Remodeling of the leg sensory system during metamorphosis of the hawkmoth, Manduca sexta

Journal of Comparative Neurology

Volumn 419, Issue 2, 2000, Pages 154-174

  Consoulas, Christos ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Axon guidance; Development; Navigation; Sensory neuron

Indexed keywords

BIOCYTIN; BROXURIDINE; CARBOCYANINE;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CHEMICAL LABELING; CONFOCAL MICROSCOPY; LARVA; LEG; LEPIDOPTERA; METAMORPHOSIS; NERVE FIBER TRANSPORT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SENSORY SYSTEM; SENSORY SYSTEM ELECTROPHYSIOLOGY;

AGING; ANIMALS; AXONS; LARVA; LEG; MANDUCA; METAMORPHOSIS, BIOLOGICAL; NERVOUS SYSTEM; NEURONS, AFFERENT; SENSE ORGANS;

EID: 0034094678     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000403)419:2<154::AID-CNE2>3.0.CO;2-A     Document Type: Article

References (88)

1. Bate CM. 1973. The mechanism of the pupal gin trap. III. Interneurons and the origin of the closure mechanism. J Exp Biol 59:121-135.
2. Bate CM. 1976. Pioneer neurons in an insect embryo. Nature (London) 260:54-56.
3. Bate CM. 1978. Development of sensory systems. In: Jacobsen M, editor: Handbook of sensory physiology, vol IX. New York: Springer-Verlag. p 1-53.
4. Bell RA, Joachim FA. 1976. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entymol Soc Am 69:365-373.
5. Bollenbacher WE, Smith SL, Goodman W, Gilbert LI. 1981. Ecdysteroid titer during the larval-pupal-adult development of the tobacco hornworm, Manduca sexta. Gen Comp Endocrinol 44:302-306.
6. Booker R, Truman JW. 1987. Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis. J Comp Neurol 255:548-559.
7. Breidbach O. 1987a. Constancy of ascending projections in the metamorphosing brain of the meal-beetle Tenebrio molitor L. (Insecta, Coleoptera). Rouxs Arch Dev Biol 196:450-459.
8. Breidbach O. 1987b. The fate of persisting thoracic neurons during metamorphosis of the meal beetle Tenebrio molitor (Insecta, Coleoptera). Rouxs Arch Dev Biol 196:93-100.
9. Breidbach O. 1990. Metamorphic changes in the central projections of hair sensilla in Tenebrio molitor L. (Insecta: Coleoptera). Cell Tissue Res 259:159-176.
10. Campos-Ortega JA, Hartenstein V. 1985. The embryonic development of Drosophila melanogaster. Berlin: Springer-Verlag.
11. Casaday GB, Camhi JM. 1976. Metamorphosis of flight motor neurons in the moth Manduca sexta. J Comp Physiol 112:143-158.
12. Consoulas C, Levine RB. 1997. Accumulation and proliferation of adult leg muscle precursors in Manduca are dependent on innervation. J Neurobiol 32:531-553.
13. Consoulas C, Levine RB. 1998a. Presynaptic function during muscle remodeling in insect metamorphosis. J Neurosci 18:5817-5831.
14. Consoulas C, Levine RB. 1998b. Remodeling of the leg sensory system during metamorphosis of Manduca sexta. Soc Neurosci Abstr 63:155.
15. Consoulas C, Kent KS, Levine RB. 1996. Remodeling of the peripheral processes and presynaptic terminals of leg motoneurons during metamorphosis of the hawkmoth, Manduca sexta. J Comp Neurol 372:415-434.
16. Consoulas C, Anezaki M, Levine RB. 1997. Development of adult thoracic leg muscles during metamorphosis of the hawkmoth Manduca sexta. Cell Tissue Res 287:383-412.
17. Dodd J, Morton SB, Karagogeous D, Yamamoto M, Jessell TM. 1988. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1:105-116.
18. Dominick OS, Truman JW. 1986. The physiology of wandering behaviour in Manduca sexto. III. Organization of wandering behaviour in the larval nervous system. J Exp Biol 121:115-132.
19. Eaton JL. 1974. Nervous system of the head and thorax of the adult tobacco hornworm, Manduca sexta (Lepidoptera: Sphingidae). Int J Insect Morphol Embryol 3:47-66.
20. Eisen JS, Myers PZ, Westerfield M. 1986. Pathway selection by growth cones of identified motoneurones in live zebra fish embryos. Nature 320:269-271.
21. Fahrbach SE, Schwartz LM. 1994. Localization of immunoreactiveubiquitin in the nervous system of the Manduca sexta moth. J Comp Neurol 1994:343:464-482.
22. Fahrbach SE, Truman JW. 1987. Possible interactions of a steroid hormone and neural inputs in controlling the death of an identified neuron in the moth Manduca sexta. J Neurobiol 18:497-508.
23. Fahrbach SE, Choi MK, Truman JW. 1994. Inhibitory effects of actinomycin D and cycloheximide on neuronal death in adult Manduca sexta. J Neurobiol 25:59-69.
24. Gan WB, Macagno ER. 1995. Developing neurons use a putative pioneer's peripheral arbor to establish their terminal fields. J Neurosci 15:3254-3262.
25. Ghosh A, Antonini A, McConnell SK, Shatz CJ. 1990. Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347:179-181.
26. Ghysen A, Dambly-Chaudiére C, Aceves E, Jan LY, Jan YN. 1986. Sensory neurons and peripheral pathways in Drosophila embryos. Rouxs Arch Dev Biol 195:281-289.
27. Hoffman KL, Weeks JC. 1998. Programmed cell death of an identified motoneuron in vitro: temporal requirements for steroid exposure and protein synthesis. J Neurobiol 35:300-322.
28. Horikawa K, Armstrong WF. 1988. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:1-12.
29. Jacobs GA, Weeks JC. 1990. Postsynaptic changes at a sensory-to-motoneuron synapse contribute to the developmental loss of a reflex behavior during insect metamorphosis. J Neurosci 10:1341-1356.
30. Jan YN, Chysen A, Christoph I, Barbel S, Yan LY. 1985. Formation of neuronal pathways in the imaginal discs of Drosophila melanogaster. J Neurosci 5:2453-2464.
31. Jellies J, Johansen KM, Johansen J. 1995. Peripheral neurons depend on CNS-derived guidance cues for proper navigation during leech development. Dev Biol 171:471-482.
32. Johnston RM, Levine RB. 1996. Locomotory behavior in the hawkmoth Manduca sexta: kinematic and electromyographical analysis of the thoracic legs in larvae and adult. J Exp Biol 199:759-774.
33. Kent KS, Griffin LM. 1990. Sensory organs of the thoracic legs of the moth Manduca sexta. Cell Tissue Res 259:209-223.
34. Kent KS, Levine RB. 1988. Neural control of leg movements in a metamorphic insect: persistence of larval leg motor neurons to innervate the adult legs of Manduca sexta. J Comp Neurol 276:30-43.
35. Kent KS, Levine RB. 1993. Debdritic reorganization of an identified neuron during metamorphosis of the moth Manduca sexta: the influence of interactions with the periphery. J Neurobiol 24:1-22.
36. Kent KS, Consoulas C, Duncan C, Johnston RM, Luedeman R, Levine RB. 1995. Remodeling of neuromuscular systems during insect metamorphosis. Am Zool 35:578-584.
37. Kent KS, Fjeld CC, Anderson R. 1996. Leg proprioceptors of the tobacco hornworm, Manduca sexta: organization of central projections at larval and adult stages. Microsc Res Tech 35:265-284.
38. Keshishian H, Bentley D. 1983a. Embryogenesis of peripheral nerve pathways in grasshopper legs. I. The initial nerve pathway to the CNS. Dev Biol 96:89-102.
39. Keshishian H, Bentley D. 1983b. Embryogenesis of peripheral nerve pathways in grasshopper legs. II. Development without pioneer neurons. Dev Biol 96:116-124.
40. Kim CW. 1959. The differentiation centre inducing the development from larval to adult leg in Pieris brassicae (Lepidoptera). J Embryol Exp Morphol 7:572-584.
41. Kimura K, Truman JW. 1990. Postmetamorphic cell death in the nervous and muscular systems of Drosophila melanogaster. J Neurosci 10:403-411.
42. Kuwada JY. 1986. Cell recognition by neuronal growth cones in a simple vertebrate embryo. Science 233:740-746.
43. Lakes-Harlan R, Pollack GS, Merrit DJ. 1991a. From embryo to adult: anatomy and development of a leg sensory organ in Phormia regina, Meigen (Insecta: Diptera). I. Anatomy and physiology of a larval "leg" sensory organ. J Comp Neurol 308:188-199.
44. Lakes-Harlan R, Pollack GS, Merrit DJ. 1991b. From embryo to adult: anatomy and development of a leg sensory organ in Phormia regina, Meigen (Insecta: Diptera). II. Development and persistence of sensory neurons. J Comp Neurol 308:200-208.
45. Levine RB. 1989. Expansion of the central arborization of persistent sen" sory neurons during insect metamorphosis: the role of the steroid hormone, 20-hydroxyecdysone. J Neurosci 9:1045-1054.
46. Levine RB, Truman JW. 1982. Metamorphosis of the insect nervous sys" tem: changes in morphology and synaptic interactions of identified neurons. Nature 299:250-252.
47. Levine RB, Truman JW. 1985. Dendritic reorganization of abdominal motoneurons during metamorphosis of the moth Manduca sexta. J Neurosci 5:2424-2431.
48. Levine RB, Pac C, Linn D. 1985. The structure, function and metamorphic reorganization of somatotopically projecting sensory neurons in Manduca sexta larvae. J Comp Physiol 157:1-13.
49. Levine RB, Truman JW, Linn D, Bate CM. 1986. Endocrine regulation of the form and function of axonal arbors during insect metamorphosis. J Neurosci 6:293-299.
50. Levine RB, Morton DB, Restifo LL. 1995. Remodeling of the insect nervous system. Curr Opin Neurobiol 5:28-35.
51. Lewis FP, Fullard JH. 1996. Neurometamorphosis of the ear in the gypsy moth, Lymantria dispar, and its homologue in the earless forest tent caterpillar moth, Malacosoma disstria. J Neurobiol 31:245-262.
52. LoPresti V, Macagno ER, Levinthal C. 1973. Structure and development of neuronal connections in isogenic organisms: cellular interactions in the development of the optic lamina of Daphnia. Proc Natl Acad Sci USA 70:433-437.
53. McConnell SK, Ghosh A, Shatz CJ. 1994. Subplate pioneers and the formation of descending connections from cerebral cortex. J Neurosci 4:1892-1897.
54. Miles CI, Booker R. 1993. Octopod, a homeotic mutation of the moth Manduca sexta, affects development of both mesodermal and ectodermal structures. Dev Biol 155:147-160.
55. Nijhout HF, Williams CM. 1974. Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. J Exp Biol 61:481-491.
56. Paspalas C, Consoulas C, Theophilidis G. 1993. The fate of specific motoneurons and sensory neurons of the pregenital abdominal segments in Tenebrio molitor (Insecta: Coleoptera) during metamorphosis. Rouxs Arch Dev Biol 202:204-213.
57. Peinado A, Zipser B, Macagno ER. 1990. Segregation of afferent projections in the central nervous system of the leech Hirudo medicinalis. J Comp Neurol 301:232-242.
58. Prokop A, Technau GM. 1991. The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111:79-88.
59. Raper JA, Bastiani MJ, Goodman CS. 1983. Pathfinding by neuronal growth cones in grasshopper embryos. II. Selective fasciculation onto specific axonal pathways. J Neurosci 3:31-41.
60. Reinecke JP, Buckner JS, Grugel SR. 1980. Life cycle of laboratory-reared tobacco hornworms, Manduca sexta, a study of development and behavior using time-lapse cinematography. Biol Bull 158:129-140.
61. Robinow S, Talbot WS, Hogness DS, Truman JW. 1993. Programmed cell death in the Drosophila CNS is ecdysone-regulated and coupled with specific receptor isoform. Development 119:1251-1259.
62. Sandstorm DJ, Weeks JC. 1991. Reidentification of larval interneurons in the pupal stage of the tobacco hornworm Manduca sexta. J Comp Neurol 308:311-327.
63. Sanes JR, Hildebrand JG. 1976. Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51:300-319.
64. Shepherd D, Smith SA. 1996. Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila. Development 122:2375-2384.
65. Smith SA, Shepherd D. 1996. Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique. J Comp Neurol 364:311-323.
66. Stanier DYR, Gilbert W. 1990. Pioneer neurons in the mouse trigeminal system. Proc Natl Acad Sci USA 87:923-927.
67. Steller H, Fischbach K-F, Rubin GM. 1987. Disconnected: a locus required for neuronal pathway formation in the visual system of Drosophila. Cell 50:1139-1153.
68. Streichelt LC, Pierce JT, Nelson JA, Weeks JC. 1997. Steroid hormones act directly to trigger segment-specific programmed cell death of identified motoneurons in vitro. Dev Biol 183:95-107.
69. Sun XJ, Tolbert LP, Hildebrand JG. 1993. Ramification pattern and ultrastructural characteristics of the serotonin-immunoreactive neuron in the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 338:5-16.
70. Tamarkin DA, Levine RB. 1996. Synaptic interactions between a muscle-associated proprioceptor and body wall muscle motor neurons in larval and adult Manduca sexta. J Neurophysiol 76:1597-1610.
71. Technau G, Heisenberg M. 1982. Neural reorganization during metamorphosis of the corpora pedinculata in Drosophila melanogaster. Nature 295:405-407.
72. Theophilidis G, Buens MD. 1979. Muscle tension receptor in the locust leg. J Comp Physiol 131:247-254.
73. Thorn RS, Truman JW. 1989. Sex-specific neuronal respecification of the genital segments of the tobacco hornworm moth Manduca sexta. J Comp Neurol 284:489-503.
74. Tix S, Minten JS, Technau GM. 1989a. Pre-existing neuronal pathways in the developing optic lobes of Drosophila. Development 105:739-746.
75. Tix S, Bate M, Technau GM. 1989b. Pre-existing neuronal pathways in the leg imaginai discs of Drosophila. Development 107:855-862.
76. Tolbert LP, Matsumoto SG, Hildebrand JG. 1983. Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3:1158-1175.
77. Trimmer BA, Weeks JC. 1993. Muscarinic acetylcholine receptors modulate the excitability of an identified insect motoneuron. J Neurophysiol 69:1821-1836.
78. Truman JW. 1983. Programmed cell death in the nervous system of an adult insect. J Comp Neurol 216:445-452.
79. Truman JW, Bate M. 1988. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125:145-157.
80. Truman JW, Reiss SE. 1976. Dendritic reorganization of an identified motoneuron during metamorphosis of the tobacco horn-worm, Manduca sexta. Science 192:477-479.
81. Truman JW, Schwartz LM. 1984. Steroid regulation of neuronal death in the moth nervous system. J Neurosci 4:274-280.
82. Truman JW, Taghert PH, Reynolds SE. 1980. Physiology of pupal ecdysis in the tobacco hornworm, Manduca sexta. I. Evidence for control by eclosion hormone. J Exp Biol 88:327-337.
83. Truman JW, Thorn RS, Robinow S. 1992. Programmed neuronal death in insect development. J Neurobiol 1992:1295-1311.
84. Waldrop B, Levine RB. 1989. Development of the gin trap reflex in Manduca sexta: a comparison of larval and pupal motor responses. J Comp Physiol 165:743-753.
85. Waldrop B, Levine RB. 1992. Intersegmental interneurons serving larval and pupal mechanosensory reflexes in the moth Manduca sexta. J Comp Physiol 171:195-205.
86. Weeks JC, Truman JW. 1985. Independent steroid control of the fates of motoneurons and their muscles during metamorphosis. J Neurosci 5:2290-2300.
87. Weeks JC, Davidson SK, Debu BH. 1993. Effects of a protein synthesis inhibitor on the hormonally mediated regression and death of motoneurons in the tobacco hornworm, Manduca sexta. J Neurobiol 24:125-140.
88. Wigglesworth VB. 1953. Origin of sensory neurons in an insect Rhodnius prolixus (Hemiptera). Quart J Microsc Soc 94:93-112.