How Do We Perceive Our Own Movements?

Even with our eyes closed, we are able to lift a bottle of water to our mouth. This feat is made possible thanks to a kind of “sixth sense” called proprioception that enables us to perceive the position and movement of our limbs within a space. Neuroscientists at the University of Fribourg have pinpointed the key role certain neurons play in the somatosensory cortex. Published in the journal Nature Communications, these findings can eventually help develop neuroprosthetics with improved performance.

It is so banal that we easily forget the marvelous complexity of our slightest gesture. Grasping a bottle and raising it to the mouth to drink its contents, even with eyes closed, holds no difficulties and impresses no one. Yet, such coordinated movement is made possible thanks to specialized sensors called proprioceptors, located in our muscles, tendons, and joints. These receptors send to the brain information on the current position of the limb. “Proprioception is an overlooked sensory system that is nevertheless essential for how we perceive where our limbs are and how they move in space,” explains Assistant Professor Mario Prsa from the Department of Neurosciences and Movement Science at the University of Fribourg (UNIFR) who led this work. ”We therefore sought to identify which specific signals are perceived and encoded in the brain when the proprioceptive system is activated”.

The body acts as a reference to its own limb movements
To find these signals, the neuroscientists at UNIFR studied the behavior of mice trained to perform a perceptual task. “We developed a robotic system for delivering quantifiable proprioceptive stimuli to the mouse forelimb,” explains Irina Scheer, a PhD student in Assistant Professor Prsa’s team. “By moving their limbs in different directions, we noticed that mice make a striking distinction between stimuli that bring the limb towards their body and those that displace it further away.” Thus, irrespective of how the different limb joints might rotate, perception of limb movement occurs in relation to the body’s peripersonal space. The neuroscientists also demonstrated that proprioceptive signals ascend from the mouse forelimb muscles to the cortex and identified cortical regions that process proprioceptive stimuli that are consciously perceived.

What do neurons encode?
In a second series of experiments, the researchers used a technique called two-photon  microscopy  to peer into the activity of hundreds of neurons in the previously identified proprioceptive cortical zones. Individual neurons showed strong directional selectivity; they were activated only when the limb moved in a specific direction. “We observed that these neurons encode limb proprioception in terms of movement direction rather than spatial location or posture,” explains Ignacio Alonso, a PhD student and co-first author. “However, all directions are not equally represented and, surprisingly, this non-uniform representation is not organized along the axis of the limb but rather along the body-fugal/petal axis.” These results, published in the journal Nature Communications, then suggest that proprioceptive neurons do not specify whether a limb is being flexed or extended, but rather that it moves towards or away from the body.

A blueprint for bi-directional neuroprosthetics
If we want a neuroprosthetic to completely replace a paralyzed or amputated limb, the device must be able to send back sensory signals to the brain to mimic proprioception. A key question then is which properties of the movement need to be taken into consideration by these new generation devices when designing stimulation parameters. “Our discoveries suggest that stimulation paradigms ought to be based on how the prosthetic arm moves relative to behaviorally relevant targets, such as the patient’s own body,” argues Mario Prsa. Beyond setting the groundwork for developing more precise, bi-directional neural prostheses, this line of research can give us a better understanding of the often bizarre nature of proprioceptive disorders and inspire new therapeutic approaches.

> Alonso I., Scheer I., Palacio-Manzano M., Frézel-Jacob N., Philippides A., Prsa M.:
Peripersonal encoding of forelimb proprioception in the mouse somatosensory cortex