–373PubMedCrossRefGoogle Scholar
  23. el Jundi B, Homberg U (2010) Evidence for the possible existence of a second polarization-vision pathway in the locust brain. J Insect Physiol 56:971–979PubMedCrossRefGoogle Scholar
  24. el Jundi B, Heinze S, Lenschow C, Kurylas A, Rohlfing T, Homberg U (2009a) The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3:21PubMedCrossRefGoogle Scholar
  25. el Jundi B, Huetteroth W, Kurylas AE, Schachtner J (2009b) Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 517:210–225PubMedCrossRefGoogle Scholar
  26. el Jundi B, Pfeiffer K, Homberg U (2011) A distinct layer of the medulla integrates sky compass signals in the brain of an insect. PLoS One 6, e27855PubMedPubMedCentralCrossRefGoogle Scholar
  27. el Jundi B, Pfeiffer K, Heinze S, Homberg U (2014) Integration of polarization and chromatic cues in the insect sky compass. J Comp Physiol A 200:575–589Google Scholar
  28. el Jundi B, Warrant EJ, Byrne MJ, Khaldy L, Baird E, Smolka J, Dacke M (2015) Neural coding underlying the cue preference for celestial orientation. Proc Natl Acad Sci USA 112:11395–11400PubMedPubMedCentralCrossRefGoogle Scholar
  29. Farris SM (2008) Tritocerebral tract input to the insect mushroom bodies. Arthropod Struct Dev 37:492–503PubMedCrossRefGoogle Scholar
  30. Farris SM (2011) Are mushroom bodies cerebellum-like structures? Arthropod Struct Dev 40:368–379PubMedCrossRefGoogle Scholar
  31. Farris SM (2013) Evolution of complex higher brain centers and behaviors: behavioral correlates of mushroom body elaboration in insects. Brain Behav Evol 82:9–18PubMedCrossRefGoogle Scholar
  32. Farris SM (2015) Evolution of brain elaboration. Philos Trans R Soc Lond B Biol Sci 370:20150054PubMedPubMedCentralCrossRefGoogle Scholar
  33. Farris SM, Roberts NS (2005) Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc Natl Acad Sci USA 102:17394–17399PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fischbach K-F, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475CrossRefGoogle Scholar
  35. Forger NG, de Vries GJ (2010) Cell death and sexual differentiation of behavior: worms, flies, and mammals. Curr Opin Neurobiol 20:776–783PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fukushima R, Kanzaki R (2009) Modular subdivision of mushroom bodies by Kenyon cells in the silkmoth. J Comp Neurol 513:315–330PubMedCrossRefGoogle Scholar
  37. Galizia CG (2014) Olfactory coding in the insect brain: data and conjectures. Eur J Neurosci 39:1784–1795PubMedPubMedCentralCrossRefGoogle Scholar
  38. Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420PubMedCrossRefGoogle Scholar
  39. Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735PubMedCrossRefGoogle Scholar
  40. Glanzman DL (2010) Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Curr Biol 20:R31–R36PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gould JL (1998) Sensory bases of navigation. Curr Biol 8:R731–R738PubMedCrossRefGoogle Scholar
  42. Gouranton J (1964) Contribution a l’étude de la structure des ganglions céréböides de Locusta migratoria migratorioides. Bull Soc Zool Fr 89:785–797Google Scholar
  43. Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232PubMedCrossRefGoogle Scholar
  44. Gronenberg W (1999) Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54:85–95PubMedCrossRefGoogle Scholar
  45. Guven-Ozkan T, Davis RL (2014) Functional neuroanatomy of Drosophila olfactory memory formation. Learn Mem 21:519–526PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63PubMedCrossRefGoogle Scholar
  47. Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617–1630Google Scholar
  48. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146–156PubMedPubMedCentralGoogle Scholar
  49. Hausen K, Egelhaaf M (1989) Neural mechanisms of visual course control in insects. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin/Heidelberg, pp 391–424CrossRefGoogle Scholar
  50. Heinze S, Homberg U (2007) Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995–997PubMedCrossRefGoogle Scholar
  51. Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511:454–478PubMedCrossRefGoogle Scholar
  52. Heinze S, Reppert SM (2011) Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69:345–358PubMedCrossRefGoogle Scholar
  53. Heinze S, Reppert SM (2012) Anatomical basis of sun compass navigation. I: The general layout of the monarch butterfly brain. J Comp Neurol 520:1599–1628PubMedCrossRefGoogle Scholar
  54. Heinze S, Florman J, Asokaraj S, el Jundi B, Reppert SM (2012) Anatomical basis of sun compass navigation. II: The neuronal composition of the central complex of the monarch butterfly. J Comp Neurol 521:267–298CrossRefGoogle Scholar
  55. Helfrich-Förster C (2000) Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster: sex-specific differences suggest a different quality of activity. J Biol Rhythms 15:135–154PubMedCrossRefGoogle Scholar
  56. Helfrich-Förster C (2004) The circadian clock in the brain: a structural and functional comparison between mammals and insects. J Comp Physiol A 190:601–613CrossRefGoogle Scholar
  57. Helfrich-Förster C (2014) From neurogenetic studies in the fly brain to a concept in circadian biology. J Neurogenet 28:329–347PubMedCrossRefGoogle Scholar
  58. Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594PubMedCrossRefGoogle Scholar
  59. Herculano-Houzel S, Mota B, Lent R (2006) Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103:12138–12143PubMedPubMedCentralCrossRefGoogle Scholar
  60. Hildebrandt JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631CrossRefGoogle Scholar
  61. Homberg U (2008) Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37:347–362PubMedCrossRefGoogle Scholar
  62. Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255–281PubMedCrossRefGoogle Scholar
  63. Homberg U, Hofer S, Pfeiffer K, Gebhardt S (2003a) Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462:415–430PubMedCrossRefGoogle Scholar
  64. Homberg U, Reischig T, Stengl M (2003b) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591PubMedCrossRefGoogle Scholar
  65. Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B (2011) Central neural coding of sky polarization in insects. Philos Trans R Soc Lond B Biol Sci 366:680–687PubMedPubMedCentralCrossRefGoogle Scholar
  66. Ito H, Fujitani K, Usui K, Shimizu-Nishikawa K, Tanaka S, Yamamoto D (1996) Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci USA 93:9687–9692PubMedPubMedCentralCrossRefGoogle Scholar
  67. Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, Harzsch S, Heisenberg M, Homberg U, Jenett A, Keshishian H, Restifo LL, Rössler W, Simpson JH, Strausfeld NJ, Strauss R, Vosshall LB (2014) A systematic nomenclature for the insect brain. Neuron 81:755–765PubMedCrossRefGoogle Scholar
  68. Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A (2010) ON and OFF pathways in Drosophila motion vision. Nature 468:300–304PubMedCrossRefGoogle Scholar
  69. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038PubMedCrossRefGoogle Scholar
  70. Kazawa T, Namiki S, Fukushima R, Terada M, Soo K, Kanzaki R (2009) Constancy and variability of glomerular organization in the antennal lobe of the silkmoth. Cell Tissue Res 336:119–136PubMedCrossRefGoogle Scholar
  71. Keene AC, Waddell S (2007) Drosophila olfactory memory: signal genes to complex neural circuits. Nat Rev 8:341–354CrossRefGoogle Scholar
  72. Kimura K, Ote M, Tazawa T, Yamamoto D (2005) Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438:229–233PubMedCrossRefGoogle Scholar
  73. Kimura K, Hachiya T, Koganezawa M, Tazawa T, Yamamoto D (2008) Fruitless and doublesex coordinate to generate male-specific neurons that can initiate courtship. Neuron 59:759–769PubMedCrossRefGoogle Scholar
  74. Kinoshita M, Pfeiffer K, Homberg U (2007) Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 210:1350–1361PubMedCrossRefGoogle Scholar
  75. Kinoshita M, Shimohigasshi M, Tominaga Y, Arikawa K, Homberg U (2015) Topographically distinct visual and olfactory inputs to the mushroom body in the swallowtail butterfly, Papilio xuthus. J Comp Neurol 523:162–182PubMedCrossRefGoogle Scholar
  76. Kirkhart C, Scott K (2015) Gustatory learning and processing in the Drosophila mushroom bodies. J Neurosci 35:5950–5958PubMedPubMedCentralCrossRefGoogle Scholar
  77. Koganezawa M, Haba D, Matsuo T, Yamamoto D (2010) The shaping of male courtship posture by lateralized gustatory inputs to male-specific interneurons. Curr Biol 20:1–8PubMedCrossRefGoogle Scholar
  78. Kohatsu S, Koganezawa M, Yamamoto D (2011) Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69:498–508PubMedCrossRefGoogle Scholar
  79. Kolmes SA (1983) Ecological and sensory aspects of prey capture by the whirligig beetle Dineutes discolor (Coleoptera: Gyrinidae). J New York Entomol Soc 91:405–412Google Scholar
  80. Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416–427PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kurylas AE, Rohlfing T, Krofczik S, Jenett A, Homberg U (2008) Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res 333:125–145PubMedCrossRefGoogle Scholar
  82. Leinwand SG, Chalasani SH (2011) Olfactory networks: from sensation to perception. Curr Opin Gen Dev 21:806–811CrossRefGoogle Scholar
  83. Leitinger G, Pabst MA, Kral K (1999) Serotonin-immunoreactive neurones in the visual system of the praying mantis: an immunohistochemical, confocal laser scanning and electron microscopic study. Brain Res 823:11–23PubMedCrossRefGoogle Scholar
  84. Lewis LP, Siju KP, Aso Y, Friedrich AB, Bulteel AJ, Rubin GM, Grunwald Kadow IC (2015) A higher brain circuit for immediate integration of conflicting sensory information in Drosophila. Curr Biol 25:2203–2214PubMedCrossRefGoogle Scholar
  85. Li Q, Liberless SD (2015) Aversion and attraction through olfaction. Curr Biol 25:R120–R129PubMedPubMedCentralCrossRefGoogle Scholar
  86. Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity (Edinb) 94:465–477CrossRefGoogle Scholar
  87. Lin C, Strausfeld NJ (2012) Visual inputs to the mushroom body calyces of the whirligig beetle Dineutus sublineatus: modality switching in an insect. J Comp Neurol 520:2562–2574PubMedCrossRefGoogle Scholar
  88. Lin C, Strausfeld NJ (2013) A precocious adult visual center in the larva defines the unique optic lobe of the split-eyed whirligig beetle Dineutus sublineatus. Front Zool 10:7PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lin S, Owald D, Chandra V, Talbot C, Huetteroth W, Waddell S (2014) Neural correlates of water reward in thirsty Drosophila. Nat Neurosci 17:1536–1542PubMedPubMedCentralCrossRefGoogle Scholar
  90. Liu C, Placais PY, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, Siwanowicz I, Rubin GM, Preat T, Tanimoto H (2012) A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488:512–516PubMedCrossRefGoogle Scholar
  91. Lohmann KJ, Lohmann CM, Ehrhart LM, Bagley DA, Swing T (2004) Animal behaviour: geomagnetic map used in sea-turtle navigation. Nature 428:909–910PubMedCrossRefGoogle Scholar
  92. Maisak MS, Haag J, Ammer G, Serbe E, Meier M, Leonhardt A, Schilling T, Bahl A, Rubin GM, Nern A, Dickson BJ, Reiff DR, Hopp E, Borst A (2013) A directional tuning map of Drosophila elementary motion detectors. Nature 500:212–216PubMedCrossRefGoogle Scholar
  93. Matsuo E, Kamikouchi A (2013) Neural encoding of sound, gravity, and wind in the fruit fly. J Comp Physiol A 199:253–262CrossRefGoogle Scholar
  94. Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62Google Scholar
  95. Menzel R (2014) The insect mushroom body, an experience-dependent recoding device. J Physiol Paris 108:84–95Google Scholar
  96. Menzel R, Erber J (1978) Learning and memory in bees. Sci Am 239(1):80–87CrossRefGoogle Scholar
  97. Menzel R, Giurfa M (2001) Cognitive architecture of a mini-brain: the honeybee. Trends Cogn Sci 5:62–71PubMedCrossRefGoogle Scholar
  98. Mizunami M, Unoki S, Mori Y, Hirashima D, Hatano A, Matsumoto Y (2009) Roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in an insect. BMC Biol 7:46PubMedPubMedCentralCrossRefGoogle Scholar
  99. Mizunami M, Hamanaka Y, Nishino H (2015) Toward elucidating diversity of neural mechanisms underlying insect learning. Zool Lett 1:8CrossRefGoogle Scholar
  100. Mobbs PG (1985) Brain structure. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology, vol 5. Pergamon Press, New York, pp 299–370Google Scholar
  101. Nishino H, Iwasaki M, Yasuyama K, Hongo H, Watanabe H, Mizunami M (2012) Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach. Arthropod Struct Dev 41:3–16PubMedCrossRefGoogle Scholar
  102. Okamura JY, Strausfeld NJ (2007) Visual system of calliphorid flies: motion- and orientation-sensitive visual interneurons supplying dorsal optic glomeruli. J Comp Neurol 500:189–208PubMedCrossRefGoogle Scholar
  103. Otsuna H, Ito K (2006) Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J Comp Neurol 497:928–958PubMedCrossRefGoogle Scholar
  104. Owald D, Waddell S (2015) Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila. Curr Opin Neurobiol 35:178–184PubMedPubMedCentralCrossRefGoogle Scholar
  105. Panda S, Hogenesch JB, Kay SA (2002) Circadian rhythms from flies to human. Nature 417:329–335PubMedCrossRefGoogle Scholar
  106. Paulk AC, Phillips-Portillo J, Dacks AM, Fellous JM, Gronenberg W (2008) The processing of color, motion, and stimulus timing are anatomically segregated in the bumblebee brain. J Neurosci 28:6319–6332PubMedPubMedCentralCrossRefGoogle Scholar
  107. Perisse E, Burke C, Huetteroth W, Waddell S (2013a) Shocking revelations and saccharin sweetness in the study of Drosophila olfactory memory. Curr Biol 23:R752–R763PubMedPubMedCentralCrossRefGoogle Scholar
  108. Perisse E, Yin Y, Lin AC, Lin S, Huetteroth W, Waddell S (2013b) Different Kenyon cell populations drive learned approach and avoidance in Drosophila. Neuron 79:945–956PubMedPubMedCentralCrossRefGoogle Scholar
  109. Pfeiffer K, Homberg U (2007) Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17:960–965PubMedCrossRefGoogle Scholar
  110. Pfeiffer K, Homberg U (2014) Organization and functional roles of the central complex in the insect brain. Annu Rev Entomol 59:165–184PubMedCrossRefGoogle Scholar
  111. Pfeiffer K, Kinoshita M (2012) Segregation of visual inputs from different regions of the compound eye in two parallel pathways through the anterior optic tubercle of the bumblebee (Bombus ignitus). J Comp Neurol 520:212–229PubMedCrossRefGoogle Scholar
  112. Pfeiffer K, Kinoshita M, Homberg U (2005) Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 94:3903–3915PubMedCrossRefGoogle Scholar
  113. Reichardt W (1987) Evaluation of optical motion information by movement detectors. J Comp Physiol A 161:533–547PubMedCrossRefGoogle Scholar
  114. Ribi W (1987) Anatomical identification of spectral receptor types in the retina and lamina of the Australian orchard butterfly, Papilio aegeus aegeus D. Cell Tissue Res 247:393–407CrossRefGoogle Scholar
  115. Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26:2531–2543PubMedCrossRefGoogle Scholar
  116. Roberts AC, Glanzman DL (2003) Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci 26:662–670PubMedCrossRefGoogle Scholar
  117. Rosenkranz JA, Grace AA (2002) Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning. Nature 417:282–287PubMedCrossRefGoogle Scholar
  118. Rospars JP, Hildebrand JG (1992) Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270:205–227PubMedCrossRefGoogle Scholar
  119. Rossel S, Wehner R (1984) Celestial orientation in bees: the use of spectral cues. J Comp Physiol A 155:605–613CrossRefGoogle Scholar
  120. Rossel S, Wehner R (1986) Polarization vision in bees. Nature 323:128–131CrossRefGoogle Scholar
  121. Ruta V, Datta SR, Vasconcelos ML, Freeland J, Looger LL, Axel R (2010) A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468:686–690PubMedCrossRefGoogle Scholar
  122. Ryner LC, Goodwin SF, Castrillon DH, Anand A, Villella A, Baker BS, Hall JC, Taylor BJ, Wasserman SA (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87:1079–1089PubMedCrossRefGoogle Scholar
  123. Sandrelli F, Costa R, Kyriacou CP, Rosato E (2008) Comparative analysis of circadian clock genes in insects. Insect Mol Biol 17:447–463PubMedCrossRefGoogle Scholar
  124. Sane SP, Dieudonné A, Willis M, Daniel TL (2007) Antennal mechanosensors mediate flight control in moths. Science 315:863–866PubMedCrossRefGoogle Scholar
  125. Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34:257–299CrossRefGoogle Scholar
  126. Schmeling F, Tegtmeier J, Kinoshita M, Homberg U (2015) Photoreceptor projections and receptive fields in the dorsal rim area and main retina of the locust eye. J Comp Physiol A 201:427–440CrossRefGoogle Scholar
  127. Schröter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327:647–667PubMedCrossRefGoogle Scholar
  128. Seelig JD, Jayaraman V (2013) Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–266PubMedPubMedCentralGoogle Scholar
  129. Seelig JD, Jayaraman V (2015) Neural dynamics for landmark orientation and angular path integration. Nature 521:186–191PubMedPubMedCentralCrossRefGoogle Scholar
  130. Sjöholm M, Sinakevitch I, Strausfeld NJ, Ignell R, Hansson BS (2006) Functional division of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis revealed by antibodies against aspartate, taurine, FMRF-amide, Mas-allatotropin and DC0. Arthropod Struct Dev 35:153–168PubMedCrossRefGoogle Scholar
  131. Srinivasan MV (2011) Honeybees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. Physiol Rev 91:413–460PubMedCrossRefGoogle Scholar
  132. Stalleicken J, Mukhida M, Labhart T, Wehner R, Frost B, Mouritsen H (2005) Do monarch butterflies use polarized skylight for migratory orientation? J Exp Biol 208:2399–2408PubMedCrossRefGoogle Scholar
  133. Staudacher E, Gebhardt MJ, Dürr V (2005) Antennal movements and mechanoreception: neurobiology of active tactile sensors. Adv Insect Physiol 32:49–205Google Scholar
  134. Stengl M, Arendt A (2016) Peptidergic circadian clock circuits in the Madeira cockroach. Curr Opin Neurobiol 41:44–52Google Scholar
  135. Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862–868PubMedCrossRefGoogle Scholar
  136. Stopfer M (2014) Central processing in the mushroom bodies. Curr Opin Insect Sci 6:99–103PubMedPubMedCentralCrossRefGoogle Scholar
  137. Strausfeld NJ (1970) The optic lobes of Diptera. Philos Trans R Soc Lond B 258:135–223CrossRefGoogle Scholar
  138. Strausfeld NJ (1976) Atlas of an insect brain. Springer, BerlinCrossRefGoogle Scholar
  139. Strausfeld NJ (1989) Beneath the compound eye: neuroanatomical analysis and physiological correlates in the study of insect vision. In: Stavenga DG, Hadie RC (eds) Facets of vision. Springer, Heidelberg/Berlin, pp 317–359CrossRefGoogle Scholar
  140. Strausfeld NJ (2012) Arthropod brains. Belknap Press/Harvard University Press, CambridgeGoogle Scholar
  141. Strausfeld NJ, Bassemir U, Singh RN, Bacon JP (1984) Organizational principles of outputs from dipteran brains. J Insect Physiol 30:73–93CrossRefGoogle Scholar
  142. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37PubMedPubMedCentralGoogle Scholar
  143. Takemura SY, Kinoshita M, Arikawa K (2005) Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus. J Comp Neurol 483:341–350PubMedCrossRefGoogle Scholar
  144. Takemura SY, Bharioke A, Lu Z, Nern A, Vitaladevuni S, Rivlin PK, Katz WT, Olbris DJ, Plaza SM, Winston P, Zhao T, Horne JA, Fetter RD, Takemura S, Blazek K, Chang LA, Ogundeyi O, Saunders MA, Shapiro V, Sigmund C, Rubin GM, Scheffer LK, Meinertzhagen IA, Chklovskii DB (2013) A visual motion detection circuit suggested by Drosophila connectomics. Nature 500:175–181PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711–755PubMedCrossRefGoogle Scholar
  146. Tomioka K, Matsumoto A (2010) A comparative view of insect circadian clock systems. Cell Mol Life Sci 67:1397–1406PubMedCrossRefGoogle Scholar
  147. Träger U, Homberg U (2011) Polarization-sensitive descending neurons in the locust: connecting the brain to thoracic ganglia. J Neurosci 31:2238–2247PubMedCrossRefGoogle Scholar
  148. Träger U, Wagner R, Bausenwein B, Homberg U (2008) A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 506:288–300Google Scholar
  149. Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22:1409–1416PubMedCrossRefGoogle Scholar
  150. Usui-Aoki K, Ito H, Ui-Tei K, Takahashi K, Lukacsovich T, Awano W, Nakata H, Piao ZF, Nilsson EE, Tomida J, Yamamoto D (2000) Formation of the male-specific muscle in female Drosophila by ectopic fruitless expression. Nat Cell Biol 2:500–506PubMedCrossRefGoogle Scholar
  151. Vitzthum H, Müller M, Homberg U (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22:1114–1125PubMedGoogle Scholar
  152. Vogt K, Schnaitmann C, Dylla KV, Knapek S, Aso Y, Rubin GM, Tanimoto H (2014) Shared mushroom body circuits underlie visual and olfactory memories in Drosophila. Elife 3, e02395PubMedPubMedCentralCrossRefGoogle Scholar
  153. von Frisch K (1950) Bees: their vision, chemical senses and language. Cornell University Press, Ithaca/LondonGoogle Scholar
  154. von Frisch K (1974) Decoding the language of the bee. Science 185:663–668CrossRefGoogle Scholar
  155. Waddell S (2013) Reinforcement signalling in Drosophila: dopamine does it all after all. Curr Opin Neurobiol 23:324–329PubMedCrossRefGoogle Scholar
  156. Watanabe H, Nishino H, Nishikawa M, Mizunami M, Yokohari F (2010) Complete mapping of glomeruli based on sensory nerve branching pattern in the primary olfactory center of the cockroach Periplaneta americana. J Comp Neurol 518:3907–3930PubMedCrossRefGoogle Scholar
  157. Watanabe H, Matsumoto CS, Nishino H, Mizunami M (2011) Critical roles of mecamylamine-sensitive mushroom body neurons in insect olfactory learning. Neurobiol Learn Mem 95:1–13PubMedCrossRefGoogle Scholar
  158. Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588CrossRefGoogle Scholar
  159. Wehner R, Müller M (2006) The significance of direct sunlight and polarized skylight in the ant’s celestial system of navigation. Proc Natl Acad Sci USA 103:12575–12579PubMedPubMedCentralCrossRefGoogle Scholar
  160. Wolff T, Iyer NA, Rubin GM (2015) Neuroarchitecture and neuroanatomy of the Drosophila central complex: A GAL4-based dissection of protocerebral bridge neurons and circuits. J Comp Neurol 523:997–1037PubMedCrossRefGoogle Scholar
  161. Yamagata N, Ichinose T, Aso Y, Placais PY, Friedrich AB, Sima RJ, Preat T, Rubin GM, Tanimoto H (2015) Distinct dopamine neurons mediate reward signals for short- and long-term memories. Proc Natl Acad Sci USA 112:578–583PubMedCrossRefGoogle Scholar
  162. Yamamoto D, Koganezawa M (2013) Genes and circuits of courtship behaviour in Drosophila males. Nat Rev Neurosci 14:681–692PubMedCrossRefGoogle Scholar
  163. Yamamoto D, Jallon JM, Komatsu A (1997) Genetic dissection of sexual behavior in Drosophila melanogaster. Annu Rev Entomol 42:551–585PubMedCrossRefGoogle Scholar
  164. Yamamoto Y, Shibata H, Ueda H (2013) Olfactory homing of chum salmon to stable compositions of amino acids in natal stream water. Zool Sci 30:607–612PubMedCrossRefGoogle Scholar
  165. Yamamoto D, Sato K, Koganezawa M (2014) Neuroethology of male courtship in Drosophila: from the gene to behavior. J Comp Physiol A 200:251–264CrossRefGoogle Scholar
  166. Yang EC, Lin HC, Hung YS (2004) Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. J Insect Physiol 50:913–925PubMedCrossRefGoogle Scholar
  167. Yu JY, Kanai MI, Demir E, Jefferis GS, Dickson BJ (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20:1602–1614PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan KK 2017

Authors and Affiliations

  1. 1.Laboratory of NeuroethologySOKENDAI, The Graduate University for Advanced StudiesHayamaJapan
  2. 2.Department of Biology, Animal PhysiologyUniversity of MarburgMarburgGermany

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