Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death

<p>Abstract</p> <p>Background</p> <p>For the establishment of functional neural circuits that support a wide range of animal behaviors, initial circuits formed in early development have to be reorganized. One way to achieve this is local remodeling of the circuitry hard...

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Main Authors: Sugimura Kaoru, Hattori Yukako, Sato Motohiko, Yamamoto-Kochi Misato, Tsuyama Taiichi, Fujimoto Azusa, Shimono Kohei, Usui Tadao, Kimura Ken-ichi, Uemura Tadashi
Format: Article
Language:English
Published: BMC 2009-10-01
Series:Neural Development
Online Access:http://www.neuraldevelopment.com/content/4/1/37
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author Sugimura Kaoru
Hattori Yukako
Sato Motohiko
Yamamoto-Kochi Misato
Tsuyama Taiichi
Fujimoto Azusa
Shimono Kohei
Usui Tadao
Kimura Ken-ichi
Uemura Tadashi
author_facet Sugimura Kaoru
Hattori Yukako
Sato Motohiko
Yamamoto-Kochi Misato
Tsuyama Taiichi
Fujimoto Azusa
Shimono Kohei
Usui Tadao
Kimura Ken-ichi
Uemura Tadashi
author_sort Sugimura Kaoru
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>For the establishment of functional neural circuits that support a wide range of animal behaviors, initial circuits formed in early development have to be reorganized. One way to achieve this is local remodeling of the circuitry hardwiring. To genetically investigate the underlying mechanisms of this remodeling, one model system employs a major group of <it>Drosophila </it>multidendritic sensory neurons - the dendritic arborization (da) neurons - which exhibit dramatic dendritic pruning and subsequent growth during metamorphosis. The 15 da neurons are identified in each larval abdominal hemisegment and are classified into four categories - classes I to IV - in order of increasing size of their receptive fields and/or arbor complexity at the mature larval stage. Our knowledge regarding the anatomy and developmental basis of adult da neurons is still fragmentary.</p> <p>Results</p> <p>We identified multidendritic neurons in the adult <it>Drosophila </it>abdomen, visualized the dendritic arbors of the individual neurons, and traced the origins of those cells back to the larval stage. There were six da neurons in abdominal hemisegment 3 or 4 (A3/4) of the pharate adult and the adult just after eclosion, five of which were persistent larval da neurons. We quantitatively analyzed dendritic arbors of three of the six adult neurons and examined expression in the pharate adult of key transcription factors that result in the larval class-selective dendritic morphologies. The 'baseline design' of A3/4 in the adult was further modified in a segment-dependent and age-dependent manner. One of our notable findings is that a larval class I neuron, ddaE, completed dendritic remodeling in A2 to A4 and then underwent caspase-dependent cell death within 1 week after eclosion, while homologous neurons in A5 and in more posterior segments degenerated at pupal stages. Another finding is that the dendritic arbor of a class IV neuron, v'ada, was immediately reshaped during post-eclosion growth. It exhibited prominent radial-to-lattice transformation in 1-day-old adults, and the resultant lattice-shaped arbor persisted throughout adult life.</p> <p>Conclusion</p> <p>Our study provides the basis on which we can investigate the genetic programs controlling dendritic remodeling and programmed cell death of adult neurons, and the life-long maintenance of dendritic arbors.</p>
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spelling doaj.art-19d5c784f5664193948cad92c01030742022-12-22T01:37:56ZengBMCNeural Development1749-81042009-10-01413710.1186/1749-8104-4-37Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell deathSugimura KaoruHattori YukakoSato MotohikoYamamoto-Kochi MisatoTsuyama TaiichiFujimoto AzusaShimono KoheiUsui TadaoKimura Ken-ichiUemura Tadashi<p>Abstract</p> <p>Background</p> <p>For the establishment of functional neural circuits that support a wide range of animal behaviors, initial circuits formed in early development have to be reorganized. One way to achieve this is local remodeling of the circuitry hardwiring. To genetically investigate the underlying mechanisms of this remodeling, one model system employs a major group of <it>Drosophila </it>multidendritic sensory neurons - the dendritic arborization (da) neurons - which exhibit dramatic dendritic pruning and subsequent growth during metamorphosis. The 15 da neurons are identified in each larval abdominal hemisegment and are classified into four categories - classes I to IV - in order of increasing size of their receptive fields and/or arbor complexity at the mature larval stage. Our knowledge regarding the anatomy and developmental basis of adult da neurons is still fragmentary.</p> <p>Results</p> <p>We identified multidendritic neurons in the adult <it>Drosophila </it>abdomen, visualized the dendritic arbors of the individual neurons, and traced the origins of those cells back to the larval stage. There were six da neurons in abdominal hemisegment 3 or 4 (A3/4) of the pharate adult and the adult just after eclosion, five of which were persistent larval da neurons. We quantitatively analyzed dendritic arbors of three of the six adult neurons and examined expression in the pharate adult of key transcription factors that result in the larval class-selective dendritic morphologies. The 'baseline design' of A3/4 in the adult was further modified in a segment-dependent and age-dependent manner. One of our notable findings is that a larval class I neuron, ddaE, completed dendritic remodeling in A2 to A4 and then underwent caspase-dependent cell death within 1 week after eclosion, while homologous neurons in A5 and in more posterior segments degenerated at pupal stages. Another finding is that the dendritic arbor of a class IV neuron, v'ada, was immediately reshaped during post-eclosion growth. It exhibited prominent radial-to-lattice transformation in 1-day-old adults, and the resultant lattice-shaped arbor persisted throughout adult life.</p> <p>Conclusion</p> <p>Our study provides the basis on which we can investigate the genetic programs controlling dendritic remodeling and programmed cell death of adult neurons, and the life-long maintenance of dendritic arbors.</p>http://www.neuraldevelopment.com/content/4/1/37
spellingShingle Sugimura Kaoru
Hattori Yukako
Sato Motohiko
Yamamoto-Kochi Misato
Tsuyama Taiichi
Fujimoto Azusa
Shimono Kohei
Usui Tadao
Kimura Ken-ichi
Uemura Tadashi
Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death
Neural Development
title Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death
title_full Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death
title_fullStr Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death
title_full_unstemmed Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death
title_short Multidendritic sensory neurons in the adult <it>Drosophila </it>abdomen: origins, dendritic morphology, and segment- and age-dependent programmed cell death
title_sort multidendritic sensory neurons in the adult it drosophila it abdomen origins dendritic morphology and segment and age dependent programmed cell death
url http://www.neuraldevelopment.com/content/4/1/37
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