DOI: 10.1242/dev.122.8.2375. Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of <i>Drosophila</i>

Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila

10.1242/dev.122.8.2375

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

ABSTRACT We have used a GAL4 enhancer-trap line driving the expression of a lacZ construct to examine the reorganisation of an identified group of proprioceptive sensory neurons during metamorphosis in Drosophila. The results show that whilst most larval sensory neurons degenerate during the first 24 hours of metamorphosis a segmentally repeated array of 6 neurons per segment persists into the adult stages to become functional adult neurons. These sensory neurons retain their axonal projections in the central nervous system intact and unchanged throughout. The adult sensory neuron axons enter the central nervous system at around 44 hours after puparium formation. Most of these axons grow along the pathways defined by the persistent larval sensory axons. The ordering of the adult sensory projections is, therefore, established upon the larval pattern of projections. The possibility that the larval neurons act as guidance cues for organising the ordered arrays of sensory neurons is discussed.

Bibliography

Shepherd, D., & Smith, S. A. (1996). Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila. Development, 122(8), 2375â2384.

Authors 2

David Shepherd (first)
Simon A. Smith (additional)

References 33 Referenced 41

10.1242/jeb.59.1.121 / J. Exp. Biol / The mechanism of the pupal gin trap III. Interneurons and the origin of the closure mechanism by Bate (1973)
{'key': '2025021323061211400_DEVELOP_122_8_2375C2', 'first-page': '54', 'article-title': 'Pioneer neurons in an insects embryo. Nature (Lond', 'volume': '260', 'author': 'Bate', 'year': '1976'} / Pioneer neurons in an insects embryo. Nature (Lond by Bate (1976)
{'key': '2025021323061211400_DEVELOP_122_8_2375C3', 'first-page': '1', 'volume-title': 'Handbook of Sensory Physiology, Vol 9', 'author': 'Bate', 'year': '1978'} / Handbook of Sensory Physiology, Vol 9 by Bate (1978)
10.1002/cne.902550407 / J. Comp. Neurol / Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis by Booker (1987)
10.1523/JNEUROSCI.07-12-04107.1987 / J. Neurosci / Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. II. Hormonal control of imaginal nest cell degeneration and differentiation during metamorphosis by Booker (1987)
10.1242/dev.118.2.401 / Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes by Brand (1993)
10.1007/BF00571440 / Cell Tissue Res / Metamorphic changes in the central projections of hair sensilla in Tenebrio molitor L. (Insecta: Coleoptera by Breidbach (1990)
{'key': '2025021323061211400_DEVELOP_122_8_2375C8', 'first-page': '499', 'volume-title': 'The Genetics and Biology of Drosophila 2b', 'author': 'Crossley', 'year': '1978'} / The Genetics and Biology of Drosophila 2b by Crossley (1978)
10.1242/dev.113.1.91 / Development / The development of adult abdominal muscles in Drosophila: myoblasts express twist and are associated with nerves by Currie (1991)
10.1016/0012-1606(83)90314-7 / Dev. Biol / Embryogenesis of peripheral nerve pathways in grasshopper legs. I. The initial nerve pathway to the CNS by Keshishian (1983)
10.1016/0012-1606(83)90316-0 / Dev. Biol / Embryogenesis of peripheral nerve pathways in grasshopper legs. III. Development without pioneer neurons by Keshishian (1983)
10.1002/cne.903080206 / J. Comp. Neurol / 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 by Lakes-Harlan (1991)
10.1002/cne.903080207 / J. Comp. Neurol / 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 by Lakes-Harlan (1991)
10.1007/BF00611089 / J. Comp. Physiol. A / The structure, function, and metamorphic reorganisation of somatotopically projecting sensory neurons in Manduca sexta larvae by Levine (1985)
10.1038/299250a0 / Nature / Metamorphosis of the insect nervous system: Changes in the morphology and synaptic interactions of identified cells by Levine (1982)
10.1523/JNEUROSCI.05-09-02424.1985 / J. Neurosci / Dendritic reorganisation of abdominal motoneurons during metamorphosis of the moth, Manduca sexta by Levine (1985)
10.1002/cne.903220103 / J. Comp. Neurol / Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion by Merritt (1992)
10.1523/JNEUROSCI.15-03-01755.1995 / J. Neurosci / Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, soma position and proneural gene function by Merritt (1995)
10.1002/cne.902900203 / J. Comp. Neurol / Modality specific axon projections in the CNS of the flies Phormia and Drosophila by Murphey (1989)
10.1242/dev.111.1.79 / Development / The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster by Prokop (1991)
10.1523/JNEUROSCI.03-01-00020.1983 / J. Neurosci / Pathfinding by neuronal growth cones in grasshopper embryos. I. Divergent choices made by the growth cones of sibling neurons by Raper (1983)
10.1523/JNEUROSCI.03-01-00031.1983 / J. Neurosci / Pathfinding by neuronal growth cones in grasshopper embryos. II.Selective fasciculation onto specific axonal pathways by Raper (1983)
10.1101/SQB.1983.048.01.063 / Cold Spring Harbor Symp. Quant. Biol / Guidance of neuronal growth cones: selective fasciculation in the grasshopper embryo by Raper (1983)
10.1002/(SICI)1096-9861(19960108)364:2<311::AID-CNE9>3.0.CO;2-8 / J. Comp. Neurol / The central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique by Smith (1996)
10.1016/0092-8674(87)90180-2 / Cell / disconnected: A locus required for neuronal pathway formation in the visual system of Drosophila by Steller (1987)
10.1242/dev.107.4.855 / Development / Preexisting neuronal pathways in the leg imaginal discs of Drosophila by Tix (1989)
10.1242/dev.105.4.739 / Development / Preexisting neuronal pathways in the developing optic lobes of Drosophila by Tix (1989)
10.1002/cne.902160410 / J. Comp. Neurol / Programmed cell death in the nervous system of an adult insect by Truman (1983)
10.1002/neu.480231005 / J. Neurobiol / Developmental neuroethology of insect metamorphosis by Truman (1992)
10.1016/0012-1606(88)90067-X / Dev. Biol / Spatial and temporal patterns of neurogenesis in the CNS of Drosophila melanogaster by Truman (1988)
10.1126/science.1257782 / Science / Dendritic reorganisation of an identified motoneuron during metamorphosis of the tobacco hornworm moth by Truman (1976)
10.1002/neu.480260204 / J. Neurobiol / Development of wing sensory axons in the central nervous system of Drosophila during metamorphosis by Whitlock (1995)
10.1016/0896-6273(95)90063-2 / Neuron / Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns by Yang (1995)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 10:47 p.m.)
Deposited	6 months, 2 weeks ago (Feb. 13, 2025, 6:06 p.m.)
Indexed	6 months, 2 weeks ago (Feb. 14, 2025, 12:32 a.m.)
Issued	29 years, 1 month ago (Aug. 1, 1996)
Published	29 years, 1 month ago (Aug. 1, 1996)
Published Online	29 years, 1 month ago (Aug. 1, 1996)
Published Print	29 years, 1 month ago (Aug. 1, 1996)

Funders 0

None

BibTeX

@article{Shepherd_1996, title={Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila}, volume={122}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.122.8.2375}, DOI={10.1242/dev.122.8.2375}, number={8}, journal={Development}, publisher={The Company of Biologists}, author={Shepherd, David and Smith, Simon A.}, year={1996}, month=aug, pages={2375–2384} }

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