Functional Recovery of Aimed Scratching Movements after a Graded Proprioceptive Manipulation

Abstract

To demonstrate the role of proprioceptive feedback in aimed limb movements, we induced graded changes in the signals provided by the principal receptor in a leg of a locust. The femoro-tibial chordotonal organ (FCO) of the hindleg monitors extension and flexion movements of the tibia and provides the main source of proprioceptive feedback about tibial kinematics. The FCO apodeme (tendon) was surgically shortened by different amounts to provide a systematic bias to this feedback, and aimed scratching movements were analyzed over the week after surgery. Shortening the apodeme led to increased firing of sensory neurons of the FCO at flexed joint angles and is thus functionally similar to flexing the tibia. Immediately after surgery, limb movements shifted dorsally and posteriorly, driven by overextension of the femoro-tibial joint and changes at other joints of the limb. The extent of tibial overextension reflected the extent of apodeme shortening. Overextension would tend to renormalize the FCO feedback signal and can be explained by known interjoint reflex pathways. Our data demonstrate that proprioceptive feedback provides a graded signal that is used to control these aimed limb movements. Over the course of 7 d after surgery, there was a functional recovery in aiming as the overall patterns of movement returned toward control values driven by reciprocal compensatory changes at two joints. The sensory to motor pathways are monosynaptic and oligosynaptic in this system, thus providing us with a powerful opportunity to investigate further the sensorimotor transformations and plasticity of aimed limb movements.

Recovery of locomotion after injury inDrosophiladepends on proprioception

“…Equally important has been an exploration of the interplay of proprioception and recovery in motor control in various insects. For example, Page and Matheson considered locusts and found a shift in limb movements intended for scratching after a surgery-induced decrease in proprioception, followed by recovery to pre-surgery values over the course of a week (Page and Matheson, 2009); Büschges and Pearson discovered that the removal of wing proprioceptors in locusts led to a decreased recovery of the flight motor pattern after wing injury (Büschges and Pearson, 1991;Büschges et al, 1992). Our study points to proprioception as a crucial player in mediating orientation profile plasticity by determining how well an animal can control the individual forces it exerts.…”

Proprioception

“…Increasing tension on the femoral chordotonal organ, by surgical shortening of the tendon (left), leads to consistent reaching errors produced by changes at each leg joint angle (right). Republished with permission of the Society for Neuroscience, adapted from Page and Matheson (2009). R200 Current Biology 28, R187-R207, March 5, 2018 appears that regulatory circuits have evolved to deal with the physiological delays inherent in the proprioceptive system and adjust feedback gains to prevent tremor and maintain stability.…”

Central processing of leg proprioception inDrosophila

“…1E). Experimental manipulation of the FeCO in several insect species has revealed its importance during behaviors like walking and targeted reaching (Bässler, 1988;Field and Burrows, 1982;Mendes et al, 2013;Page and Matheson, 2009).…”