Central processing of leg proprioception inDrosophila

Abstract

Proprioception, the sense of self-movement and position, is mediated by mechanosensory neurons that detect diverse features of body kinematics. Although proprioceptive feedback is crucial for accurate motor control, little is known about how downstream circuits transform limb sensory information to guide motor output. Here, we investigate neural circuits in Drosophila that process proprioceptive information from the fly leg. We identify three cell-types from distinct developmental lineages that are positioned to receive input from proprioceptor subtypes encoding tibia position, movement, and vibration. 13Bα neurons encode femur-tibia joint angle and mediate postural changes in tibia position. 9Aα neurons also drive changes in leg posture, but encode a combination of directional movement, high frequency vibration, and joint angle. Activating 10Bα neurons, which encode tibia vibration at specific joint angles, elicits pausing in walking flies. Altogether, our results reveal that central circuits integrate information across proprioceptor subtypes to construct complex sensorimotor representations that mediate diverse behaviors, including reflexive control of limb posture and detection of leg vibration.

Functional architecture of neural circuits for leg proprioception inDrosophila

“…However, blocking acetylcholine receptors with MLA reduced but did not eliminate club-driven calcium signals in 10Bα neurons (Figure 3C-D). These data suggest that the connection between club and 10Bα neurons consists of mixed chemical/electrical signaling, which is consistent with previous work (Agrawal et al, 2020). Interestingly, we observed that the time to peak of the 10Bα calcium signals was significantly longer in the presence of MLA (Figure 3D), which suggests that chemical and electrical transmission may have distinct temporal dynamics.…”

“…A subset of 10Bα neurons also project to the brain, arborizing in the contralateral antennal mechanosensory and motor center (AMMC, data not shown). Previous work showed that optogenetic activation of 10Bα neurons caused walking flies to pause, consistent with a role in detecting substrate vibration (Agrawal et al, 2020).…”

“…This organization suggests that signals from different FeCO subtypes may be processed by separate downstream neurons (Figure 1A, right). However, apart from three specific VNC cell classes (Agrawal et al, 2020), little is known about how information from different FeCO subtypes is integrated by downstream circuits in the Drosophila VNC that underlie sensation and guide movement of the leg.…”

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae

“…Second, these mechanosensory neurons are morphologically diverse and have topographically organized projections into the CNS ( Kamikouchi et al, 2006 ; Mamiya et al, 2018 ). Third, the subpopulations can differentially interface with downstream circuitry to influence distinct behaviors or movements ( Agrawal et al, 2020 ; Hampel et al, 2015 ; Kim et al, 2020 ; Vaughan et al, 2014 ). Fourth, similar features of mechanosensory stimuli can be represented in neurons downstream of the JO and FeCO ( Agrawal et al, 2020 ; Chang et al, 2016 ).…”

“…Third, the subpopulations can differentially interface with downstream circuitry to influence distinct behaviors or movements ( Agrawal et al, 2020 ; Hampel et al, 2015 ; Kim et al, 2020 ; Vaughan et al, 2014 ). Fourth, similar features of mechanosensory stimuli can be represented in neurons downstream of the JO and FeCO ( Agrawal et al, 2020 ; Chang et al, 2016 ). These commonalities suggest that results obtained through studies of different chordotonal organs could be mutually informative.…”