Abstract
SUMMARYTo effectively control their bodies, animals rely on feedback from proprioceptive mechanosensory neurons. In the Drosophila leg, different proprioceptor subtypes monitor joint position, movement direction, and vibration. Here, we investigate how these diverse sensory signals are integrated by central proprioceptive circuits. We find that signals for leg joint position and directional movement converge in second-order neurons, revealing pathways for local feedback control of leg posture. Distinct populations of second-order neurons integrate tibia vibration signals across pairs of legs, suggesting a role in detecting external substrate vibration. In each pathway, the flow of sensory information is dynamically gated and sculpted by inhibition. Overall, our results reveal parallel pathways for processing of internal and external mechanosensory signals, which we propose mediate feedback control of leg movement and vibration sensing, respectively. The existence of a functional connectivity map also provides a resource for interpreting connectomic reconstruction of neural circuits for leg proprioception.
Highlights
Proprioception, the sense of limb position and movement, plays an indispensable role in motor control by providing continuous sensory feedback to motor circuits in the central nervous system
Functional connectivity identifies second-order proprioceptive neurons in the fly ventral nerve cord (VNC) We began by creating genetic driver lines to manipulate the activity of each femoral chordotonal organ (FeCO) subtype with optogenetics
The VNC is composed of about 20,000 neurons that develop from 34 hemilineages.[25]
Summary
Proprioception, the sense of limb position and movement, plays an indispensable role in motor control by providing continuous sensory feedback to motor circuits in the central nervous system. Golgi tendon organs detect mechanical load on the body, and muscle spindles encode muscle fiber length and contraction velocity.[9,10] Proprioceptors in invertebrates detect similar features. The three predominant classes of proprioceptors in insects are campaniform sensilla, hair plates, and chordotonal neurons.[11] Domeshaped campaniform sensilla encode mechanical load by detecting strain in the cuticle,[4] hair plates act as joint limit detectors,[12] and chordotonal neurons detect multiple features of joint kinematics.[13,14] they differ in structure, the common functional properties of vertebrate and invertebrate proprioceptors suggest that they have convergently evolved to encode similar mechanical features.[9]
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