Recovery of locomotion after injury in Drosophila depends on proprioception

Author:

Isakov Alexander12,Buchanan Sean M.3,Sullivan Brian24,Ramachandran Akshitha24,Chapman Joshua K. S.3,Lu Edward S.24,Mahadevan L.1245,de Bivort Benjamin234

Affiliation:

1. Department of Physics, Harvard University, Cambridge, MA 02138, USA

2. Center for Brain Science, Harvard University, Cambridge, MA 02138, USA

3. Rowland Institute at Harvard, Cambridge, MA 02142, USA

4. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA

5. School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138, USA

Abstract

Locomotion is necessary for survival in most animal species. However, injuries to the appendages mediating locomotion are common. We assess the recovery of walking in Drosophila melanogaster following leg amputation. Whereas flies pre-amputation explore open arenas in a symmetric fashion, foreleg amputation induces a strong turning bias away from the side of the amputation. However, we find that unbiased walking behavior returns over time in wild type flies, while recovery is significantly impaired in proprioceptive mutants. To identify the biomechanical basis of this locomotor impairment and recovery, we then examine individual leg motion (gait) at a fine scale. A minimal mathematical model that links neurodynamics to body mechanics during walking shows that redistributing leg forces between the right and left side enables the observed recovery. Altogether, our study suggests that proprioceptive input from the intact limbs plays a critical role in the behavioral plasticity associated with locomotor recovery after injury.

Funder

Air Force Office of Scientific Research

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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