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On structural-functional organization of dragonfly mushroom bodies and some general considerations about purpose of these formations

  • V. L. Svidersky
  • S. I. Plotnikova
Article

Abstract

Anatomy as well as (for the first time) the fine structure have been studied of the mushroom bodies located in protocerebrum of the supraesophageal ganglion of dragonflies—the most ancient flying insects on Earth. Used in the work are larvae of the last age (prior to winging), in which the mushroom body structure has already been completely formed and corresponds to that in imago. The total organization of the dragonfly mushroom bodies has been established to be more primitive than that of other insects studied so far. This involves both the number of interneurons (Kenyon cells) present in the mushroom bodies and the character of anaptic connections formed by these cells. There is confirmed the absence in dragonflies of the mushroom body calyces that in opinion of some authors are obligatory “input gates” into these structures. Peculiarities of the neuropil structure in the area of the absent calyces are studied in detail. For the first time in insects there are revealed the direct (without additional synaptic switching) pathways forming the “afferent input” from optic lobes into the mushroom body calyx area. Also detected are the direct pathways going from the mushroom bodies to the abdominal chain (“efferent output”). A possible functional significance of these findings as well as the general role of mushroom bodied in control of some forms of insect behavior are discussed.

Keywords

Fine Structure Functional Significance General Consideration Body Structure General Role 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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REFERENCES

  1. 1.
    Dujardin, F., Mèmoire sur le Systéme Nerveux des Insectes, Ann. Sci. Nat. Zool., 1850, vol. 14, pp. 195–206.Google Scholar
  2. 2.
    Dujardin, F., Quelques Observations sur les Abeilles et Particulièrement sur les Actes qui, chez ces Insectes Peuvent être Rapportès à l’Intelligence, Ann. Sci. Nat. Zool., 1853, vol. 18, pp. 231–240.Google Scholar
  3. 3.
    Flogel, J.H.L., Über den Feineren Bau des Arthropodengehirns, Tagesbl. Versamml. Dtschr. Naturforsch. Arzte, 1876, pp. 115–120.Google Scholar
  4. 4.
    Kenyon, F.C., The Meaning and Structure of the So-Called “Mushroom Bodies” of the Hexapod Brain, Amer. Natur., 1896, vol. 30, pp. 643–652.Google Scholar
  5. 5.
    Kenyon, F.C., The Brain of the Bee. A Preliminary Contribution to the Morphology of the Nervous System of the Arthropoda, J. Comp. Neurol., 1896, vol. 6, pp. 133–210.Google Scholar
  6. 6.
    Trompson, G.B., A Comparative Study of the Brains of Three Genera of Ants with Special Reference to the Mushroom Bodies, J. Comp. Neurol., 1913, vol. 23, pp. 515–567.Google Scholar
  7. 7.
    Malaterre, J., Strambi, C, Chiang, Ann-shyn, Aoyane, A., Strambi, A., and Cayre, M., Development of Cricket Mushroom Bodies, Comp. Neurol., 2002, vol. 452, no. 3, pp. 215–227.Google Scholar
  8. 8.
    Strausfeld, N.J., Hansen, L., Li, Y., Gomez, R.S., and Ito, K., Evolution, Discovery and Interpretation of Arthropod Mushroom Bodies, Learn. Mem., 1998, vol. 5, pp. 11–37.Google Scholar
  9. 9.
    Weiss, P.H., Neuronal Connections and the Function of the Corpora Pedunculata in the Brain of the American Cockroach, Periplaneta americana (L.), J. Morphol., 1974, vol. 142, pp. 21–69.Google Scholar
  10. 10.
    Howse, P.E., Brain Structure and Behavior in Insects, Annu. Rev. Entomol., 1975, vol. 20, pp. 359–379.Google Scholar
  11. 11.
    Schildberger, K., Some Physiological Features of Mushroom Body Linked Fibres in the House Cricket Brain, Naturwiss., 1981, vol. 67, p. 623.Google Scholar
  12. 12.
    Kaulen, P., Erber, J., and Mobbs, P.G., Current Source-Density Analysis in the Mushroom Bodies of the Honey Bee (Apis mellifera carnica), J. Comp. Physiol. A., 1984, vol. 154, pp. 569–582.Google Scholar
  13. 13.
    Mobbs, P.G., Brain Structure, Comprehensive Insect Pharmacology, vol. 5. Nervous System: Structure and Motor Function, Oxford et al., 1985, pp. 299–370.Google Scholar
  14. 14.
    Zawarzin, A.A., Zur Morphologie der Nervenzentren. Das Bauchmark der Insekten. Ein Beitrag zur Vergleichenden Histologie (Histologische Studien über Insekten V. VI), Z. wiss. Zool., 1924, vol. 122, pp. 323–424.Google Scholar
  15. 15.
    Neder, R., Allometrisches Wachatum von Hirnteiler bei Drei Verschieden Grossen Schabenarter, Zool. Jahrb. Anat., 1959, vol. 4, pp. 411–464.Google Scholar
  16. 16.
    Witthöft, W., Absolute Anzahl und Verteilung der Zellen im Hirn der Honigsbine, Z. Morhol. Tiere., 1967, vol. 61, pp. 160–184.Google Scholar
  17. 17.
    Schürmann, F.W., Über die Struktur der Pilzkörper des Insektenhirns. III. Die Anatomie der Nervenfasern in den Corpora Pedunculata bei Acheta domesticus L. (Orthoptera): eine Golgi-Studie, Z. Zellforsch., 1973, vol. 145, pp. 247–285.Google Scholar
  18. 18.
    Leitch, B. and Laurent, G., GABAergic Synapses in the Antennal Lobe and Mushroom Body of the Locust Olfactory System, J. Comp. Neurol., 1996, vol. 372, pp. 487–514.Google Scholar
  19. 19.
    Strausfeld, N.J., Atlas of an Insect Brain, Berlin; Heidelberg; New York, 1976.Google Scholar
  20. 20.
    Gronenberg, W., Physiological and Anatomical Properties of Optical Input-Fibers to the Mushroom Body of the Bee Brain, J. Insect Physiol., 1986, vol. 32, pp. 625–704.Google Scholar
  21. 21.
    Mizunami, M., Okada, R., Li, Y., and Strausfeld, N.J., Mushroom Bodies of the Cockroach: Activity and Identities of Neurons Recorded in Freely Moving Animals, J. Comp. Neurol., 1998, vol. 402, pp. 501–519.Google Scholar
  22. 22.
    Mizunami, M., Weibrecht, J.M., and Strausfeld, N.J., The Cockroach Mushroom Body: Its Participation in Place Memory, J. Comp. Neurol., 1998, vol. 402, pp. 520–537.Google Scholar
  23. 23.
    Strausfeld, N.J., The Insect Mushroom Body: A Uniquely Identifiable Neuropil, Identified Neurons in Model Systems, Cambridge, 1998.Google Scholar
  24. 24.
    Strausfeld, N.J. and Li, Y., Organization of Olfactory and Multimodal Afferent Neurons Supplying the Calyx and Pedunculus of the Cockroach Mushroom Bodies, J. Comp. Neurol., 1999, vol. 409, pp. 603–625.Google Scholar
  25. 25.
    Li, Y.-S. and Strausfeld, N.J., Morphology and Sensory Modality of Mushroom Body Efferent Neurons in the Brain of the Cockroach, Periplaneta americana, J. Comp. Neurol., 1997, vol. 387, pp. 631–650.Google Scholar
  26. 26.
    Mizunami, M., Jwazaki, M., and Okada, R., Topography of Modular Subunits in the Mushroom Bodies of the Cockroach, J. Comp. Neurol., 1998, vol. 399, pp. 153–161.Google Scholar
  27. 27.
    Strausfeld, N.J., Bassemir, U., Singh, R.N., and Bacon, J.P., Organizational Principles of Outputs from Dipteran Brains, J. Insect Physiol., 1984, vol. 30, pp. 73–93.Google Scholar
  28. 28.
    Heisenberg, M., Borst, A., Wagner, S., and Byers, J., Drosophila Mushroom Body Mutants Are Deficient in Olfactory Learning, J. Neurogen., 1985, vol. 2, pp. 1–30.Google Scholar
  29. 29.
    Mauelshagen, J., Neural Correlates of Olfactory Learning Paradigms in an Identified Neuron in the Honeybee Brain, J. Neurophysiol., 1993, vol. 69, pp. 609–625.Google Scholar
  30. 30.
    de Belle, J.S. and Heisenberg, M., Associative Odor Learning in Drosophila Abolished by Chemical Ablation of Mushroom Bodies, Science, 1994, vol. 263, pp. 692–695.Google Scholar
  31. 31.
    Davis, R., Mushroom Bodies and Drosophila Learning, Neuron, 1993, vol. 3, pp. 1–14.Google Scholar
  32. 32.
    Mobbs, P.G., Neural Networks in the Mushroom Bodies, J. Insect Physiol., 1984, vol. 30, pp. 43–58.Google Scholar
  33. 33.
    Gronenberg, W., Anatomical and Physiological Properties of Feedback Neurons of the Mushroom Bodies in the Bee Brain, Exp. Biol., 1987, vol. 46, pp. 115–125.Google Scholar
  34. 34.
    Grünewald, B., Morphology of Feedback Neurons in the Mushroom Body of the Honey Bee, Apis mellifera, J. Comp. Neurol., 1999, vol. 404, pp. 114–126.Google Scholar
  35. 35.
    Erber, J., Homberg, U., and Gronenberg, W., Functional Roles of the Mushroom Bodies in Insects, Arthropod Brain, New York, 1980, pp. 485–511.Google Scholar
  36. 36.
    Voskresenskaya, A.K., On Role of Mushroom Bodies of the Supraesophageal Ganglion in Conditioned Reflexes of the Honeybee, Dokl. Akad. Nauk SSSR, 1957, vol. 112, pp. 964–967.Google Scholar
  37. 37.
    Panov, A.A., On Formation of the Neuropil Glomerular Structure of the Insect Brain, Zool. Zh., 1959, vol. 38, pp. 775–777.Google Scholar
  38. 38.
    Gronenberg, W., Physiological and Anatomical Properties of Optical Input Fibers to the Mushroom Body of the Bee Brain, J. Insect. Physiol., 1986, vol. 32, pp. 625–704.Google Scholar
  39. 39.
    Li, Y.-S. and Strausfeld, N.J., Afferents Supplying Insect Mushroom Bodies Carry Multimodal Sensory Information, Soc. Neurosci. Abstr., 1977, vol. 23, p. 1571.Google Scholar
  40. 40.
    Strausfeld, N.J., Oculomotor Control in Flies: from Muscles to Elementary Motion Detectors, Neurons, Networks and Motor Behavior, Oxford, 1997, pp. 277–284.Google Scholar
  41. 41.
    Wolf, R., Witting, T., Liu, L., Wustman, G., Eyding, D., and Heisenberg, M., Drosophila Mushroom Bodies Are Dispensable for Visual, Tactile and Motor Learning, Learn. Mem., 1998, vol. 5, pp. 166–178.Google Scholar
  42. 42.
    Huber, F., Central Control of Sound Production in Crickets and Some Speculation on Its Evolution, Evolution, 1962, vol. 14, pp. 429–442.Google Scholar
  43. 43.
    Huber, F., Neural Integration (Central Nervous System), The Physiology of Insecta, New York, 1965, vol. 2, pp. 333–406.Google Scholar
  44. 44.
    Huber, F., Untersuchungen über der Fortbewegung und der Lauterzeugung der Grillen, Z. Vergl. Physiol., 1960, vol. 44, pp. 60–132.Google Scholar
  45. 45.
    Wadepuhl, M., Control of Grasshopper Singing Behavior by the Brain: Responses to Electrical Stimulation, Z. Tierpsychol., 1983, vol. 63, pp. 173–200.Google Scholar
  46. 46.
    Ferveur, J.F., Stortkuhl, K.F., Stoker, R.F., and Greenspan, R.F., Genetic Feminization of Brain Structure and Changed Sexual Orientation in Male Drosophila melanogaster, Science, 1995, vol. 267, pp. 902–905.Google Scholar
  47. 47.
    Neckameyer, W., Dopamine and Mushroom Bodies in Drosophila: Experience-Dependent and-Independent Aspects of Sexual Behavior, Learn. Mem., 1998, vol. 5, pp. 157–165.Google Scholar
  48. 48.
    Mizunami, M., Weibrecht, J.M., and Strausfeld, N.J., A New Role for the Insect Mushroom Bodies: Place Memory and Motor Control, Biological Neural Networks in Invertebrate Neuroethology and Robotics, Cambridge, 1993, pp. 199–225.Google Scholar
  49. 49.
    Martin, J.P. and Heisenberg, M., Effect of MushroomBody on Locomotor Activity in Drosophila, New Neuroethology on the Move, Proc. of the 26th Göttingen Neurobiology Conference, Stuttgart, 1998, vol. II, p. 70.Google Scholar
  50. 50.
    Chauvin, R., Vie et Moeurs des Insects, Paris, 1956.Google Scholar
  51. 51.
    Hanström, B., Vergleichende Anatomie des Nervensystems der wirbellosen Tiere unter Berücksichtigung Seiner Funktion, Berlin, 1928.Google Scholar
  52. 52.
    Lapitskii, V.P., Morphophysiological Peculiarities of Dorsal Connective Fibers of the Abdominal Nervous Chain of the Cockroach Periplaneta americana, Zh. Evol. Biokhim. Fiziol., 1987, vol. 18, pp. 361–365.Google Scholar
  53. 53.
    Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D., and Strausfeld, N.J., The Organization of Extrinsic Neurons and their Implications in the Functional Roles of the Mushroom Bodies of Drosophila melanogaster Meigen, Learn. Mem., 1998, vol. 5, pp. 52–77.Google Scholar
  54. 54.
    Svidersky, V.L., Osnovy neirofiziologii nasekomykh (Fundamentals of Insect Neurophysiology), Leningrad, 1980.Google Scholar
  55. 55.
    Bernshtein, N.A., O postroeinii dvizhenii (On Formation of Movements), Moscow, 1947.Google Scholar
  56. 56.
    Bernshtein, N.A., Ocherki po fiziologii dvizhenii i fiziologii aktivnosti (Essays of Physiology of Movements and Physiology of Activity), Moscow, 1966.Google Scholar
  57. 57.
    Erber, J., Masuhr, T., and Menzel, R., Localization of Short-Term Memory in the Brain of the Bee, Apies mellifera, Physiol. Entomol., 1980, vol. 5, pp. 343–358.Google Scholar
  58. 58.
    Heisenberg, M., Central Brain Function in Insects: Genetic Studies on the Mushroom Bodies and Central Complex in Drosophila, Neural Basis of Behavioural Adaptations, Stuttgart, 1994, pp. 61–79.Google Scholar
  59. 59.
    Heisenberg, M., What Do Mushroom Bodies Do for the Insect Brain?, Learn. Mem., 1998, vol. 5, pp. 1–10.Google Scholar
  60. 60.
    Pascual, A. and Preat, T., Localization of Long-Term Memory within the Drosophila Mushroom Body, Science, 2001, vol. 294, pp. 1115–1117.Google Scholar
  61. 61.
    Zars, T., Fischer, M., Schulz, R., and Heisenberg, M., Localization of a Short-Term Memory in Drosophila, Science, 2000, vol. 288, pp. 672–675.Google Scholar
  62. 62.
    Strausfeld, N.J., Organization of the Honey Bee Mushroom Body: Representation of the Calyx within the Vertical and Gamma Lobes, J. Comp. Neurol., 2002, vol. 450, pp. 4–33.Google Scholar
  63. 63.
    Tang, S. and Guo, A., Choice Behavior of Drosophila Facing Contradictory Visual Cues, Science, 2001, vol. 294, pp. 1543–1547.Google Scholar
  64. 64.
    Svidersky, V.L. and Plotnikova, S.I., Insects and Vertebrates: Analogous Structures in the Higher Integrative Brain Centers, Zh. Evol. Biokhim. Fiziol., 2002, vol. 38, pp. 493–501.Google Scholar
  65. 65.
    Zawarzin, A.A., Ocherki po evolyutsionnoi gistologii nervnoi sistemy (Essays on Evolutionary Histology of the Nervous System), Moscow, Leningrad, 1941.Google Scholar
  66. 66.
    Svidersky, V.L., Neirofiziologiya poleta nasekomykh (Neurophysiology of the Insect Flight), Leningrad, 1973.Google Scholar
  67. 67.
    Svidersky, V.L., Evolution of the Nervous System and Some General Problems of Locomotion of Invertebrates, Evoylutsionnaya fiziologiya (Evolutionary Physiology), Leningrad, 1979, pp. 24–80.Google Scholar
  68. 68.
    Svidersky, V.L., Mechanisms of Control of Insect Locomotion and Some General Problems of Neurophysiology of Motor Apparatus, Razvitie nauchnogo naslediya L.A. Orbeli (Development of L.A. Orbeli’s Scientific Inheritance), Leningrad, 1982, pp. 94–110.Google Scholar
  69. 69.
    Svidersky, V.L., The Main Principles of Control of Movements, Voprosy evolyutsionnoi fiziologii: Mater. IX Soveshch. po evol. fiziol. (Problems of Evolutionary Physiology: Proceed. IX Meet. Evol. Physiol.), Leningrad, 1986, p. 253.Google Scholar
  70. 70.
    Pearson, K.G., The Control of Walking, Sci. Amer., 1976, vol. 235, pp. 72–86.Google Scholar
  71. 71.
    Pearson, K.G., Common Principles of Motor Control in Vertebrates and Invertebrates, Annu. Rev. Neurosci., 1993, vol. 16, pp. 265–297.Google Scholar
  72. 72.
    Herrick, C.J., Neurological Foundation of Animal Behavior, New York, 1924.Google Scholar
  73. 73.
    Shepherd, G.M., Models for Molecules, Nature, 1992, vol. 358, pp. 456–457.Google Scholar
  74. 74.
    Zawarzin, A.A., Gistologicheskoe issledovanie chuvstvitel’ noi nervnoi sistemy i opticheskikh gangliev nasekomykh (Histological Study of the Sensory Nervous System and Optical Ganglia of Insects), St. Petersburg, 1913.Google Scholar
  75. 75.
    Zawarzin, A.A., Histologische Studien über Insekten. IV. Die Optische Ganglion der Aeschnalarven, Z. wiss. Zool., 1914, vol. 108, pp. 175–257.Google Scholar
  76. 76.
    Zawarzin, A.A., Einige Bemerkungen über den Bau der Optischen Zentren, Anat. Anz., 1924, vol. 59, pp. 551–559.Google Scholar
  77. 77.
    Sotnichenko, T.S., Fiziologiya i patofiziologiya limbikoretikulyarnoi sistemy (Physiology and Pathophysiology of the Limbic-Reticular System), Moscow, 1971.Google Scholar
  78. 78.
    Tolkunov, B.F., Non-Specific Brain Structures and Specialization in the Central Nervous System, Zh. Evol. Biochim. Fiziol., 1978, vol. 14, pp. 205–211.Google Scholar
  79. 79.
    Tolkunov, B.F., On Principles of Determination of Function of the Nervous Center (on the Example of Mammalian Neostriatum), Zh. Evol. Biochim. Fiziol., 1991, vol. 27, pp. 598–607.Google Scholar
  80. 80.
    Tolkunov, B.F., Orlov, A.A., and Mochenkov, B.P., Activity of Monkey Neostriatal Neurons in the Process of Instrumental Behavior, Neirofiziol., 1993, vol. 1, pp. 132–140.Google Scholar
  81. 81.
    Tolkunov, B.F., Role of Striatum in Evolution of the Mammalian Forebrain, Zh. Evol. Biochim. Fiziol., 1998, vol. 34, pp. 393–400.Google Scholar
  82. 82.
    Svidersky, V.L., Lokomotsiya nasekomykh: neirofiziologicheskie aspekty (Insect Locomotion: Neurophysiological Aspects), Leningrad, 1988.Google Scholar
  83. 83.
    Tolkunov, B.F., Orlov, A.A., and Afanas’ev, S.V., Model Concepts of Function of Neostriatum and Activity of Its Neurons in Behavior of Monkeys, Sechenov Fiziol. Zh., 1995, vol. 81, pp. 12–20.Google Scholar
  84. 84.
    Afanas’ev, S.V., Tolkunov, B.F., Orlov, A.A., and Selezneva, E.V., Collective Reactions of Neurons of Neostriatum (Putamen) during the Monkey Alternative Behavior, Sechenov Fiziol. Zh., 1997, vol. 83, pp. 19–27.Google Scholar

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© MAIK “Nauka/Interperiodica” 2004

Authors and Affiliations

  • V. L. Svidersky
    • 1
  • S. I. Plotnikova
    • 1
  1. 1.Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia

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