A mechanical time window for correct proprioceptor development

Proprioception requires the transduction of mechanical strain generated by muscle contractions into sensory neuron activity. Although mechanical forces are essential for the function of mechanosensory organs, their role in the development of these organs remains largely unknown. It was already shown that the fly chordotonal organ (ChO), a multicellular proprioceptor, must acquire correct mechanical properties for proper function. Here, using an in vivo approach, we identify a critical mechanical time window during which the ChOs must experience appropriate mechanical forces to acquire the mechanical properties required for sensory function. To define this developmental window, we downregulated Pericardin (Prc), a major component of the ChO extracellular matrix, at different time points during embryonic and larval development. We then measured in vivo the efficiency with which muscle-generated deformations are converted into compressive strain in the ChO cap cell, a key step in transmitting mechanical forces to the sensory neuron. The most severe effect on conversion efficiency was evident when prc was downregulated during late embryogenesis, a time window which coincides with the onset of embryonic muscle contractions. This observation suggests that muscle-generated forces provide developmental cues required for the development of ChOs with correct mechanical properties. Consistent with this hypothesis, reducing muscle-generated forces during the same embryonic period resulted in a similar phenotype of impaired ChO mechanics and sensory function. Together, our findings reveal a previously unknown role for muscle-generated forces in shaping the development of fully functional proprioceptors.