The brain uses extrasomatic information to estimate limb displacement

Abstract

A fundamental problem faced by the brain is to estimate whether a touched object is rigidly attached to a ground reference or is movable. A simple solution to this problem would be for the brain to test whether pushing on the object with a limb is accompanied by limb displacement. The mere act of pushing excites large populations of mechanoreceptors, generating a sensory response that is only weakly sensitive to limb displacement if the movements are small, and thus can hardly be used to determine the mobility of the object. In the mechanical world, displacement or deformation of objects frequently co-occurs with microscopic fluctuations associated with the frictional sliding of surfaces in contact or with micro-failures inside an object. In this study,we provide compelling evidence that the brain relies on these microscopic mechanical events to estimate the displacement of the limb in contact with an object, and hence the mobility of the touched object. We show that when pressing with a finger on a stiff surface, fluctuations that resemble the mechanical response of granular solids provoke a sensation of limb displacement. Our findings suggest that when acting on an external object, prior knowledge about the sensory consequences of interacting with the object contributes to proprioception.

Figure 1.

Stimuli description. (a) Observers pressed on an active surface comprising individually controlled, laterally moving, actuated elements. A load cell reported the vertical component of the applied force. A stiff servomechanism could optionally move the tactile active surface vertically. (b) The elements oscillated at a rate proportional to the temporal change of the pressing force. The oscillations occurred only when the force was above a constant lower limit and below a variable upper limit, at which point the observers stopped pressing. (c) In the in-phase condition, all elements moved in the same direction. In the anti-phase condition, each element moved in the direction opposite to that of its neighbours.

Figure 2.

Spectral power of the in-phase stimulus and of force fluctuations elicited when pressing on granular material. The granular material, represented by a latex rubber bag filled with beads, was pressed by the experimenter. The in-phase and anti-phase stimuli (figure 1) were produced by the stimulation device impinging on a block of silicon rubber, simulating a finger. The signal power in the 200–1000 Hz frequency band were plotted against the rate of normal force change. The solid lines denote median values, the shaded regions give non-parametric estimates of their 95% CIs. (Online version in colour.)

Figure 3.

Results of experiment 1 for n = 10 observers. Crossed vertical lines denote the average and standard deviation (s.d.) for each individual participant. The data are plotted against the upper force limit and the coefficient of modulation. The group average and s.d. are shown with boxes. The effect of the upper force limit and of the modulation coefficient was tested with the non-parametric, conservative Durbin test. The effect of the upper force limit on perceived displacement was significant only for the in-phase stimulus.

Figure 4.

Results of experiment 3. (a) Psychometric curves of a representative observer with a 5 mm reference displacement of the surface. The point at which the curve ordinates are equal to 0.5 corresponds to the same perceived displacement of the platform with and without skin stimulation. (b) The points of subjective equivalence (same perceived displacement) for n = 10 observers with group average and standard deviation. (Online version in colour.)