Motoneurons of the flight power muscles of the blowfly Calliphora erythrocephala: Structures and mutual dye coupling

Journal of Comparative Neurology

Volumn 500, Issue 3, 2007, Pages 448-464

  Schlurmann, M ^a   Hausen, K ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Gap junction; Indirect flight muscle; Insect; Neuroanatomy

Indexed keywords

BIOCYTIN; COBALT; FLUORESCENT DYE;

ARTICLE; CALLIPHORA ERYTHROCEPHALA; CELL INTERACTION; CELL LABELING; CELL STRUCTURE; CELLULAR DISTRIBUTION; FLIGHT MUSCLE; FLY; FORELIMB; GANGLION; GAP JUNCTION; INNERVATION; INTERNEURON; MOTONEURON; NERVE CELL NETWORK; NERVE FIBER; NEUROANATOMY; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; THORAX; ACTION POTENTIAL; ANIMAL; CELL COMMUNICATION; CELL JUNCTION; CYTOLOGY; DENDRITE; FEMALE; FLYING; HISTOLOGY; METABOLISM; PERIODICITY; PHYSIOLOGY; SKELETAL MUSCLE; ULTRASTRUCTURE;

ACTION POTENTIALS; ANIMALS; CELL COMMUNICATION; DENDRITES; DIPTERA; FEMALE; FLIGHT, ANIMAL; FLUORESCENT DYES; GANGLIA, INVERTEBRATE; GAP JUNCTIONS; INTERNEURONS; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE NET; PERIODICITY; WING;

EID: 33846980453     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21182     Document Type: Article

References (77)

1. Bacon JP, Strausfeld NJ. 1986. The dipteran "giant fibre" pathway: neurons and signals. J Comp Physiol 158:529-548.
2. Balint CN, Dickinson MH. 2004. Neuromuscular control of aerodynamic forces and moments in the blowfly, Calliphora vicina. J Exp Biol 207:3813-3838.
3. Blagburn JM, Alexopoulos H, Davies JA, Bacon JP. 1999. Null mutation in shaking-b eliminates electrical, but not chemical, synapses in the Drosophila giant fiber system: a structural study. J Comp Neurol 404:449-458.
4. Boettiger EG, Furshpan E. 1952. The mechanics of flight movements in Diptera. Biol Bull 102:200-211.
5. Chan WP, Dickinson MH. 1996a. In vivo length oscillations of indirect flight muscles in the fruit fly Drosophila virilis. J Exp Biol 199:2767-2774.
6. Chan WP, Dickinson MH. 1996b. Position-specific central projections of mechanosensory neurons on the haltere of the blowfly, Calliphora vicina. J Comp Neurol 369:405-418.
7. Coggshall JC. 1978. Neurons associated with the dorsal longitudinal flight muscles of Drosophila melanogaster. J Comp Neurol 177:707-720.
8. Consoulas C, Restifo LL, Levine RB. 2002. Dendritic remodeling and growth of motoneurons during metamorphosis of Drosophila melanogaster. J Neurosci 22:4906-4917.
9. Dickinson MH, Tu MS. 1997. The function of dipteran flight muscle. Comp Biochem Physiol A116:223-238.
10. Dickinson MH, Farman G, Frye MA, Bekyarova T, Gore D, Maughan D, Irving T. 2005. Molecular dynamics of cyclically contracting insect flight muscle in vivo. Nature 433:330-333.
11. Ennos AR. 1987. A comparative study of the flight mechanism of Diptera. J Exp Biol 127:355-373.
12. Fayyazuddin A, Dickinson MH. 1996. Haltere afferents provide direct, electrotonic input to a steering motor neuron in the blowfly, Calliphora. J Neurosci 16:5225-5232.
13. Friesen WO, Wyman RJ. 1980. Analysis of Drosophila motor neuron activity patterns with neural analogs. Biol Cybern 38:41-50.
14. Granzier HLM, Wang K. 1993. Interplay between passive tension and strong and weak cross-bridges in insect indirect flight muscle. J Gen Physiol 101:235-270.
15. Gronenberg W, Strausfeld NJ. 1992. Premotor descending neurons responding selectively to local visual stimuli in flies. J Comp Neurol 316:87-103.
16. Haag J, Borst A. 2002. Dendro-dendritic interactions between motion-sensitive large-field neurons in the fly. J Neurosci 22:3227-3233.
17. Haag J, Borst A. 2005. Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly. J Comp Physiol A191:445-454.
18. Harcombe ES, Wyman RJ. 1977. Output pattern generation by Drosophila flight motoneurons. J Neurophysiol 40:1066-1077.
19. Harcombe ES, Wyman RJ. 1978. The cyclically repetitive firing sequences of identified Drosophila flight motoneurons. J Comp Physiol A123:271-279.
20. Hausen K. 1982. Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol Cybern 45:143-156.
21. Hausen K, Strausfeld NJ. 1980. Sexually dimorphic interneuron arrangements in the fly visual system. Proc R Soc Lond B Biol Sci 208:57-71.
22. Hausen K, Wolburg-Buchholz K, Ribi WA. 1980. The synaptic organization of visual interneurons in the lobula complex of flies. A light electron microscopical study using silver-intensified cobalt-impregnations. Cell Tissue Res 208:371-387.
23. Heide G. 1971a. Die Funktion der nicht-fibrillären Flugmuskel von Calliphora. Teil I: Lage, Insertionsstellen und Innervierungsmuster der Muskeln. Zool Jb Physiol 76:87-98.
24. Heide G. 1971b. Die Funktion der nicht-fibrillären Flugmuskeln von Calliphora. II.Teil: Muskuläre Mechanismen der Flugsteuerung und ihre nervöse Kontrolle. Zool Jb Physiol 76:99-137.
25. Heide G. 1982. Neural mechanism of flight control in diptera. In: Nachtigall W, editor. Biona-Report 2. Stuttgart: Gustav Fischer, Akad. Wiss. Mainz. p 35-52.
26. Heide G, Götz KG. 1996. Optomotor control of course and altitude in Drosophila melanogaster is correlated with distinct activities of at least three pairs of flight steering muscles. J Exp Biol 199:1711-1726.
27. Homyk T Jr, Szidonya J, Suzuki DT. 1980. Behavioral mutants of Drosophila melanogaster. III. Isolation and mapping of mutations by direct visual observations of behavioral phenotypes. Mol Gen Genet 177:553-565.
28. Huang Q, Zhou D, DiFiglia M. 1992. Neurobiotin, a useful neuroanatomical tracer for in vivo anterograde, retrograde and transneuronal tract-tracing and for in vitro labeling of neurons. J Neurosci Methods 41:31-43.
29. Ikeda K, Koenig JH. 1988. Morphological identification of the motor neurons innervating the dorsal longitudinal flight muscle of Drosophila melanogaster. J Comp Neurol 273:436-444.
30. Josephson RK, Malamud JG, Stokes DR. 2000. Asynchronous muscle: a primer. J Exp Biol 203:2713-2722.
31. Kammer AE. 1985. Flying. In: Kerkut GA, Gilbert LI, editors. Comprehensive insect physiology biochemistry and pharmacology, vol 5. Oxford: Pergamon Press. p 491-552.
32. King DG, Wyman RJ. 1980. Anatomy of the giant fibre pathway in Drosophila. I. Three thoracic components of the pathway. J Neurocytol 9:753-770.
33. Koenig JH, Ikeda K. 1980a. Neural interactions controlling timing of flight muscle activity in Drosophila. J Exp Biol 87:121-136.
34. Koenig JH, Ikeda K. 1980b. Interspike interval relationship among flight muscle fibres in Drosophila. J Exp Biol 87:137-147.
35. Koenig JH, Ikeda K. 1983a. Characterization of the intracellularly recorded response of identified flight motor neurons in Drosophila. J Comp Physiol A150:295-303.
36. Koenig JH, Ikeda K. 1983b. Reciprocal excitation between identified flight motor neurons in Drosophila and its effect on pattern generation. J Comp Physiol A150:305-317.
37. Kondoh Y, Obara Y. 1982. Anatomy of motoneurones innervating mesothoracic indirect flight muscles in the silkmoth, Bombyx mori. J Exp Biol 98:23-37.
38. Kutsch W, Hug W. 1981. Dipteran flight motor pattern: invariabilities and changes during postlarval development. J Neurobiol 12:1-14.
39. Lazar G. 1978. Application of cobalt-filling technique to show retinal projections in the frog. Neuroscience 3:725-736.
40. Lillie RD. 1965. Histopathologic technique and practical histochemistry. New York: McGraw Hill.
41. Merritt DJ, Murphey RK. 1992. Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion. J Comp Neurol 322:16-34.
42. Milde JJ, Seyan HS, Strausfeld NJ. 1987. The neck motor system of the fly Calliphora erythrocephala. II. Sensory organization. J Comp Physiol A160:225-238.
43. Mills SL, Massey SC. 1995. Differential properties of two gap junctional pathways made by All amacrine cells. Nature 377:734-737.
44. Muller KJ, Scott SA. 1981. Transmission at a "direct" electrical connexion mediated by an interneuron in the leech. J Physiol 311:565-583.
45. Nachtigall W, Wilson DM. 1967. Neuro-muscular control of dipteran flight. J Exp Biol 47:77-97.
46. Nalbach G. 1989. The gear change mechanism of the blowfly (Calliphora erythrocephala) in thethered flight. J Comp Physiol A165:321-331.
47. Palka J, Lawrence PA, Hart SH. 1979. Neural projection patterns from homeotic tissue of Drosophila studied in bithorax mutants and mosaics. Dev Biol 69:549-575.
48. Phelan P. 2005. Innexins: members of an evolutionarily conserved family of gap-junction proteins. Biochim Biophys Acta 1711:225-245.
49. Phelan P, Nakagawa M, Wilkin MB, Moffat KG, O'Kane CJ, Davies JA, Bacon JP. 1996. Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. J Neurosci 16:1101-1113.
50. Pitman RM, Tweedle CD, Cohen MJ. 1972. Branching of central neurons: intracellular cobalt injection for light and electron microscopy. Science 176:412-414.
51. Power M. 1948. The thoracico-abdominal nervous system of an adult insect, Drosophila melanogaster. J Comp Neurol 88:347-409.
52. Pringle JWS. 1978. Stretch activation of muscle: function and mechanism. Proc R Soc Lond B Biol Sci 201:107-130.
53. Ribi WA. 1978. Gap junctions coupling photoreceptor axons in the first optic ganglion of the fly. Cell Tissue Res 195:299-308.
54. Schlurmann M, Hausen K. 2003. Mesothoracic ventral unpaired median (mesVUM) neurons in the blowfly Calliphora erythrocephala. J Comp Neurol 467:435-453.
55. Shimohigashi M, Meinertzhagen IA. 1998. The shaking B gene in Drosophila regulates the number of gap junctions between photoreceptor terminals in the lamina. J Neurobiol 35:105-117.
56. Sivan-Loukianova E, Eberl DF. 2005. Synaptic ultrastructure of Drosophila Johnston's organ axon terminals as revealed by an enhancer trap. J Comp Neurol 491:46-55.
57. Springer AD, Prokosch JH. 1982. Surgical and intensification procedures for defining visual pathways with cobaltous-lysine. J Histochem Cytochem 30:1235-1242.
58. Spüler M, Heide G. 1978. Simultaneous recordings of torque, thrust and muscle spikes from the fly Musca domestica during optomotor responses. Z Naturforsch 33c:455-457.
59. Squire JM. 1992. Muscle filament lattices and stretch activation: the match-mismatch model reassesses. J Muse Res Cell Motil 13:183-189.
60. Strausfeld NJ, Bacon JP. 1983. Multimodal convergence in the central nervous system of dipterous insects. In Horn E, editor. Multimodal convergence in sensory systems. Stuttgart: Gustav Fischer Verlag. p 47-76.
61. Strausfeld NJ, Bassemir UK. 1985. Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropil in Calliphora erythrocephala. Cell Tissue Res 240:617-640.
62. Strausfeld NJ, Gronenberg W. 1990. Descending neurons supplying the neck and flight motor of diptera: organization and neuroanatomical relationships with visual pathways. J Comp Neurol 302:954-972.
63. Strausfeld NJ, Obermayer M. 1976. Resolution of intraneuronal and transynaptic migration of cobalt in the insect visual and central nervous systems. J Comp Physiol A110:1-12.
64. Sun Y-A, Wyman RJ. 1997. Neurons of the Drosophila giant fiber system: I. Dorsal longitudinal motor neurons. J Comp Neurol 157-166.
65. Tanouye MA, Wyman RJ. 1980. Motor outputs of giant nerve fiber in Drosophila. J Neurophysiol 44:405-421.
66. Thomas JB, Wyman RJ. 1984. Mutations altering synaptic connectivity between identified neurons in Drosophila. J Neurosci 4:530-538.
67. 2 mutation disrupts electrical synapses in a flight circuit in adult Drosophila. J Neurosci 17:4700-4710.
68. Trimarchi JR, Schneiderman AM. 1993. Giant fiber activation of an intrinsic muscle in the mesothoracic leg of Drosophila melanogaster. J Exp Biol 177:149-167.
69. Trimarchi JR, Schneiderman AM. 1994. The motor neurons innervating the direct flight muscles of Drosophila melanogaster are morphologically specialized. J Comp Neurol 340:427-443.
70. Trimarchi JR, Schneiderman AM. 1995. Flight initiations in Drosophila melanogaster are mediated by several distinct motor patterns. J Comp Physiol A176:355-364.
71. Tyrer MN, Bell EM. 1974. The intensification of cobalt-filled neurone profiles using a modification of Timm's sulphide-silver method. Brain Res 73:151-155.
72. Veenstra RD, Wang HZ, Beyer EC, Brink PR. 1994. Selective dye and ionic permeability of gap junction channels formed by connexin45. Circ Res 75:483-490.
73. Wisser A, Nachtigall W. 1984. Functional-morphological investigations on the flight muscles and their insertion points in the blowfly Calliphora erythrocephala (Insecta, Diptera). Zoomorphology 104:188-195.
74. Wyman RJ. 1966. Multistable firing patterns among several neurons. J Neurophysiol 29:807-833.
75. Wyman RJ. 1969. Lateral inhibition in a motor output system. I. Reciprocal inhibition in dipteran flight motor system. J Neurophysiol 32:297-306.
76. Wyman RJ, Tanouye MA. 1982. Drosophila flight motor pattern: The evidence from interspike intervals. J Exp Biol 96:413-416.
77. Wyman RJ, Thomas JB, Salkoff L, Costello W. 1985. The Drosophila thorax as a model system for neurogenetics. In: Selverston AI, editor. Model neural networks and behavior. New York: Plenum Press. p 513-535.