Mechanical Properties of a Drosophila Larval Chordotonal Organ

Abstract

Proprioception is an integral part of the feedback circuit that is essential for locomotion control in all animals. Chordotonal organs perform proprioceptive and other mechanosensory functions in insects and crustaceans. The mechanical properties of these organs are believed to be adapted to the sensory functions, but had not been probed directly. We measured mechanical properties of a particular chordotonal organ-the lateral pentascolopidial (lch5) organ of Drosophila larvae-which plays a key role in proprioceptive locomotion control. We applied tension to the whole organ in situ by transverse deflection. Upon release of force, the organ displayed overdamped relaxation with two widely separated time constants, tens of milliseconds and seconds, respectively. When the muscles covering the lch5 organ were excised, the slow relaxation was absent, and the fast relaxation became faster. Interestingly, most of the strain in the stretched organ is localized in the cap cells, which account for two-thirds of the length of the entire organ, and could be stretched by ∼10% without apparent damage. In laser ablation experiments we found that cap cells retracted by ∼100 μm after being severed from the neurons, indicating considerable steady-state stress and strain in these cells. Given the fact that actin as well as myosin motors are abundant in cap cells, the results point to a mechanical regulatory role of the cap cells in the lch5 organ.

A Change in ECM Composition Affects Sensory Organ Mechanics and Function

“…In the wt larvae, muscle contractions lead to shortening of the cap cell with no apparent change in the length of the ligament cell ( Figures 2C and 2D), suggesting that the ChO elastic response is dominated by the cap cell and the ligament cell acts as a rigid body, in agreement with (Prahlad et al, 2017). This finding is consistent with the observation that most of the elongation of the sensory organ during development is attributed to the cap cell.…”

“…The mechanical probe was positioned next to the center of the cap cell and oscillated in a direction perpendicular to the axis of the cap cell with an amplitude of 25 mm using an Arbitrary function generator (Stanford DS345). A similar setup was used in Prahlad et al (2017).…”

Neuronal stretch reception – Making sense of the mechanosense

“…Superresolution imaging showed that dCirl colocalizes to region with the mechanosensitive channel where it suppresses cAMP levels and increases excitability of ChOs Interestingly, the opsins also seem to have a neuroprotective function, as dendrites lacking NINAE and Rh6 are more flaccid, disorganized and showed increased membrane blebbing than in wildtype flies 65 . These phenotypes are similar to neuromechanical defects seen in C. elegans mechanosensors 68 and it is interesting to speculate whether or not the mechanical pre-stress seen in chordotonal organs 57 70 , DVA interneurons 48,71,72 , the SMD neurons 73 and VA, VB motoneurons 74,75 (Fig. 1E).…”

“…How a mechanical stretch can cause bending of the cilia is a mystery, but active motility was suggested to cause lateral deflection of the ciliary microtubules 56 . Laser cutting of the ChO suggest that the sensory and support cells are under constitutive mechanical tension 57 .…”

“…Direct mechanical deformation also suggest that the bending stiffness of the organs is relatively low compared to its stretch stiffness, consistent with chord held under tension. The molecules and structures supporting this pre-tension are not known, but due to the abundance of myosin in the cap cells, it is likely that it plays a prominent role in cell mechanics 57 . The ECM seems to play a special role in cell mechanics and force transfer.…”