A leg to stand on: computational models of proprioception

Abstract

Dexterous motor control requires feedback from proprioceptors, internal mechanosensory neurons that sense the body's position and movement. An outstanding question in neuroscience is how diverse proprioceptive feedback signals contribute to flexible motor control. Genetic tools now enable targeted recording and perturbation of proprioceptive neurons in behaving animals; however, these experiments can be challenging to interpret, due to the tight coupling of proprioception and motor control. Here, we argue that understanding the role of proprioceptive feedback in controlling behavior will be aided by the development of multiscale models of sensorimotor loops. We review current phenomenological and structural models for proprioceptor encoding and discuss how they may be integrated with existing models of posture, movement, and body state estimation.

Figure 1:

Examples of experimental perturbations used to probe the role of proprioceptive feedback in motor control. Top left: Vibration of hamstring muscles in humans stimulated muscle spindles, leading to an increase in walking speed [7]. Bottom left: Inverting sensory feedback from the femoral chordotonal organ of a stick insect front leg by crossing the receptor tendon (arrow) led to saluting or dragging of the leg during walking and waving during rest (front leg in the air, other legs on the ground). The normal rest posture of the front leg (extended in air) recovered after a few days, but saluting and dragging during walking remained unchanged [8]. Top right: Optogenetic stimulation of second-order proprioceptive neurons in tethered Drosophila walking on a treadmill caused a decrease in walking speed. Trace shows mean of multiple animals [9]. Bottom right: Genetic ablation of hindlimb muscle spindles in the mouse lumbar spinal cord caused inter-limb coordination deficits only during fast walking. 3D plots show timing (phase) of right hindlimb (RH), right forelimb (RF), and left forelimb (LF) relative to left hindlimb (LH) for gait cycles with (gray) and without (green) muscle spindles [10].

Figure 2:

Anatomical and computational view of proprioceptive feedback in motor control. Left: Proprioceptors from the limbs project to the spinal cord (in vertebrates) and the ventral nerve cord (VNC, in invertebrates), where they transmit sensory signals to distributed circuits for posture and movement control. Right: Proprioceptive signals affect motor control on different timescales through multiple nested feedback loops. Proprioceptive signals are integrated in low- and high-level controllers for posture, movement, and planning. They may also be used to estimate the state of the body. Note that each box represents a computation, not necessarily an anatomically confined circuit. Computations higher up in the hierarchy are more abstract and operate at longer timescales.