Research article

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

Kohei Shimono^1* , Azusa Fujimoto^1* , Taiichi Tsuyama¹ , Misato Yamamoto-Kochi¹ , Motohiko Sato^1,2 , Yukako Hattori¹ , Kaoru Sugimura^1,3 , Tadao Usui¹ , Ken-ichi Kimura⁴ and Tadashi Uemura¹

¹  Laboratory of Cell Recognition and Pattern Formation, Graduate School of Biostudies, South Campus Research Building (Building G), Kyoto University, Yoshida Konoe-cho, Sakyo-ku, Kyoto 606-8507, Japan

²  Laboratory of Neural Development, Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan

³  Laboratory of Cell Function Dynamics, Advanced Technology Development Group, Brain Science Institute, RIKEN, Wako 351-0198, Japan

⁴  Hokkaido University of Education, Sapporo Campus, Sapporo 002-8502, Japan

author email corresponding author email* Contributed equally

Neural Development 2009, 4:37doi:10.1186/1749-8104-4-37

Published:	2 October 2009

Abstract

Background

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 Drosophila 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.

Results

We identified multidendritic neurons in the adult Drosophila 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.

Conclusion

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.