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X-ray holographic nanotomography unveils fruit-fly leg sensors

X-ray holographic nanotomography, RNA sequencing and computer modelling were combined to investigate how neurons sense leg movements in the common fruit fly, Drosophila. The mechanism was discovered to be a specialised biomechanical architecture, which could also apply to other sensory systems.

Our ability to sense and move our bodies without relying on visual cues relies on proprioceptors, sensory neurons that detect mechanical forces within the body. All walking animals use proprioceptors to control limb movements, and they work similarly in both vertebrates and invertebrates. Different types of proprioceptors detect different kinematic features, such as joint position, movement and vibration, but the mechanisms that underlie how each proprioceptor senses different aspects of movement remain poorly understood. One possibility is that differences in cellular properties, such as gene expression, allow different sensory neuron subtypes to sense distinct mechanical features. An alternative mechanism is biomechanical specialisation, whereby specialised attachment structures could detect and transmit distinct forces to different proprioceptor subtypes.

This work investigated how different proprioceptors in a fruit-fly leg detect different aspects of movement, assessing both genetic and biomechanical contributions. Fruit flies, or Drosophila, are an often-studied model system in neuroscience due to their well-known and relatively simple neuroanatomy. Drosophila has a proprioceptor called the femoral chordotonal organ (FeCO), which has a range of different sensory neurons that help the fly know where its leg is or which way its leg is moving, or sense vibrations. Nano-imaging technique X-ray holographic nanotomography (XHN) was employed at beamline ID16A to reconstruct the neural structure of FeCO in the Drosophila leg in 3D and at high spatial resolution (Figure 2).

The reconstruction revealed that FeCO neurons are organised into three anatomical compartments within the femur: claw neurons, which encode tibia position (flexion or extension); hook neurons, which encode directional movement (flexion or extension); and club neurons, which encode bidirectional movement and low amplitude, high-frequency vibration (Figure 3). Each type of neuron is connected to the leg structure in a very different mechanical way, suggesting they are able to receive different mechanical signals from the same joint and are therefore biomechanically specialised to detect distinct features of leg joint movement. In this way, claw

Fig. 2: X-ray holographic nanotomography reconstruction of Drosophila femur revealing FeCO organisation. FeCO

compartments and tendons are indicated by colour shading: green: club; magenta: claw; hook: orange).