Mushroom bodies of the cockroach: Their participation in place memory

Journal of Comparative Neurology

Volumn 402, Issue 4, 1998, Pages 520-537

  Mizunami, Makoto ^a,c   Weibrecht, Josette M ^a,b   Strausfeld, Nicholas J ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

lobes; Insect brain; Insect vision; Learning; Microlesions; Motor control

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN; COCKROACH; CONTROLLED STUDY; FEMALE; LEARNING; LOCOMOTION; MALE; MAZE TEST; MEMORY; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BRAIN MAPPING; HOMING BEHAVIOR; LEARNING; MEMORY; PERIPLANETA;

EID: 0032576535     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19981228)402:4<520::AID-CNE6>3.0.CO;2-K     Document Type: Article

References (76)

1. Balderrama, N. (1980) One trial learning in the American cockroach, Periplaneta americana. J. Insect Physiol. 26:499-504.
2. Bicker, G., S. Schäfer, and V. Render (1987) Chemical neuroanatomy of the honeybee brain. In R. Menzel and A. Mercer (eds): Neurobiology and Behavior of Honeybees. Berlin: Springer, pp. 202-224.
3. Bitterman, M.E. and P.A. Couvillon (1991) Failures to find evidence of adaptive specialization in the learning of honeybees. In L.J. Goodman and R.C. Fisher (eds): The Behavior and Physiology of Bees. London: C.A.B. International, pp. 288-305.
4. Bodian, D. (1936) Anew method for staining nerve fibres and nerve endings in mounted paraffin sections. Anat. Rec. 65:89-97.
5. Cartwright, B.A. and T.S. Collett (1982) How honeybees use landmarks to guide their return to a food source. Nature 295:521-543.
6. Cartwright, B.A. and T.S. Collett (1983) Landmark learning in bees: Experiments and models. J. Comp. Physiol. A 757:521-543.
7. Castro, C.A., L.H. Silbert, B.L. McNaughton, and C.A. Barnes (1980) Recovery of spatial learning deficit after decay of the electrically induced synaptic enhancement in the hippocampus. Nature 342:545-548.
8. Cayre, M.C., C. Strambi, and A. Strambi (1994) Neurogenesis in an adult brain and its hormonal control. Nature 368:57-59.
9. Cayre, M., C. Strambi, P. Charpin, R. Augier, M.R. Meyer, J.S. Edwards, and A. Strambi (1996) Neurogenesis in adult insect mushroom bodies. J. Comp. Neurol. 377:300-310.
10. Cheng, K., T.S. Collett, A. Pickhard, and R. Wehner (1989) The use of visual landmarks by honeybees: Bees weight landmarks according to their distance from the goal. J. Comp. Physiol. A 767:469-475.
11. Collett, T.S. (1978) Peering: A locust behavior for obtaining motion parallax information. J. Exp. Biol. 76:23-24.
12. Collett, T.S. (1992). Landmark learning and guidance in insects. Philos. Trans. R. Soc. Lond. B 337:295-303.
13. Collett, T.S., S.N. Fry, and R. Wehner (1993) Sequence learning in honeybees. J. Comp. Physiol. A 772:693-706.
14. Cleveland, L.R., S.R. Hall, E.P. Sanders, and J. Collier (1932) The wood-feeding roach, Cryptocercus, its protozoa, and the symbiosis between protozoa and roach. Mem. Am. Acad. Arts Sci. 77:185.
15. Davis, R.L. and K.-A. Han. (1996) Mushrooming mushroom bodies. Curr. Biol. 6:146-148.
16. de Belle, J.S. and M. Heisenberg (1994) Associative learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
17. Dujardin, F. (1850) Mémoire sur le système nerveux des insects. Ann. Sci. Nat. Zool. 74:195-206.
18. Dujardin, F. (1853) Quelques observations sur les abeilles et particulirement sur les actes qui, chez ces insectes peuvent être rapportés à l'intelligence. Ann. Sci. Nat. Zool. 78:231-240.
19. Dyer, F.C. (1991) Bees acquire route-based memories but not cognitive maps in a familiar landscape. Anim. Behav. 47:234-246.
20. Erber, J., U. Homberg, and W. Gronenberg (1987) Functional roles of the mushroom bodies in insects. In A.P. Gupta (ed): Arthropod Brain. New York: Wiley-Interscience, pp. 485-511.
21. Fahre, J.-H. (1910) Souvenirs entomologiques. Etudes sur l'instinct et les moeurs des insectes. Paris: C. Delagrave.
22. Frisch, K von. (1965) Tanzsprache und Orientierung der Bienen. Heidelberg: Springer.
23. Gould, J.L. (1986) The locale map of honey bees: Do insects have cognitive maps? Science 232:861-863.
24. Gregory, G.E. (1980) The Bodian protargol technique. In: N.J. Strausfeld and T.A. Miller (eds): Neuroanatomical Techniques: Insect Nervous System. New York, Heidelberg, Berlin: Springer, pp. 75-95.
25. Gronenberg, W. (1986) Physiological and anatomical properties of optical input-fibers to the mushroom body in the bee brain. J. Insect Physiol. 32:695-704.
26. Gronenberg, W., S. Heeren, and B. Hölldobler (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotusfloridanus. J. Exp. Biol. 759:2011-2019.
27. Heisenberg, M. (1980) Mutations of brain structure and function: What is the significance of the mushroom bodies for behavior. In O. Siddiqi, P. Babu, L.M. Hall, and J.C. Hall (eds): Development and Neurobiology of Drosophila. New York: Plenum, pp. 373-390.
28. Heisenberg, M. (1998) What do the mushroom bodies do for the insect brain? Learning Memory 5:1-10.
29. Heisenberg, M., A. Borst, S. Wagner, and D. Byers (1985). Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet.2:l-30.
30. Homberg, U. (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J. Comp. Physiol. A 154:825-836.
31. Huber, F. (I960) Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirns bei der Fortbewegung und der Lauterzeugung der Grillen. Z. Vgl. Physiol. 44:60-132.
32. Hughes, D. (1966) Behavioral and ecological investigations of the crab Ocypode ceratopthalmus (Crustacea: Ocypodidae). J. Zool. 150:129-143.
33. Ito, K. and Y. Hotta (1992) Proliferation pattern of embryonic neuroblasts in the brain of Drosophila melanogaster. Dev. Biol. 149:134-148.
34. Ito, K., W. Awano, K. Suzuki, Y. Hiromi, and D. Yamamato (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:161-111.
35. Ito, K., K. Suzuki, P. Estes, M. Ramaswami, D. Yamamoto, and N.J. Strausfeld (1998) The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learning Memory 5:52-77.
36. Kandel, E. and T. Abel (1995) Neuropeptides, adenylyl cyclase, and memory storage. Science 265:8225-8226.
37. Kukalovd-Peck, L. (1991) Fossil history and the evolution of hexapod structures. In: The Insects of Australia, Vol. 1. Melbourne: Melbourne University Press, pp. 141-180.
38. Labhart, T. (1988) Polarization-opponent interneurons in the insect visual system. Nature 33/:435-437.
39. Lehrer, M. (1993) Why do bees turn back and look? J. Comp. Physiol. A 172:549-563.
40. Lehrer, M., M.V. Srinivasan, S.W. Zhang, and G.A. Horridge (1988) Motion cues provide the bee's visual world with a third dimension. Nature 332:356-357.
41. Li, Y.-S. and N.J. Strausfeld (1997) Morphology and sensory modality of mushroom body efferent neurons in the brain of the cockroach, Periplaneta americana. J. Comp. Neurol. 357:631-650.
42. Martin, J.-P. and M. Heisenberg (1998) Effect of mushroom-body on locomotor activity in Drosophila. In N. Eisner and R. Wehner (eds): New Neuroethology on the Move (Proceedings of the 26th Göttingen Neurobiology Conference. Vol. II). Stuttgart: Thieme, p. 70.
43. Mizunami, M., J.M. Weibrecht, and N.J. Strausfeld (1993) A new role for the insect mushroom bodies: Place memory and motor control. In R.D. Beer, R. Ritzmann, and T. McKenna (eds): Biological Neural Networks in Invertebrate Neuroethology and Robotics. Cambridge, MA: Academic Press, pp. 199-225.
44. Mizunami, M., R. Okada, Y.-S. Li, and N.J. Strausfeld (1998) Cockroach mushroom bodies: Activity and identity of neurons in freely moving animals. J. Comp. Neurol. 402:501-519.
45. Mobbs, P.G. (1982) The brain of the honeybee Apis mellifcra. I. The connections and spatial organizations of the mushroom bodies. Philos. Trans. R. Soc. Lond. B 298:309-354.
46. Mobbs, P.G. (1984) Neural networks in the mushroom bodies of the honeybee. J. Insect Physiol. 30:43-58.
47. Morris, R.G.M., P. Garrud, J.N.P. Raulins, and J. O'Keefe (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
48. Mote, M.I. (1990) Structure and function of the visual systems of the American cockroach. In I. Huber, E.P. Masler, and B.R. Rao (eds): Cockroaches as Models for Neurobiology. Boca Raton: CRC Press, pp. 203-224.
49. Muller, R. (1996) Aquarter of a century of place cells. Neuron J7.-813-822.
50. O'Keefe, J. and D.H. Conway (1978) Hippocampal place units in the freely moving rat: Why they fire where they fire. Exp. Brain Res. 31:573-590.
51. O'Shea, M. and M. Adams (1981) Pentapeptide (proctolin) associated with an identified neuron. Science 213:567-569.
52. Papi, F. (1992) Animal homing: General aspects. In F. Papi (ed): Animal Homing. London: Chapman and Hall, pp. 1-18.
53. Quinn, W.G., W.A. Harris, and S. Benzer (1974) Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 7J.-708-712.
54. Rossel, S. (1989) Polarization sensitivity in compound eyes. In D.G. Stavenga and R.C. Hardie (eds): Facets of Vision. Heidelberg: Springer, pp. 298-316.
55. Rybak, J. and R. Menzel (1993) Anatomy of the mushroom bodies in the honey bee brain: The neuronal connections of tbe alpha-lobe. J. Comp. Neurol. 334:444-465.
56. Schildberger, K. (1981). Some physiological features of mushroom body linked fibers in the house cricket brain. Naturwissenschaften 67:623.
57. Schildberger, K. (1984) Multimodal interneurons in the cricket brain: Properties of identified extrinsic mushroom body cells. J. Comp. Physiol. A 754:71-79.
58. Schürmann, F.W. and J. Erber (1990) FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifcra): A light and electron microscopical study. Neuroscience 38:797-807.
59. Srinivasan, M.V., M. Lehrer, S.W. Zhang, and G.A. Horridge (1989) How honeybees measure distance from objects of unknown size. J. Comp. Physiol. A 165:119-122.
60. Stocker, R.F.M. (1994) The organization of the chemosensory system in Drosophila melanogaster. Cell Tissue Res. 275:3-26.
61. Strausfeld, N.J. and H.J. Wunderer (1985) Optic lobe projections of marginal ommatidia in Calliphora specialized for detecting polarized light. Cell Tissue Res. 242:163-178.
62. Strausfeld, N.J., L. Hansen, Y.-S. Li, R.S. Gomez, and K. Ito (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning Memory 5:11-37.
63. Strauss, R. and M. Heisenberg (1993) A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13:1852-1861.
64. Tinbergen, N. and W. Kruyt (1938) über die Orientierung des Bienenwolfes (Philanthus triangulum Fabre). III. Die Bevorzugung bestimmter Wegmarken. Z. Vgl. Physiol. 25:292-334.
65. Tolman, E.G. (1948) Cognitive maps in rats and men. Psychol. Rev. 55:189-208.
66. Vowles, D.M. (1964) Olfactory learning and brain lesion in the wood ant (Formica rufa). J. Camp. Physiol. Psychol. 58:105-111.
67. Wehner, R. (1987) Matched filters as neural models of the external world. J. Comp. Physiol.A767:511-531.
68. Wehner, R. (1992) Arthropods. In F. Papi (ed): Animal Homing. London: Chapman and Hall, pp. 45-144.
69. Wehner, R. and R. Menzel (1990) Do insects have cognitive maps? Annu. Rev. Neurosci. 73:403-414.
70. Wehner, R. and S. Wehner (1990) Insect navigation: Use of maps or Ariadne's thread. Ethol. Ecol. Evol. 2:27-48.
71. Weibrecht, J. and N.J. Strausfeld (1993) Strategies employed in visual discrimination and searching by cockroaches during place memory acquisition. Soc. Neurosci. Abstr. 79:815.
72. Wilson, M.A. and B.L. McNaughton (1993) Dynamics of the hippocampal ensemble code for space. Science 267:1055-1058.
73. Withers, O.S., S.E. Fahrbach, and G.E. Robinson (1995) Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J. Neurobiol. 26:130-144.
74. Yang, M.Y., J.D. Armstrong, I. Vilinsky, N.J. Strausfeld, and K. Kaiser (1995) Subdivision of the Drosophila mushroom bodies by enhancertrap expression patterns. Neuron 75:45-54.
75. Zeil, J. (1993a) Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera). I. Description of flight. J. Comp. Physiol. A 772:189-205.
76. Zeil, J. (1993b) Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera). II. Similarities between orientation and return flights and the use of motion parallax. J. Comp. Physiol. A 7 72:207-222.