Proprioception Is Necessary for Body Schema Plasticity: Evidence from a Deafferented Patient

Abstract

The ability of using a large variety of tools is important in our daily life. Behind human tool-use abilities lays the brain capacity to incorporate tools into the body representation for action (Body Schema, BS), thought to rely mainly on proprioceptive information. Here, we tested whether tool incorporation is possible in absence of proprioception by studying a patient with right upper-limb deafferentation. We adopted a paradigm sensitive to changes of the BS and analyzed the kinematics of free-hand movements before and after tool-use, in three sessions over a period of 2 years. In the first session, before tool-use, the kinematics of the deafferented hand was disrupted. Similarly, the first movements with the tool (a mechanical grabber elongating the arm by ~40 cm) showed an abnormal profile that tended to normalize at the end of the session. Subsequent free-hand movements were also normalized. At session 2, 6 months later, the patient exhibited normal free-hand kinematic profiles, additionally showing changes in grasping kinematics after tool-use, but no sign of tool incorporation. A follow-up 2 years later, further confirmed the normalized kinematic profile but the absence of tool incorporation. This first description of tool-use in absence of proprioception shows the fundamental role of proprioception in the update of the BS. These results provide an important further step in understanding human motor control and have implications for future development of rehabilitation programs for patients with sensory deficits.

Keywords: body schema; deafferentation; grasping; kinematic; tool-use.

FIGURE 1

Patient D.C. post surgery MRI and experimental timeline. (A) Coronal (left) and midsagittal (right) view of patient D.C.’s post surgery lesion. (B) Experimental timeline for the three testing sessions.

FIGURE 2

Acceleration and velocity profile for free-hand and tool grasping movements during Session 1. Velocity (blue) and Acceleration (yellow) profile of representative movements performed before tool use (A), during the first and last tool blocks (B,C) and after (D) tool use in Session 1. D.C.’s kinematic profile was characterized by multiple peaks in the pre tool-use phase as well as in the very first block of tool-use. The kinematic profile evolved during the use of the grabber and in the last block D.C. showed a cleaner profile. The same profile was then transferred to the hand in the post-tool use phase where D.C. shows single Velocity and Acceleration main peaks.

FIGURE 3

Free-hand grasping movements were affected after tool-use in session 2. Patient D.C. showed longer latencies for all parameters and reduced peak amplitude for acceleration and Velocity of Fingers Aperture (VFA). Velocity and Deceleration peaks showed the same tendency but failed to reach significance. Asterisks indicate significant differences, error bars represent SD.

FIGURE 4

Free-hand grasping movements were affected after tool-use in session 3. Patient D.C. showed longer latencies for all parameters [except Maximal Grip Aperture (MGA)] and reduced peak amplitude for the transport component parameters. Asterisks indicate significant differences, error bars represent SD.