Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain

Journal of Comparative Neurology

Volumn 520, Issue 8, 2012, Pages 1599-1628

  Heinze, Stanley ^a   Reppert, Steven M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Antennal lobes; Central complex; Comparative neuroanatomy; Danaus plexippus; Mushroom body; Visual system

Indexed keywords

4 AMINOBUTYRIC ACID; SEROTONIN; SYNAPSIN;

ACCESSORY NERVE; ANATOMICAL VARIATION; ANTENNA (ORGAN); ANTIBODY LABELING; ARTICLE; ASSOCIATION; BRAIN; BRAIN FUNCTION; BRAIN GANGLION; BUTTERFLY; CENTRAL SULCUS; CEREBRAL PEDUNCLE; CIRCADIAN RHYTHM; COMPARATIVE ANATOMY; DANAUS PLEXIPPUS; IMAGE ANALYSIS; IMAGE RECONSTRUCTION; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MUSHROOM BODY; NERVE FIBER; NEUROANATOMY; NEURONAVIGATION; NEUROPIL; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; OPTIC LOBE; PRIORITY JOURNAL;

ANIMAL MIGRATION; ANIMALS; BRAIN; BUTTERFLIES; CUES; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; NEUROPIL; SUNLIGHT;

EID: 84859305210     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23054     Document Type: Article

References (78)

1. Berg BG, Galizia CG, Brandt R, Mustaparta H. 2002. Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J Comp Neurol 446: 123-134.
2. Berg BG, Schachtner J, Homberg U. 2009. Gamma-aminobutyric acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropeptides. Cell Tissue Res 335: 593-605.
3. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege H-C, Menzel R. 2005. Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492: 1-19.
4. Dacks AM, Christensen TA, Hildebrand JG. 2006. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498: 727-746.
5. Dickens J, Eaton J. 1973. External ocelli in Lepidoptera previously considered to be anocellate. Nature 242: 205-206.
6. 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.
7. 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.
8. El Jundi B, Huetteroth W, Kurylas AE, Schachtner J. 2009. Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 517: 210-225.
9. Fischbach KF, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I: A. Golgi analysis of wild-type structure. Cell Tissue Res 258: 441-475.
10. Froy O, Gotter AL, Casselman AL, Reppert SM. 2003. Illuminating the circadian clock in monarch butterfly migration. Science 300: 1303-1305.
11. Gronenberg W. 2001. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435: 474-489.
12. Gronenberg W, Hölldobler B. 1999. Morphologic representation of visual and antennal information in the ant brain. J Comp Neurol 412: 229-240.
13. Hanesch U, Fischbach KF, Heisenberg M. 1989. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343-366.
14. Heinze S, Homberg U. 2007. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315: 995-997.
15. Heinze S, Homberg U. 2008. Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511: 454-478.
16. Heinze S, Reppert SM. 2011. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69: 345-358.
17. Heinze S, Gotthardt S, Homberg U. 2009. Transformation of polarized light information in the central complex of the locust. J Neurosci 29: 11783-11793.
18. Homberg U. 1991. Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303: 245-254.
19. Homberg U. 2004. In search of the sky compass in the insect brain. Naturwissenschaften 91: 199-208.
20. Homberg U. 2008. Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37: 347-362.
21. Homberg U, Hildebrand JG. 1989. Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res 258: 1-24.
22. Homberg U, Paech A. 2002. Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30: 271-280.
23. Homberg U, Kingan TG, Hildebrand JG. 1987. Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248: 1-24.
24. 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.
25. Homberg U, Würden S, Dircksen H, Rao K. 1991. Comparative anatomy of pigment-dispersing hormone-immunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 266: 343-357.
26. Homberg U, Vitzthum H, Müller M, Binkle U. 1999. Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409: 495-507.
27. Homberg U, Hofer S, Pfeiffer K, Gebhardt S. 2003. Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462: 415-430.
28. 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.
29. Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG. 1986. Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 244: 243-252.
30. Huetteroth W, Schachtner J. 2005. Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity. Cell Tissue Res 319: 513-524.
31. Huetteroth W, El Jundi B, El Jundi S, Schachtner J. 2010. Frontiers: 3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta. Front Syst Neurosci 4: 7.
32. Ignell R, Dekker T, Ghaninia M. 2005. Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493: 207-240.
33. Iwano M, Hill ES, Mori A, Mishima T, Mishima T, Ito K, Kanzaki R. 2010. Neurons associated with the flip-flop activity in the lateral accessory lobe and ventral protocerebrum of the silkworm moth brain. J Comp Neurol 518: 366-388.
34. 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.
35. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16: 3154-3165.
36. 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.
37. Kvello P, Løfaldli BB, Rybak J, Menzel R, Mustaparta H. 2009. Digital, three-dimensional average shaped atlas of the Heliothis virescens brain with integrated gustatory and olfactory neurons. Front Syst Neurosci 3: 14.
38. Labhart T, Meyer EP. 1999. Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47: 368-379.
39. Labhart T, Baumann F, Bernard GD. 2009. Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have non-functional reflecting tapeta. Cell Tissue Res 338: 391-400.
40. Merlin C, Gegear RJ, Reppert SM. 2009. Antennal circadian clocks coordinate sun compass orientation in migratory monarch butterflies. Science 325: 1700-1704.
41. Mota T, Yamagata N, Giurfa M, Gronenberg W, Sandoz JC. 2011. Neural organization and visual processing in the anterior optic tubercle of the honeybee brain. J Neurosci 31: 11443-11456.
42. Mouritsen H, Frost BJ. 2002. Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. Proc Natl Acad Sci U S A 99: 10162-10166.
43. Müller M, Homberg U, Kühn A. 1997. Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288: 159-176.
44. Nordlander RH, Edwards JS. 1968. Morphology of the larval and adult brains of the monarch butterfly, Danaus plexippus plexippus, L. J Morphol 126: 67-94.
45. 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.
46. Ott SR. 2008. Confocal microscopy in large insect brains: zinc-formaldehyde fixation improves synapsin immunostaining and preservation of morphology in whole-mounts. J Neurosci Methods 172: 220-230.
47. Pearson L. 1971. The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera - an anatomical study. Philos Trans R Soc Lond B Biol Sci 259: 477-516.
48. Perez S, Taylor O, Jander R. 1997. A sun compass in monarch butterflies. Nature 387: 29-29.
49. Pfeiffer K, Homberg U. 2007. Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17: 960-965.
50. 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: 212-219.
51. 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 Neurophys 94: 3903-3915.
52. Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M. 2002. The Drosophila standard brain. Curr Biol 12: 227-231.
53. Reppert SM. 2006. A colorful model of the circadian clock. Cell 124: 233-236.
54. Reppert SM, Zhu H, White RH. 2004. Polarized light helps monarch butterflies navigate. Curr Biol 14: 155-158.
55. Reppert SM, Gegear RJ, Merlin C. 2010. Navigational mechanisms of migrating monarch butterflies. Trends Neurosci 33: 399-406.
56. Sakura M, Lambrinos D, Labhart T. 2008. Polarized skylight navigation in insects: model and electrophysiology of e-vector coding by neurons in the central complex. J Neurophys 99: 667-682.
57. Sauman I, Briscoe AD, Zhu H, Shi D, Froy O, Stalleicken J, Yuan Q, Casselman A, Reppert SM. 2005. Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 46: 457-467.
58. Schildberger K. 1983. Local interneurons associated with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res 230: 573-586.
59. Sjöholm M, Sinakevitch I, Ignell R, Strausfeld NJ, Hansson BS. 2005. Organization of Kenyon cells in subdivisions of the mushroom bodies of a lepidopteran insect. J Comp Neurol 491: 290-304.
60. 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.
61. Skiri HT, Rø H, Berg BG, Mustaparta H. 2005. Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J Comp Neurol 491: 367-380.
62. Stalleicken J, Labhart T, Mouritsen H. 2006. Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J Comp Physiol A 192: 321-331.
63. Strausfeld NJ. 1970. Golgi studies on insects. Part II. The optic lobes of diptera. Philos Trans R Soc Lond B Biol Sci 258: 135-223.
64. Strausfeld NJ. 1976. Atlas of an insect brain. New York: Springer.
65. Strausfeld NJ. 1999. A brain region in insects that supervises walking. Prog Brain Res 123: 273-284.
66. Strausfeld NJ. 2002. Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450: 4-33.
67. Strausfeld N, Blest AD. 1970. Golgi studies on insects. Part I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond B Biol Sci 258: 81-134.
68. Strausfeld NJ, Sinakevitch I, Brown SM, Farris SM. 2009. Ground plan of the insect mushroom body: functional and evolutionary implications. J Comp Neurol 513: 265-291.
69. Strauss R. 2002. The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12: 633-638.
70. 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.
71. Wei H, El Jundi B, Homberg U, Stengl M. 2010. Implementation of pigment-dispersing factor-immunoreactive neurons in a standardized atlas of the brain of the cockroach Leucophaea maderae. J Comp Neurol 518: 4113-4133.
72. Weiss MJ. 1981. Structural patterns in the corpora pedunculata of orthoptera: a reduced silver analysis. J Comp Neurol 203: 515-553.
73. Wendt B, Homberg U. 1992. Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol 321: 387-403.
74. Williams JLD. 1975. Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool 176: 67-86.
75. Young JM, Armstrong J. 2010. Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J Comp Neurol 518: 1500-1524.
76. Zhan S, Merlin C, Boore JL, Reppert SM. 2011. The monarch butterfly genome yields insights into long-distance migration. Cell 147: 1171-1185.
77. Zhu H, Casselman AL, Reppert SM. 2008. Chasing migration genes: a brain expressed sequence tag resource for summer and migratory monarch butterflies (Danaus plexippus). PLoS ONE 3: e1345.
78. Zhu H, Gegear RJ, Casselman AL, Kanginakudru S, Reppert SM. 2009. Defining behavioral and molecular differences between summer and migratory monarch butterflies. BMC Biol 7: 14.