Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position

Abstract

A central problem in motor control, in the representation of space, and in the perception of body schema is how the brain encodes the relative positions of body parts. According to psychophysical studies, this sense of limb position depends heavily on vision. However, almost nothing is currently known about how the brain uses vision to determine or represent the location of the arm or any other body part. The present experiment shows that the position of the arm is represented in the premotor cortex of the monkey (Macaca fascicularis) brain by means of a convergence of visual cues and proprioceptive cues onto the same neurons. These neurons respond to the felt position of the arm when the arm is covered from view. They also respond in a similar fashion to the seen position of a false arm.

Figure 1

Visual responses of a typical premotor neuron with a tactile RF (hatched) on the forearm and hand, and a visual RF within 10 cm of the tactile RF. (A) On each trial, the arm contralateral to the neuron was fixed in one of two positions and the visual stimulus was advanced along one of four trajectories (–4). For this neuron, the two arm positions were chosen to align the visual RF near the hand and forearm with trajectories 2 and 3. For other neurons, the arm was moved to different extents depending on the location of the visual RF, to better capture the movement of the visual RF with the arm. (B) Responses of the neuron to the four stimulus trajectories when the arm was visible to the monkey. When the arm was fixed on the right, the response was maximum at position 3. When the arm was fixed on the left, the maximum response moved to the left, to position 2. (C) Responses of the neuron when the arm was covered. The movement of the visual RF with the arm was reduced but not eliminated, indicating that the neuron combined both proprioceptive and visual information about the position of the arm. Each point is a mean of 10 trials. Error bars are standard error.

Figure 2

Mean SI (amount that the visual RF shifted when the arm was moved) under three conditions: first, when the arm was uncovered and the monkey had both visual and proprioceptive information about arm position; second, when the arm was covered and the monkey had only proprioceptive information about arm position; and third, when the monkey’s arm was stationary and blocked from view, and a detached, stuffed monkey arm was placed in view and moved to two different positions. N = number of neurons per mean. Error bars are standard error of the mean. The SI for Arm Uncovered was significantly greater than zero: mean = 0.18, SEM = 0.04, t = 4.97, P < 0.0001. The SI for Arm Covered was significantly greater than zero: mean = 0.08, SEM = 0.03, t = 2.75, P < 0.01. The SI for Visual + Proprioceptive was significantly greater than the SI for Proprioceptive: t test for correlated data, t = 2.77, P < 0.05, adjusted with the Bonferroni correction for multiple tests. The SI for Fake Arm was significantly greater than zero: mean = 0.12, SEM = 0.06, t = 2.20, P < 0.05.

Figure 3

Effect of the sight of the monkey’s own arm and of a detached, stuffed monkey arm on responses of premotor neurons. For each neuron, three SIs were calculated. SI_{visual+proprioceptive} indicates the amount that the visual RF moved with the monkey’s arm, when the arm was uncovered and within view. SI_{proprioceptive} indicates the amount that the visual RF moved with the arm, when the arm was covered from view. SI_visual indicates the amount that the visual RF moved when the monkey’s arm was blocked from view and a stuffed arm was placed in view and moved to different positions. SI_{visual+proprioceptive} − SI_{proprioceptive} provides an estimate of the amount that the sight of the arm influences the neuron. SI_visual provides an independent measure of the same property. These two measures were highly correlated. The line at slope = 1 is also plotted.