Transmedulla Neurons in the Sky Compass Network of the Honeybee (Apis mellifera) Are a Possible Site of Circadian Input

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Zeller, Maximilian ^a   Held, Martina ^a   Bender, Julia ^a   Berz, Annuska ^a   Heinloth, Tanja ^a   Hellfritz, Timm ^a   Pfeiffer, Keram ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; PHALLOIDIN; SEROTONIN; SYNAPSIN; NEUROPEPTIDE;

ANIMAL TISSUE; APIS MELLIFERA; ARTICLE; CELL COMPARTMENTALIZATION; CIRCADIAN INPUT; CIRCADIAN RHYTHM; CONTROLLED STUDY; IMMUNOREACTIVITY; NERVE CELL; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; SKY COMPASS NETWORK; SYNAPTIC TRANSMISSION; SYNAPTOSOME; TRANSMEDULLA NEURON; ANIMAL; BEE; CYTOLOGY; DEPTH PERCEPTION; MEDULLA OBLONGATA; METABOLISM; ORIENTATION; PHYSIOLOGY;

ANIMALS; BEES; CIRCADIAN CLOCKS; GAMMA-AMINOBUTYRIC ACID; MEDULLA OBLONGATA; NERVE NET; NEURONS; NEUROPEPTIDES; ORIENTATION; SEROTONIN; SPACE PERCEPTION;

EID: 84955589673     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143244     Document Type: Article

References (87)

1. von Frisch K. Die Sonne als Kompass im Leben der Bienen. Experientia 1950; 6:210-21.
2. von Frisch K. Gelöste und ungelöste Rätsel der Bienensprache. Naturwissenschaften 1948; 35:12-23.
3. von Frisch K. Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 1949; 5:142-8. PMID: 18126348
4. Strutt JW. On the light from the sky, its polarization and color. Phil Mag 1871; 41:274-9.
5. Coulson KL. Polarization and intensity of light in the atmosphere. Hampton: A. Deepak Publishing; 1988.
6. Coemans MA, Vos Hzn JJ, Nuboer JF. The relation between celestial colour gradients and the position of the sun, with regard to the sun compass. Vision Res 1994; 34:1461-70. PMID: 8023458
7. Lehrer M, editor. Orientation and Communication in Arthropods. Basel: Birkhäuser; 1997.
8. el Jundi B, Smolka J, Baird E, Byrne MJ, Dacke M. Diurnal dung beetles use the intensity gradient and the polarization pattern of the sky for orientation. J Exp Biol 2014; 217: 2422-9. doi: 10.1242/jeb. 101154 PMID: 24737763
9. Lebhardt F, Ronacher B. Transfer of directional information between the polarization compass and the sun compass in desert ants. J Comp Physiol A 2014; 201:599-608. doi: 10.1007/s00359-014-0928-9
10. Kinoshita M, Pfeiffer K, Homberg U. Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 2007; 210:1350-61. doi: 10. 1242/jeb.02744 PMID: 17401118
11. Pfeiffer K, Homberg U. Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 2007; 17:960-5. doi: 10.1016/j.cub.2007.04.059 PMID: 17524646
12. Heinze S, Reppert SM. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 2011; 69:345-58. doi: 10.1016/j.neuron.2010.12.025 PMID: 21262471
13. el Jundi B, Warrant EJ, Byrne MJ, Khaldy L, Baird E, Smolka J, et al. Neural coding underlying the cue preference for celestial orientation. Proc Nat Acad Sci 2015; 112:11395-400. doi: 10.1073/pnas. 1501272112 PMID: 26305929
14. Labhart T, Meyer EP. Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 1999; 47:368-79. doi: 10.1002/(SICI) 1097-0029(19991215)47:6<368::AID-JEMT2>3.0.CO;2-Q PMID: 10607378
15. el Jundi B, Pfeiffer K, Homberg U. A distinct layer of the medulla integrates sky compass signals in the brain of an insect. PLoS One 2011; 6:e27855. doi: 10.1371/journal.pone.0027855 PMID: 22114712
16. Lindauer M. Dauertänze im Bienenstock und ihre Beziehung zur Sonnenbahn. Naturwissenschaften 1954; 41:506-7.
17. Helfrich-Förster C, Homberg U. Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 1993; 337:177-90. doi: 10.1002/cne.903370202 PMID: 8276996
18. Helfrich-Förster C, Stengl M, Homberg U. Organization of the circadian system in insects. Chronobiol Int 1998; 15:567-94. PMID: 9844747
19. Stengl M, Homberg U. Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A 1994; 175:203-13. PMID: 8071895
20. Park JH, Helfrich-Förster C, Lee G, Liu L, Rosbash M, Hall JC. Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Nat Acad Sci 2000; 97:3608-13. doi: 10. 1073/pnas.070036197 PMID: 10725392
21. Hassaneen E, El-Din Sallam A, Abo-Ghalia A, Moriyama Y, Karpova SG, Abdelsalam S, et al. Pigmentdispersing factor affects nocturnal activity rhythms, photic entrainment, and the free-running period of the circadian clock in the cricket Gryllus bimaculatus. J Biol Rhythms 2011; 26:3-13. doi: 10.1177/ 0748730410388746 PMID: 21252361
22. Shafer OT, Zepeng Y. Pigment-dispersing factor signaling and circadian rhythms in insect locomotor activity. Curr Opin Insect Sci 2014; 1:73-80. doi: 10.1016/j.cois.2014.05.002 PMID: 25386391
23. Sumiyoshi M, Sato S, Takeda Y, Sumida K, Koga K, Itoh T, et al. A circadian neuropeptide PDF in the honeybee, Apis mellifera: cDNA cloning and expression of mRNA. Zoolog Sci 2011; 28:897-909. doi: 10.2108/zsj.28.897 PMID: 22132787
24. Pyza E, Meinertzhagen IA. Neurotransmitters regulate rhythmic size changes amongst cells in the fly's optic lobe. J Comp Physiol A 1996; 178:33-45. PMID: 8568723
25. Tomioka K, Ikeda M. Involvement of serotonin in the circadian rhythm of an insect visual system. Naturwissenschaften 1993; 80:137-9.
26. Saifullah ASM, Tomioka K. Serotonin sets the day state in the neurons that control coupling between the optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. J Exp Biol 2002; 205:1305-14. PMID: 11948207
27. Saifullah ASM, Tomioka K. Pigment-dispersing factor sets the night state of the medulla bilateral neurons in the optic lobe of the cricket, Gryllus bimaculatus. J Insect Physiol 2003; 49:231-9. PMID: 12769998
28. Chen B, Meinertzhagen IA, Shaw SR. Circadian rhythms in light-evoked responses of the fly's compound eye, and the effects of neuromodulators 5-HT and the peptide PDF. J Comp Physiol A 1999; 185:393-404. PMID: 10573867
29. Kloppenburg P, Erber J. The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). II. Electrophysiological analysis of motion-sensitive neurons in the lobula. J Comp Physiol A 1995; 176:119-29.
30. Labhart T. Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: polarizational and angular sensitivity. J Comp Physiol A 1980; 141:19-30.
31. Neumann E, Kakorin S, Toensing K. Fundamentals of electroporative delivery of drugs and genes. Bioelectrochemistry and bioenergetics (Lausanne, Switzerland) 1999; 48:3-16. doi: 10.1016/S0302- 4598(99)00008-2
32. Dircksen H, Zahnow C, Gaus G, Keller R, Rao K, Riehm J. The ultrastructure of nerve endings containing pigment-dispersing hormone (PDH) in crustacean sinus glands: Identification by an antiserum against a synthetic PDH. Cell Tissue Res 1987; 250:377-87.
33. Bonomelli SL, Rao KR, Riehm JP. Development and application of an ELISA for crustacean beta-PDH. Am Zool 1988; 28:A117-117.
34. Homberg U, Davis NT, Hildebrand JG. Peptide-immunocytochemistry of neurosecretory cells in the brain and retrocerebral complex of the sphinx moth Manduca sexta. J Comp Neurol 1991; 303:35-52. doi: 10.1002/cne.903030105 PMID: 1706364
35. Homberg U, Würden S, Dircksen H, Rao KR. Comparative anatomy of pigment-dispersing hormoneimmunoreactive neurons in the brain of orthopteroid insects. Cell Tissue Res 1991; 266:343-57. doi: 10.1007/BF00318190
36. Frisch B, Fleissner G, Brandes C, Hall JC. Staining in the brain of Pachymorpha sexguttata mediated by an antibody against a Drosophila clock-gene product: labeling of cells with possible importance for the beetle's circadian rhythms. Cell Tissue Res 1996; 286:411-29. PMID: 8929344
37. Bloch G, Solomon SM, Robinson GE, Fahrbach SE. Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): age- and time-related plasticity. J Comp Neurol 2003; 464:269-84. PMID: 12900924
38. Sehadová H, Sauman I, Sehnal F. Immunocytochemical distribution of pigment-dispersing hormone in the cephalic ganglia of polyneopteran insects. Cell and Tissue Research 2003; 312:113-25. PMID: 12712321
39. Weiss R, Dov A, Fahrbach SE, Bloch G. Body size-related variation in pigment dispersing factor-immunoreactivity in the brain of the bumblebee Bombus terrestris (Hymenoptera, Apidae). J Insect Physiol 2009; 55:479-87. doi: 10.1016/j.jinsphys.2009.01.016 PMID: 19232530
40. Paulk AC, Dacks AM, Gronenberg W. Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens). J Comp Neurol 2009; 513:441-56. doi: 10.1002/cne.21993 PMID: 19226517
41. Dacks AM, Christensen TA, Hildebrand JG. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 2006; 498:727-46. doi: 10.1002/cne.21076 PMID: 16927264
42. Ehmer B, Gronenberg W. Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 2002; 451:362-73. PMID: 12210130
43. Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG. Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 1986; 244:243-52. doi: 10. 1007/BF00219199 PMID: 3521878
44. Homberg U, Vitzthum H, Müller M, Binkle U. Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 1999; 409:495-507. doi: 10.1002/(SICI)1096-9861(19990705)409:3<495:: AID-CNE12>3.0.CO;2-F PMID: 10379833
45. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, et al. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 1996; 16:3154-65. PMID: 8627354
46. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, et al. Three-dimensional averageshape atlas of the honeybee brain and its applications. J Comp Neurol 2005; 492:1-19. doi: 10.1002/ cne.20644 PMID: 16175557
47. Wei H, el Jundi B, Homberg U, Stengl M. Implementation of pigment-dispersing factor-immunoreactive neurons in a standardized atlas of the brain of the cockroach Leucophaea maderae. J Comp Neurol 2010; 518:4113-33. doi: 10.1002/cne.22471 PMID: 20878779
48. Leitinger G, Pabst MA, Rind FC, Simmons PJ. Differential expression of synapsin in visual neurons of the locust Schistocerca gregaria. J Comp Neurol 2004; 480:89-100. doi: 10.1002/cne.20333 PMID: 15514920
49. Kurylas AE, Rohlfing T, Krofczik S, Jenett A, Homberg U. Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res 2008; 333:125-45. doi: 10.1007/s00441-008-0620-x PMID: 18504618
50. Godenschwege TA, Reisch D, Diegelmann S, Eberle K, Funk N, Heisenberg M, et al. Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 2004; 20:611-22. doi: 10.1111/j.1460-9568.2004.03527.x PMID: 15255973
51. Baschong W, Duerrenberger M, Mandinova A, Suetterlin R. Three-dimensional visualization of cytoskeleton by confocal laser scanning microscopy. Methods Enzymol 1999; 307:173-89. PMID: 10506974
52. Groh C, Tautz J, Rössler W. Synaptic organization in the adult honey bee brain is influenced by broodtemperature control during pupal development. Proc Nat Acad Sci 2004; 101:4268-73. PMID: 15024125
53. Groh C, Rössler W. Comparison of microglomerular structures in the mushroom body calyx of neopteran insects. Evolution of the Arthropod Nervous System: Part 2 2011; 40:358-67. doi: 10.1016/j.asd. 2010.12.002
54. Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, et al. A Systematic Nomenclature for the Insect Brain. Neuron 2014; 81:755-65. doi: 10.1016/j.neuron.2013.12.017 PMID: 24559671
55. Mota T, Yamagata N, Giurfa M, GronenbergW, Sandoz J. Neural organization and visual processing in the anterior optic tubercle of the honeybee brain. J Neurosci 2011; 31:11443-56. doi: 10.1523/ JNEUROSCI.0995-11.2011 PMID: 21832175
56. Pfeiffer K, Kinoshita M. 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 2012; 520:212-29. doi: 10.1002/cne.22776 PMID: 21953619
57. Homberg U, Hofer S, Pfeiffer K, Gebhardt S. Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 2003; 462:415-30. PMID: 12811810
58. Pfeiffer K, Kinoshita M, Homberg U. Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 2005; 94:3903-15. doi: 10.1152/jn.00276.2005 PMID: 16049147
59. Heinze S, Florman J, Asokaraj S, el Jundi B, Reppert SM. Anatomical basis of sun compass navigation II: The neuronal composition of the central complex of the monarch butterfly. J Comp Neurol 2013; 521:267-98. doi: 10.1002/cne.23214 PMID: 22886450
60. Träger U, Wagner R, Bausenwein B, Homberg U. A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 2008; 506:288-300. doi: 10.1002/ cne.21512 PMID: 18022957
61. Schäfer S, Bicker G. Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 1986; 246:287-300. doi: 10.1002/cne.902460302 PMID: 3700720
62. Homberg U, Paech A. Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 2002; 30:271-80. doi: 10.1016/S1467-8039(02)00010-5 PMID: 18088961
63. Schmitt F, Stieb SM, Wehner R, Rössler W. Experience-related reorganization of giant synapses in the lateral complex: Potential role in plasticity of the sky-compass pathway in the desert ant Cataglyphis fortis. Dev Neurobiol 2015. doi: 10.1002/dneu.22322
64. Brockmann A, Robinson GE. Central projections of sensory systems involved in honey bee dance language communication. Brain Behav Evol 2007; 70:125-36. PMID: 17519525
65. Sauman I, Briscoe AD, Zhu H, Shi D, Froy O, Stalleicken J, et al. Connecting the navigational clock to sun compass input in monarch butterfly brain. Neuron 2005; 46:457-67. PMID: 15882645
66. Vitzthum H, Müller M, Homberg U. Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 2002; 22:1114-25. PMID: 11826140
67. Strausfeld NJ, Okamura J. Visual system of calliphorid flies: organization of optic glomeruli and their lobula complex efferents. J Comp Neurol 2007; 500:166-88. doi: 10.1002/cne.21196 PMID: 17099891
68. el Jundi B, Hütteroth W, Kurylas AE, Schachtner J. Anisometric brain dimorphism revisited: Implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 2009; 517:210-25. doi: 10. 1002/cne.22150 PMID: 19731336
69. Heinze S, Reppert SM. Anatomical basis of sun compass navigation I: The general layout of the monarch butterfly brain. J Comp Neurol 2012; 520:1599-628. doi: 10.1002/cne.23054 PMID: 22473804
70. Montgomery SH, Ott SR. Brain composition in Godyris zavaleta a diurnal butterfly, Reflects an increased reliance on olfactory information. J Comp Neurol 2015; 523:869-91. doi: 10.1002/cne. 23711 PMID: 25400217
71. Mota T, Gronenberg W, Giurfa M, Sandoz J. Chromatic processing in the anterior optic tubercle of the honey bee brain. J Neurosci 2013; 33:4-16. doi: 10.1523/JNEUROSCI.1412-12.2013
72. Hertel H, Maronde U. The physiology and morphology of centrally projecting visual interneurones in the honeybee brain. J Exp Biol 1987; 133:301-15.
73. Aptekar JW, Kele MF, Lu PM, Zolotova NM, Frye MA. Neurons forming optic glomeruli compute figureground discriminations in Drosophila. J Neurosci 2015; 35:7587-99. doi: 10.1523/JNEUROSCI.0652- 15.2015 PMID: 25972183
74. Otsuna H, Shinomiya K, Ito K. Parallel neural pathways in higher visual centers of the Drosophila brain that mediate wavelength-specific behavior. Front Neural Circuits 2014; 8:8. doi: 10.3389/fncir.2014. 00008 PMID: 24574974
75. Schmeling F, Tegtmeier J, Kinoshita M, Homberg U. Photoreceptor projections and receptive fields in the dorsal rim area and main retina of the locust eye. J Comp Physiol A 2015. doi: 10.1007/s00359- 015-0990-y
76. Labhart T, Petzold J, Helbling H. Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J Exp Biol 2001; 204:2423-30. PMID: 11511657
77. Labhart T. How polarization-sensitive interneurones of crickets see the polarization pattern of the sky: a field study with an opto-electronic model neurone. J Exp Biol 1999; 202:757-70. PMID: 10069965
78. Bech M, Homberg U, Pfeiffer K. Receptive fields of locust brain neurons are matched to polarization patterns of the sky. Curr Biol 2014; 24:2124-9. doi: 10.1016/j.cub.2014.07.045 PMID: 25201687
79. Strausfeld N. Atlas of an insect brain. New York: Springer; 1976.
80. Ribi WA, Scheel M. The second and third optic ganglia of the worker bee: Golgi studies of the neuronal elements in the medulla and lobula. Cell Tissue Res 1981; 221:17-43. PMID: 7032703
81. Pfeiffer K, Negrello M, Homberg U. Conditional perception under stimulus ambiguity: polarization- and azimuth-sensitive neurons in the locust brain are inhibited by low degrees of polarization. J Neurophysiol 2011; 105:28-35. doi: 10.1152/jn.00480.2010 PMID: 20962068
82. Merlin C, Heinze S, Reppert SM. Unraveling navigational strategies in migratory insects. Curr Opin Neurobiol 2012; 22:353-61. doi: 10.1016/j.conb.2011.11.009 PMID: 22154565
83. Homberg U, Kingan TG, Hildebrand JG. Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 1987; 248:1-24. PMID: 3552234
84. Homberg U. Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 2002; 56:189-209. doi: 10.1002/jemt.10024 PMID: 11810722
85. Hamanaka Y, Kinoshita M, Homberg U, Arikawa K. Immunocytochemical localization of amines and GABA in the optic lobe of the butterfly, Papilio xuthus. PLoS One 2012; 7:e41109. doi: 10.1371/journal. pone.0041109 PMID: 22844431
86. Bülthoff H, Bülthoff I. GABA-antagonist inverts movement and object detection in flies. Brain research 1987; 407:152-8. doi: 10.1016/0006-8993(87)91230-3 PMID: 3107753
87. Warzecha AK, Egelhaaf M, Borst A. Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques. J Neurophysiol 1993; 69:329-39. PMID: 8459270