Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Author:

Ferreira Castro André123ORCID,Baltruschat Lothar3,Stürner Tomke34ORCID,Bahrami Amirhoushang5ORCID,Jedlicka Peter167ORCID,Tavosanis Gaia38ORCID,Cuntz Hermann12ORCID

Affiliation:

1. Frankfurt Institute for Advanced Studies, Frankfurt am Main, Germany

2. Ernst Strüngmann Institute (ESI) for Neuroscience in cooperation with Max Planck Society, Frankfurt am Main, Germany

3. Center for Neurodegenerative Diseases (DZNE), Bonn, Germany

4. Department of Zoology, University of Cambridge, Cambridge, United Kingdom

5. Max Planck Institute for Dynamics and Self Organization, Göttingen, Germany

6. Faculty of Medicine, ICAR3R – Interdisciplinary Centre for 3Rs in Animal Research, Justus Liebig University Giessen, Giessen, Germany

7. Neuroscience Center, Institute of Clinical Neuroanatomy, Goethe University, Frankfurt am Main, Germany

8. LIMES Institute, University of Bonn, Bonn, Germany

Abstract

Class I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of stochastic growth and retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure–function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.

Funder

Bundesministerium für Bildung und Forschung

Deutsche Forschungsgemeinschaft

University Medical Center Giessen and Marburg

Deutsches Zentrum für Neurodegenerative Erkrankungen

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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