The cephalic and pharyngeal sense organs of Calliphora vicina 3rd instar larvae are mechanosensitive but have no profound effect on ongoing feeding related motor patterns

Journal of Insect Physiology

Volumn 56, Issue 11, 2010, Pages 1530-1541

  Hückesfeld, Sebastian ^a   Niederegger, Senta ^b   Heinzel, H G ^a   Spieß, Roland ^a  

^a UNIVERSITY OF BONN   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Cephalic sense organs; Diptera larvae; Electrophysiology; Fictive feeding; Mechanosensitivity

Indexed keywords

EXPERIMENTAL STUDY; FLY; LARVA; OLFACTORY CUE; PHYSIOLOGICAL RESPONSE;

ANIMAL; ARTICLE; FEEDING BEHAVIOR; FLY; HISTOLOGY; LARVA; MECHANORECEPTOR; MOTOR ACTIVITY; PHYSIOLOGY;

ANIMALS; DIPTERA; FEEDING BEHAVIOR; LARVA; MECHANORECEPTORS; MOTOR ACTIVITY;

CALLIPHORA VICINA; DIPTERA;

EID: 77955774181     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2010.05.004     Document Type: Article

References (78)

1. Bader R., Columb J., Pankratz B., Schröck A., Stocker R., Pankratz M. Genetic dissection of neural circuit anatomy underlying feeding behavior in Drosophila: distinct classes of hugin-expressing neurons. The Journal of Comparative Neurology 2007, 502:848-856.
2. Bässler U. Sense organs in the femur of the stick insect and their relevance to the control of position of the femur-tibia-joint. Journal of Comparative Physiology A 1977, 121:99-113.
3. Bauer S., Sokolowski M. Larval foraging behavior in isofemale lines of Drosophila melanogaster and D. pseudoobscura. The Journal of Heredity 1984, 75:131-134.
4. Berrigan D., Pepin D. How maggots move: allometry and kinematics of crawling in larval diptera. Journal of Insect Physiology 1995, 41:329-337.
5. Blaesing B., Cruse H. Stick insect locomotion in a complex environment: climbing over large gaps. The Journal of Experimental Biology 2004, 207:1273-1286.
6. Bolwig N. Senses and sense organs of the anterior end of the house fly larvae. Videnskabelige Meddelelser Dansk Naturhistorisk Forening 1946, 109:81-217.
7. Burrows M. Monosynaptic connexions between wing stretch receptors and flight motorneurons of the locust. The Journal of Experimental Biology 1974, 62:189-219.
8. Campos-Ortega J., Hartenstein V. The embryonic development of Drosophila melanogaster 1985, Springer-Verlag, Heidelberg.
9. Cattaert D., Birman S. Blockade of the central generator of locomotor rhythm by noncompetitive NMDA receptor antagonists in Drosophila larvae. The Journal of Neurobiology 2001, 48:58-73.
10. Chu I., Axtell R. Fine structure of the dorsal organ of the house fly larva, Musca domestica L. Zeitschrift für Zellforschung 1971, 117:17-34.
11. Chu-Wang I., Axtell R. Fine structure of the terminal organ of the house fly larva, Musca domestica L. Zeitschrift für Zellforschung 1972, 127:287-305.
12. Chu-Wang I., Axtell R. Fine structure of the ventral organ of the house fly larva, Musca domestica L. Zeitschrift für Zellforschung 1972, 130:489-495.
13. Columb J., Grillenzoni N., Ramaekers A., Stocker R. Architecture of the primary taste center of Drosophila melanogaster larvae. The Journal of Comparative Neurology 2007, 502:834-847.
14. Decolmyn F. Neural basis of rhythmic behavior in animals. Science 1980, 210:492-498.
15. Dürr V., König Y., Kittmann R. The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern during walking. Journal of Comparative Physiology A 2001, 187:131-144.
16. Gelperin A. Investigations of a foregut receptor essential to taste threshold regulation in the blowfly. Journal of Insect Physiology 1966, 12:829-841.
17. Gelperin A. Stretch receptors in the foregut of the blowfly. Science 1967, 157:208-210.
18. Gelperin A. Abdominal sensory neurons providing negative feedback to the feeding behavior of the blowfly. Zeitschrift für vergleichende Physiologie 1971, 72:17-31.
19. Gendre N., Lüer K., Friche S., Grillenzoni N., Ramaekers A., Technau G., Stocker R. Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 2004, 131:83-92.
20. Gerber B., Scherer S., Neuser K., Michels B., Hendel T., Stocker R., Heisenberg M. Visual learning in individually assayed Drosophila larvae. The Journal of Experimental Biology 2004, 207:179-188.
21. Gerber B., Stocker R. The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chemical Senses 2007, 32:65-89.
22. Green C., Burnet B., Connolly K. Organization and pattern of inter- and intraspecific variation in the behaviour of Drosophila larvae. Animal Behaviour 1983, 31:282-291.
23. Heimbeck G., Bugnon V., Gendre N., Häberlin C., Stocker R. Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. The Journal of Neuroscience 1999, 19:6599-6609.
24. Hertweck H. Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster (Meigen.). Zeitschrift für wissenschaftliche Zoologie 1931, 139:560-663.
25. Hobson R. Studies on the nutrition of blow-fly larvae. III. The liquefaction of muscle. The Journal of Experimental Biology 1932, 9:359-365.
26. Honda I., Ishikawa Y. Electrophysiological studies on the dorsal and anterior organs of the onion fly larva. Hylemya antiqua MEIGEN (Diptera: Anthomyiidae). Applied Entomology and Zoology 1987, 22:410-416.
27. Honda I., Ishikawa Y. Ultrastructure of the larval cephalic sensory organs of the onion and seed-corn flies. Hylemya antiqua MEIGEN and H. platura MEIGEN (Diptera: Anthomyiidae). Applied Entomology and Zoology 1987, 22:325-334.
28. Jürgens G., Lehmann R., Schardin M., Nüsslein-Volhard C. Segmental organisation of the head in the embryo of Drosophila melanogaster. Roux's Archives of Developmental Biology 1986, 195:359-377.
29. Liu L., Yermolaieva O., Johnson W., Abboud F., Welsh M. Identification and function of thermosensory neurons in Drosophila larvae. Nature Neuroscience 2003, 6:267-273.
30. Lowne B. The Anatomy, Physiology, Morphology and Development of the Blow-fly (Calliphora erythrocephala) 1890, 2 vols.. R.H. Porter, London.
31. Ludwig C. Embryology and morphology of the larval head of Calliphora erythrocephala (Meigen). Microentomology 1949, 14:75-111.
32. Magazanik L., Fedorova I. Modulatory role of adenosine receptors in insect motor nerve terminals. Neurochemical Research 2003, 28:617-624.
33. Marder E. Senseless motion. Nature 2002, 416:131-132.
34. Marder E., Bucher D. Central pattern generators and the control of rhythmic movements. Current Biology 2001, 11:R986-R996.
35. Marder E., Bucher D., Schulz D., Taylor A. Invertebrate central pattern generation moves along. Current Biology 2005, 15:658-699.
36. McClellan A. Re-examination of presumed feeding motor activity in the isolated nervous system of Pleurobrachaea. Journal of Experimental Biology 1982, 98:213-228.
37. Melcher C., Bader R., Pankratz M. Amino acids, taste circuits, and feeding behavior in Drosophila: towards understanding the psychology of feeding in flies and man. Journal of Endocrinology 2007, 192:467-472.
38. Melcher C, Pankratz M. Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. Plos Biology 2005, 3:1618-1629.
39. Merritt D., Whitington P. Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position, and proneural gene function. The Journal of Neuroscience 1995, 15:1755-1767.
40. Oppliger F., Guerin P., Vlimant M. Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. Journal of Insect Physiology 2000, 56:135-144.
41. Osborne M. The sensory neurons and sensilla in the abdomen and thorax of the blowfly larva. Quarterly Journal of Microscopical Science 1963, 104:227-241.
42. Pearson K. Common principles of motor control in vertebrates and invertebrates. Annual Reviews of Neuroscience 1993, 16:265-297.
43. Pearson K. Proprioceptive regulation of locomotion. Current Opinion in Neurobiology 1995, 5:786-791.
44. Pearson K. Role of sensory feedback in the control of stance duration in walking cats. Brain Research Reviews 2008, 57:222-227.
45. Python F., Stocker R. Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low number of odorant receptor neurons. The Journal of Comparative Neurology 2002, 445:374-387.
46. Reingold S., Gelperin A. Feeding motor programme in Limax. II. Modulation by sensory input in intact animals and isolated central nervous system. The Journal of Experimental Biology 1980, 85:1-19.
47. Reye D., Pearson K. Entrainment of the locust central flight oscillator by wing stretch receptor stimulation. Journal of Comparative Physiology A 1988, 162:77-89.
48. Richter S. Unmittelbarer Kontakt der Sinneszellen cuticulärer Sinnesorgane mit der Aussenwelt. Eine Licht- und Elektronenmikroskopische Untersuchung der Chemorezeptorischen Antenntensinnesorgane der Calliphora Larven. Zeitschrift für Morphologie und Ökologie der Tiere 1962, 52:171-196.
49. Rohrbacher J. Fictive chewing activity in motor neurons and interneurons of the suboesophageal ganglion of Manduca sexta larvae. Journal of Comparative Physiology A 1994, 175:629-637.
50. Schipanski A., Yarali A., Niewalda T., Gerber B. Behavioral analyses of sugar processing in choice, feeding, and learning in larval Drosophila. Chemical Senses 2008, 33:563-573.
51. Schmidt-Ott U., Gonzalez-Gaitan M., Jäckle H., Technau G.M. Number, identity, and sequence of the Drosophila head segments a revealed by neural elements and their deletion patterns in mutants. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:8363-8367.
52. Schoofs A., Niederegger S., Ooyen A.V, Heinzel H.-G., Spieß R. The brain can eat: establishing the existence of a central pattern generator for feeding in third instar larvae of Drosophila virilis and Drosophila melanogaster. Journal of Insect Physiology 2010, 56:695-705.
53. Schoofs A., Niederegger S., Spieß R. From behavior to fictive feeding: anatomy, innervation and activation pattern of pharyngeal muscles of Calliphora vicina 3rd instar larvae. Journal of Insect Physiology 2009, 55:218-230.
54. Schoofs A., Spieß R. Anatomical and functional characterisation of the stomatogastric nervous system of blowfly (Calliphora vicina) larvae. Journal of Insect Physiology 2007, 53:349-360.
55. Schrader S., Merritt D. Dorsal longitudinal stretch receptor of Drosophila melanogaster larva-fine structure and maturation. Arthropod Structure and Development 2007, 36:157-169.
56. Schrader S., Merritt D. Central projections of Drosophila sensory neurons in the transition from embryo to larva. The Journal of Comparative Neurology 2000, 425:34-44.
57. Seath I. The effects of increasing mandibular load on electrical activity in the mandibular closer muscles during feeding in the desert locust, Schistocerca gregaria. Physiological Entomology 1977, 2:237-240.
58. Seath I. Sensory feedback in the control of mouthpart movements in the desert locust Schistocerca gregaria. Physiological Entomology 1977, 2:147-156.
59. Shepherd D., Smith S. Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila. Development 1996, 122:23752384.
60. Shetreat-Klein A., Cropper E. Afferent induced changes in rhythmic motor programs in the feeding circuitry of Aplysia. Journal of Neurophysiology 2004, 92:2312-2322.
61. Singh R., Singh K. Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). International Journal of Insect Morphology and Embryology 1984, 13:255-273.
62. Smarandache C., Daur N., Hedrich U., Stein W. Regulation of motor pattern frequency by reversals in proprioceptive feedback. European Journal of Neuroscience 2008, 28:460-474.
63. Smarandache C., Stein W. Sensory-induced modification of two motor patterns in the crab, Cancer pagurus. The Journal of Experimental Biology 2007, 210:2912-2922.
64. Sokolowski M. Drosophila larval foraging behaviour: digging. Animal Behaviour 1982, 30:1252-1261.
65. Song W., Onishi M., Jan L.Y., Jan Y.N. Peripheral multidentricic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:5199-5204.
66. Stocker R. The organisation of the chemosensory system in Drosophila melanogaster: a review. Cell and Tissue Research 1994, 275:3-26.
67. Stocker R. Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microscopy Research and Technique 2001, 55:284-296.
68. Suster M., Bate M. Embryonic assembly of a central pattern generator without sensory input. Nature 2002, 416:174-178.
69. Szpila K., Pape T., Rusinek A. Morphology of the first instar of Calliphora vicina. Phormia regina and Lucilia illustris (Diptera Calliphoridae). Medical and Veterinary Entomology 2008, 22:16-25.
70. Vosshall L., Stocker R. Molecular architecture of smell and taste in Drosophila. The Annual Review of Neuroscience 2007, 30:505-533.
71. Wanischeck M., Rose U. Unusual tension receptors in insects. Journal of Neurobiology 2005, 65:115-124.
72. Wendler G. The influence of proprioceptive feedback on locust flight co-ordination. The Journal of Comparative Physiology 1974, 88:173-200.
73. Wilson D. Proprioceptive leg reflexes in cockroaches. The Journal of Experimental Biology 1965, 43:397-409.
74. Wilson D. Insect walking. Annual Reviews of Entomology 1966, 11:103-122.
75. Wolf H. The locust tegula: significance for flight rhythm generation, wing movement control and aerodynamic force production. The Journal of Experimental Biology 1993, 182:229-253.
76. Wong R., Pearson K. Properties of the trochanteral hair plate and its function in the control of walking in the cockroach. The Journal of Experimental Biology 1976, 64:233-249.
77. Yamada Y., Ishikawa Y., Ikeshoji T., Matsumoto Y. Cephalic sensory organs of the onion fly larva. Hylemya antiqua MEIGEN (Diptera: Anthomyiidae) responsible for host plant finding. Applied Entomology and Zoology 1981, 16:121-128.
78. Zinke I., Kirchner C., Chao L., Tetzlaff M., Pankratz M. Suppression of food intake and growth by amino acids in Drosophila: the role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. Development 1999, 126:5275-5284.