A developmental stretch-and-fill process that optimises dendritic wiring

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

Summary Circuit connectivity and computation depend on how dendrites branch and occupy space within neural tissue. While optimal wiring principles have long been known to constrain dendritic morphology and their scaling behaviour, the growth dynamics that produce such optimised structures remain unclear. Leveraging structural imaging across development, we identify two complementary growth strategies – inside-out versus outside-in – that together generate mature dendritic arbours. We formalise these dynamics in a mathematical model that captures the two growth modes and show that their interplay yields wiring-efficient, space-filling morphologies and class-specific developmental trajectories across species. This framework provides an algorithmic account of how local branching dynamics give rise to globally optimised architectures. By linking dendritic growth rules to functional design constraints, our theory offers a unifying description of dendritic differentiation and a basis for understanding how coverage and connectivity emerge during neural circuit formation. In brief We derive a detailed mathematical model that describes long-term time-lapse data of growing dendrites; it optimises total wiring and space-filling. Highlights Fly neurons stretch and fill a given target area with precise scaling relations. We observe a sequence of two growth strategies. Each growth type implements optimal wiring which leads to optimal space filling. A model combining these programs captures the development of dendritic structures. Abstract Figure

Authors 3

1. Lothar Baltruschat

   German Center for Neurodegenerative Diseases · Max Planck Institute for Biological Intelligence · Max Planck Institute of Neurobiology

   Affiliation as printed

   Center for Neurodegenerative Diseases (DZNE), Bonn, Germany

   Max-Planck Institute of Biological Intelligence, 82152 Martinsried, Germany

   Deprtment of Systems nd Computtionl Neurobiology, Mx-Plnck Institute of Neurobiology, Mrtinsried, Germny

2. Gaia Tavosanis Aachen Institute of Developmental Biology/ BioII

   RWTH Aachen University · German Center for Neurodegenerative Diseases · Max Planck Institute for Biological Intelligence

   Affiliation as printed

   Center for Neurodegenerative Diseases (DZNE), Bonn, Germany

   Institute of Developmental Biology/ BioII, RWTH Aachen University, Germany

   Max-Planck Institute of Biological Intelligence, 82152 Martinsried, Germany

3. Hermann Cuntz

   Justus-Liebig-Universität Gießen · Max Planck Society · Max Planck Institute for Biological Intelligence · Frankfurt Institute for Advanced Studies · Ernst Strüngmann Institute for Neuroscience

   Affiliation as printed

   Computer-Based Modelling in the field of 3R Animal Protection, Faculty of Medicine, Justus Liebig University Giessen, Giessen, Germany

   Ernst Strü ngmann Institute (ESI) for Neuroscience in cooperation with the Max Planck Society, Frankfurt-am-Main, 60528, Germany

   Frankfurt Institute for Advanced Studies, Frankfurt-am-Main, 60438, Germany

   Max-Planck Institute of Biological Intelligence, 82152 Martinsried, Germany

   Translational Neuroscience Network Giessen, Germany