Skip to main content
SpringerLink
Log in

Insect Brains: Minute Structures Controlling Complex Behaviors

  • Chapter
  • First Online:
Brain Evolution by Design

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

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alerstam T, Gudmundsson GA, Green M, Hedenstrom A (2001) Migration along orthodromic sun compass routes by arctic birds. Science 291:300–303

    Article  CAS  PubMed  Google Scholar 

  • Arendt D, Nübler-Jung K (1996) Common ground plans in early brain development in mice and flies. Bioessays 18:255–259

    Article  CAS  PubMed  Google Scholar 

  • 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, e1002768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 513:532–541

    Article  PubMed  Google Scholar 

  • Barlow HB, Hill RM (1963) Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139:412–414

    Article  CAS  PubMed  Google Scholar 

  • Behnia R, Clark DA, Carter AG, Clandinin TR, Desplan C (2014) Processing properties of ON and OFF pathways for Drosophila motion detection. Nature 512:427–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 104:7471–7476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borst A, Euler T (2011) Seeing things in motion: models, circuits, and mechanisms. Neuron 71:974–994

    Article  CAS  PubMed  Google Scholar 

  • Borst A, Haag J (2002) Neural networks in the cockpit of the fly. J Comp Physiol A 188:419–437

    Article  CAS  Google Scholar 

  • Borst A, Helmstaedter M (2015) Common circuit design in fly and mammalian motion vision. Nature Neurosci 18:1067–1076

    Article  CAS  PubMed  Google Scholar 

  • Borst A, Haag J, Reiff DF (2010) Fly motion vision. Annu Rev Neurosci 33:49–70

    Article  CAS  PubMed  Google Scholar 

  • 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 492:1–19

    Article  PubMed  Google Scholar 

  • 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 492:433–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busch S, Selcho M, Ito K, Tanimoto H (2009) A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513:643–667

    Article  PubMed  Google Scholar 

  • Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GS (2010) Sexual dimorphism in the fly brain. Curr Biol 20:1589–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19:R995–R1008

    Article  CAS  PubMed  Google Scholar 

  • 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 34:1461–1470

    Article  CAS  PubMed  Google Scholar 

  • Dacke M, Nilsson DE, Scholtz CH, Byrne M, Warrant EJ (2003) Animal behaviour: insect orientation to polarized moonlight. Nature 424:33

    Article  CAS  PubMed  Google Scholar 

  • Dickson BJ (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322:904–909

    Article  CAS  PubMed  Google Scholar 

  • 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 4:3

    PubMed  PubMed Central  Google Scholar 

  • 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 6:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehmer B, Gronenberg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451:362–373

    Article  PubMed  Google Scholar 

  • el Jundi B, Homberg U (2010) Evidence for the possible existence of a second polarization-vision pathway in the locust brain. J Insect Physiol 56:971–979

    Article  PubMed  CAS  Google Scholar 

  • 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 3:21

    Article  PubMed  Google Scholar 

  • 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 517:210–225

    Article  PubMed  Google Scholar 

  • 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, e27855

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 200:575–589

    Google Scholar 

  • 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 112:11395–11400

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farris SM (2008) Tritocerebral tract input to the insect mushroom bodies. Arthropod Struct Dev 37:492–503

    Article  PubMed  Google Scholar 

  • Farris SM (2011) Are mushroom bodies cerebellum-like structures? Arthropod Struct Dev 40:368–379

    Article  PubMed  Google Scholar 

  • Farris SM (2013) Evolution of complex higher brain centers and behaviors: behavioral correlates of mushroom body elaboration in insects. Brain Behav Evol 82:9–18

    Article  PubMed  Google Scholar 

  • Farris SM (2015) Evolution of brain elaboration. Philos Trans R Soc Lond B Biol Sci 370:20150054

    Article  PubMed  PubMed Central  Google Scholar 

  • Farris SM, Roberts NS (2005) Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc Natl Acad Sci USA 102:17394–17399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischbach K-F, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475

    Article  Google Scholar 

  • Forger NG, de Vries GJ (2010) Cell death and sexual differentiation of behavior: worms, flies, and mammals. Curr Opin Neurobiol 20:776–783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukushima R, Kanzaki R (2009) Modular subdivision of mushroom bodies by Kenyon cells in the silkmoth. J Comp Neurol 513:315–330

    Article  PubMed  Google Scholar 

  • Galizia CG (2014) Olfactory coding in the insect brain: data and conjectures. Eur J Neurosci 39:1784–1795

    Article  PubMed  PubMed Central  Google Scholar 

  • Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735

    Article  CAS  PubMed  Google Scholar 

  • Glanzman DL (2010) Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Curr Biol 20:R31–R36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould JL (1998) Sensory bases of navigation. Curr Biol 8:R731–R738

    Article  CAS  PubMed  Google Scholar 

  • Gouranton J (1964) Contribution a l’étude de la structure des ganglions céréböides de Locusta migratoria migratorioides. Bull Soc Zool Fr 89:785–797

    Google Scholar 

  • Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232

    Article  CAS  PubMed  Google Scholar 

  • Gronenberg W (1999) Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54:85–95

    Article  CAS  PubMed  Google Scholar 

  • Guven-Ozkan T, Davis RL (2014) Functional neuroanatomy of Drosophila olfactory memory formation. Learn Mem 21:519–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    Article  CAS  PubMed  Google Scholar 

  • Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617–1630

    Google Scholar 

  • Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146–156

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 391–424

    Chapter  Google Scholar 

  • Heinze S, Homberg U (2007) Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995–997

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511:454–478

    Article  PubMed  Google Scholar 

  • Heinze S, Reppert SM (2011) Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69:345–358

    Article  CAS  PubMed  Google Scholar 

  • Heinze S, Reppert SM (2012) Anatomical basis of sun compass navigation. I: The general layout of the monarch butterfly brain. J Comp Neurol 520:1599–1628

    Article  PubMed  Google Scholar 

  • 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 521:267–298

    Article  Google Scholar 

  • 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 15:135–154

    Article  PubMed  Google Scholar 

  • Helfrich-Förster C (2004) The circadian clock in the brain: a structural and functional comparison between mammals and insects. J Comp Physiol A 190:601–613

    Article  Google Scholar 

  • Helfrich-Förster C (2014) From neurogenetic studies in the fly brain to a concept in circadian biology. J Neurogenet 28:329–347

    Article  PubMed  Google Scholar 

  • Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594

    Article  PubMed  Google Scholar 

  • Herculano-Houzel S, Mota B, Lent R (2006) Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103:12138–12143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hildebrandt JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631

    Article  Google Scholar 

  • Homberg U (2008) Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37:347–362

    Article  PubMed  Google Scholar 

  • Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255–281

    Article  CAS  PubMed  Google Scholar 

  • 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 462:415–430

    Article  PubMed  Google Scholar 

  • Homberg U, Reischig T, Stengl M (2003b) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591

    Article  CAS  PubMed  Google Scholar 

  • 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 366:680–687

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 93:9687–9692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:755–765

    Article  CAS  PubMed  Google Scholar 

  • Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A (2010) ON and OFF pathways in Drosophila motion vision. Nature 468:300–304

    Article  CAS  PubMed  Google Scholar 

  • Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038

    Article  CAS  PubMed  Google Scholar 

  • 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 336:119–136

    Article  PubMed  Google Scholar 

  • Keene AC, Waddell S (2007) Drosophila olfactory memory: signal genes to complex neural circuits. Nat Rev 8:341–354

    Article  CAS  Google Scholar 

  • Kimura K, Ote M, Tazawa T, Yamamoto D (2005) Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain. Nature 438:229–233

    Article  CAS  PubMed  Google Scholar 

  • 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 59:759–769

    Article  CAS  PubMed  Google Scholar 

  • 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 210:1350–1361

    Article  PubMed  Google Scholar 

  • 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 523:162–182

    Article  PubMed  Google Scholar 

  • Kirkhart C, Scott K (2015) Gustatory learning and processing in the Drosophila mushroom bodies. J Neurosci 35:5950–5958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 20:1–8

    Article  CAS  PubMed  Google Scholar 

  • Kohatsu S, Koganezawa M, Yamamoto D (2011) Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 69:498–508

    Article  CAS  PubMed  Google Scholar 

  • Kolmes SA (1983) Ecological and sensory aspects of prey capture by the whirligig beetle Dineutes discolor (Coleoptera: Gyrinidae). J New York Entomol Soc 91:405–412

    Google Scholar 

  • 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 139:416–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 333:125–145

    Article  PubMed  Google Scholar 

  • Leinwand SG, Chalasani SH (2011) Olfactory networks: from sensation to perception. Curr Opin Gen Dev 21:806–811

    Article  CAS  Google Scholar 

  • 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 823:11–23

    Article  CAS  PubMed  Google Scholar 

  • 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 25:2203–2214

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Liberless SD (2015) Aversion and attraction through olfaction. Curr Biol 25:R120–R129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity (Edinb) 94:465–477

    Article  CAS  Google Scholar 

  • 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 520:2562–2574

    Article  PubMed  Google Scholar 

  • 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 10:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin S, Owald D, Chandra V, Talbot C, Huetteroth W, Waddell S (2014) Neural correlates of water reward in thirsty Drosophila. Nat Neurosci 17:1536–1542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 488:512–516

    Article  CAS  PubMed  Google Scholar 

  • Lohmann KJ, Lohmann CM, Ehrhart LM, Bagley DA, Swing T (2004) Animal behaviour: geomagnetic map used in sea-turtle navigation. Nature 428:909–910

    Article  CAS  PubMed  Google Scholar 

  • 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 500:212–216

    Article  CAS  PubMed  Google Scholar 

  • Matsuo E, Kamikouchi A (2013) Neural encoding of sound, gravity, and wind in the fruit fly. J Comp Physiol A 199:253–262

    Article  Google Scholar 

  • Menzel R (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53–62

    Google Scholar 

  • Menzel R (2014) The insect mushroom body, an experience-dependent recoding device. J Physiol Paris 108:84–95

    Google Scholar 

  • Menzel R, Erber J (1978) Learning and memory in bees. Sci Am 239(1):80–87

    Article  Google Scholar 

  • Menzel R, Giurfa M (2001) Cognitive architecture of a mini-brain: the honeybee. Trends Cogn Sci 5:62–71

    Article  CAS  PubMed  Google Scholar 

  • 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 7:46

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mizunami M, Hamanaka Y, Nishino H (2015) Toward elucidating diversity of neural mechanisms underlying insect learning. Zool Lett 1:8

    Article  Google Scholar 

  • Mobbs PG (1985) Brain structure. In: Kerkut GA, Gilbert LI (eds) Comparative insect physiology, biochemistry and pharmacology, vol 5. Pergamon Press, New York, pp 299–370

    Google Scholar 

  • 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 41:3–16

    Article  PubMed  Google Scholar 

  • Okamura JY, Strausfeld NJ (2007) Visual system of calliphorid flies: motion- and orientation-sensitive visual interneurons supplying dorsal optic glomeruli. J Comp Neurol 500:189–208

    Article  PubMed  Google Scholar 

  • Otsuna H, Ito K (2006) Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J Comp Neurol 497:928–958

    Article  PubMed  Google Scholar 

  • Owald D, Waddell S (2015) Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila. Curr Opin Neurobiol 35:178–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panda S, Hogenesch JB, Kay SA (2002) Circadian rhythms from flies to human. Nature 417:329–335

    Article  CAS  PubMed  Google Scholar 

  • 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 28:6319–6332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–R763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 79:945–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer K, Homberg U (2007) Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17:960–965

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer K, Homberg U (2014) Organization and functional roles of the central complex in the insect brain. Annu Rev Entomol 59:165–184

    Article  CAS  PubMed  Google Scholar 

  • 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 520:212–229

    Article  PubMed  Google Scholar 

  • 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 94:3903–3915

    Article  PubMed  Google Scholar 

  • Reichardt W (1987) Evaluation of optical motion information by movement detectors. J Comp Physiol A 161:533–547

    Article  CAS  PubMed  Google Scholar 

  • 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 247:393–407

    Article  Google Scholar 

  • Rieger D, Shafer OT, Tomioka K, Helfrich-Förster C (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26:2531–2543

    Article  CAS  PubMed  Google Scholar 

  • Roberts AC, Glanzman DL (2003) Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci 26:662–670

    Article  CAS  PubMed  Google Scholar 

  • Rosenkranz JA, Grace AA (2002) Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning. Nature 417:282–287

    Article  CAS  PubMed  Google Scholar 

  • Rospars JP, Hildebrand JG (1992) Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270:205–227

    Article  CAS  PubMed  Google Scholar 

  • Rossel S, Wehner R (1984) Celestial orientation in bees: the use of spectral cues. J Comp Physiol A 155:605–613

    Article  Google Scholar 

  • Rossel S, Wehner R (1986) Polarization vision in bees. Nature 323:128–131

    Article  Google Scholar 

  • 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 468:686–690

    Article  CAS  PubMed  Google Scholar 

  • 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 87:1079–1089

    Article  CAS  PubMed  Google Scholar 

  • Sandrelli F, Costa R, Kyriacou CP, Rosato E (2008) Comparative analysis of circadian clock genes in insects. Insect Mol Biol 17:447–463

    Article  CAS  PubMed  Google Scholar 

  • Sane SP, Dieudonné A, Willis M, Daniel TL (2007) Antennal mechanosensors mediate flight control in moths. Science 315:863–866

    Article  CAS  PubMed  Google Scholar 

  • Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34:257–299

    Article  Google Scholar 

  • 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 201:427–440

    Article  Google Scholar 

  • Schröter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327:647–667

    Article  PubMed  Google Scholar 

  • Seelig JD, Jayaraman V (2013) Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–266

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seelig JD, Jayaraman V (2015) Neural dynamics for landmark orientation and angular path integration. Nature 521:186–191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 35:153–168

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan MV (2011) Honeybees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. Physiol Rev 91:413–460

    Article  CAS  PubMed  Google Scholar 

  • 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 208:2399–2408

    Article  PubMed  Google Scholar 

  • Staudacher E, Gebhardt MJ, Dürr V (2005) Antennal movements and mechanoreception: neurobiology of active tactile sensors. Adv Insect Physiol 32:49–205

    Google Scholar 

  • Stengl M, Arendt A (2016) Peptidergic circadian clock circuits in the Madeira cockroach. Curr Opin Neurobiol 41:44–52

    Google Scholar 

  • Stoleru D, Peng Y, Agosto J, Rosbash M (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431:862–868

    Article  CAS  PubMed  Google Scholar 

  • Stopfer M (2014) Central processing in the mushroom bodies. Curr Opin Insect Sci 6:99–103

    Article  PubMed  PubMed Central  Google Scholar 

  • Strausfeld NJ (1970) The optic lobes of Diptera. Philos Trans R Soc Lond B 258:135–223

    Article  CAS  Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin

    Book  Google Scholar 

  • 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 317–359

    Chapter  Google Scholar 

  • Strausfeld NJ (2012) Arthropod brains. Belknap Press/Harvard University Press, Cambridge

    Google Scholar 

  • Strausfeld NJ, Bassemir U, Singh RN, Bacon JP (1984) Organizational principles of outputs from dipteran brains. J Insect Physiol 30:73–93

    Article  Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 483:341–350

    Article  PubMed  Google Scholar 

  • 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 500:175–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711–755

    Article  PubMed  Google Scholar 

  • Tomioka K, Matsumoto A (2010) A comparative view of insect circadian clock systems. Cell Mol Life Sci 67:1397–1406

    Article  CAS  PubMed  Google Scholar 

  • Träger U, Homberg U (2011) Polarization-sensitive descending neurons in the locust: connecting the brain to thoracic ganglia. J Neurosci 31:2238–2247

    Article  PubMed  CAS  Google Scholar 

  • 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 506:288–300

    Google Scholar 

  • 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 22:1409–1416

    Article  PubMed  Google Scholar 

  • 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 2:500–506

    Article  CAS  PubMed  Google Scholar 

  • Vitzthum H, Müller M, Homberg U (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22:1114–1125

    CAS  PubMed  Google Scholar 

  • 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, e02395

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • von Frisch K (1950) Bees: their vision, chemical senses and language. Cornell University Press, Ithaca/London

    Google Scholar 

  • von Frisch K (1974) Decoding the language of the bee. Science 185:663–668

    Article  Google Scholar 

  • Waddell S (2013) Reinforcement signalling in Drosophila: dopamine does it all after all. Curr Opin Neurobiol 23:324–329

    Article  CAS  PubMed  Google Scholar 

  • 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 518:3907–3930

    Article  PubMed  Google Scholar 

  • Watanabe H, Matsumoto CS, Nishino H, Mizunami M (2011) Critical roles of mecamylamine-sensitive mushroom body neurons in insect olfactory learning. Neurobiol Learn Mem 95:1–13

    Article  CAS  PubMed  Google Scholar 

  • Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588

    Article  CAS  Google Scholar 

  • 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 103:12575–12579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 523:997–1037

    Article  PubMed  Google Scholar 

  • 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 112:578–583

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto D, Koganezawa M (2013) Genes and circuits of courtship behaviour in Drosophila males. Nat Rev Neurosci 14:681–692

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto D, Jallon JM, Komatsu A (1997) Genetic dissection of sexual behavior in Drosophila melanogaster. Annu Rev Entomol 42:551–585

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y, Shibata H, Ueda H (2013) Olfactory homing of chum salmon to stable compositions of amino acids in natal stream water. Zool Sci 30:607–612

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto D, Sato K, Koganezawa M (2014) Neuroethology of male courtship in Drosophila: from the gene to behavior. J Comp Physiol A 200:251–264

    Article  Google Scholar 

  • Yang EC, Lin HC, Hung YS (2004) Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. J Insect Physiol 50:913–925

    Article  CAS  PubMed  Google Scholar 

  • Yu JY, Kanai MI, Demir E, Jefferis GS, Dickson BJ (2010) Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20:1602–1614

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Neuroethology, SOKENDAI, The Graduate University for Advanced Studies, Shonan Village, Hayama, 240-0193, Japan

    Michiyo Kinoshita

  2. Department of Biology, Animal Physiology, University of Marburg, D-35032, Marburg, Germany

    Uwe Homberg

Authors
  1. Michiyo Kinoshita
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Uwe Homberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michiyo Kinoshita .

Editor information

Editors and Affiliations

  1. Stazione Zoologica Anton Dohrn, Naples, Italy

    Shuichi Shigeno

  2. Ehime University, Matsuyama, Japan

    Yasunori Murakami

  3. Kyoto Prefectural University of Medicine, Kyoto, Japan

    Tadashi Nomura

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Japan KK

About this chapter

Cite this chapter

Kinoshita, M., Homberg, U. (2017). Insect Brains: Minute Structures Controlling Complex Behaviors. In: Shigeno, S., Murakami, Y., Nomura, T. (eds) Brain Evolution by Design. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56469-0_6

Download citation

Publish with us

Policies and ethics

Search

Navigation