Human standing is modified by an unconscious integration of congruent sensory and motor signals

Abstract

We investigate whether the muscle response evoked by an electrically induced vestibular perturbation during standing is related to congruent sensory and motor signals. A robotic platform that simulated the mechanics of a standing person was used to manipulate the relationship between the action of the calf muscles and the movement of the body. Subjects braced on top of the platform with the ankles sway referenced to its motion were required to balance its simulated body-like load by modulating ankle plantar-flexor torque. Here, afferent signals of body motion were congruent with the motor command to the calf muscles to balance the body. Stochastic vestibular stimulation (±4 mA, 0-25 Hz) applied during this task evoked a biphasic response in both soleus muscles that was similar to the response observed during standing for all subjects. When the body was rotated through the same motion experienced during the balancing task, a small muscle response was observed in only the right soleus and in only half of the subjects. However, the timing and shape of this response did not resemble the vestibular-evoked response obtained during standing. When the balancing task was interspersed with periods of computer-controlled platform rotations that emulated the balancing motion so that subjects thought that they were constantly balancing the platform, coherence between the input vestibular stimulus and soleus electromyogram activity decreased significantly (P < 0.05) during the period when plantar-flexor activity did not affect the motion of the body. The decrease in coherence occurred at 175 ms after the transition to computer-controlled motion, which subjects did not detect until after 2247 ms (Confidence Interval 1801, 2693), and then only half of the time. Our results indicate that the response to an electrically induced vestibular perturbation is organised in the absence of conscious perception when sensory feedback is congruent with the underlying motor behaviour.

Figure 1. Experimental set-up

A, the subject was securely strapped to a rigid backboard on top of a motion platform that could be controlled by modulating the ankle torque exerted on the force plate. The platform rotated about an axis that passed through the subject's ankles (broken line). Seatbelts placed across the shoulders and around the waist prevented the subject from falling forward without supporting the load of the body acting through the feet. Raw data of the vestibular stimulus and electromyography (EMG) activity of the right (r-SOL) and left (l-SOL) soleus muscles are shown during a trial where the subject balanced the platform programmed with the mechanics of an inverted pendulum. During standing trials, the platform was stationary, seatbelts were removed and the rigid backboard was retracted. B, the subject was seated and balanced the inverted pendulum-like platform by modulating the torque generated by abducting the extended index finger against an immovable load cell. The subject stabilised the right hand by grasping a steel cylinder that was mounted to the backboard. A vestibular stimulus was delivered as the subject balanced the platform, and EMG activity was recorded for the first dorsal interosseus (FDI).

Figure 2. Vestibular-evoked muscle responses for a single subject

Coherence was computed between the vestibular stimulus and left (grey) or right (black) soleus EMG activity. Cumulant density functions represent the evoked muscle response to vestibular stimulation. Data are shown during the reference standing trial (A), the control trial where the subject was braced to a stationary platform (B), and for the trials in which the sensory signals of body motion were either congruent (C) with or decoupled (D) from the motor command to the leg muscles. Horizontal lines represent the 95% CIs, and vertical lines indicate the short- and medium-latency peaks for the right soleus during the reference standing trial.

Figure 3. Averaged muscle responses to electrical vestibular stimulation

Group mean (n= 10) data are shown for the reference standing trial (A), the control trial where the platform was stationary (B), the balancing trial where sensory signals of body motion were congruent with the motor command to balance the body (C), and when sensory signals of body motion were decoupled from the motor command (D). Coherence between the vestibular stimulus and soleus EMG activity is shown for the left (grey) and right (black) legs. Thin lines represent the 95% confidence limits about the group means (thick lines) for the cumulant density functions.

Figure 4. Human-controlled balancing with a non-postural hand muscle

Data are shown for a single subject (A) in the top panel with group means (n= 10) below (B). Subjects were seated on top of an inverted pendulum-like platform that they balanced by modulating the abduction torque generated by the right index finger. Coherence between the vestibular stimulus and EMG activity of the right FDI is shown on the left, and the vestibular-evoked muscle response in FDI is shown on the right. Horizontal lines in the single subject data and thin lines in the group mean data represent the 95% confidence limits.

Figure 5. Mean rectified EMG data during the pseudo-balance transitions

Single-subject data are presented for the right soleus muscle as mean rectified electromyogram (EMG) from 100 transitions. Data are shown as the subject balanced the platform prior to the withdrawal of human control at time zero, during the period of computer-controlled motion (shaded area), and after the reinstatement of human control at 4 s. The group mean (n= 5) data are shown for the same muscle.

Figure 6. Pseudo-balance

Time-varying changes in coherence between the vestibular stimulus and soleus EMG activity during 100 transitions from human- to computer-controlled motion of the robotic platform. Data are shown for a single subject (A) and the group mean (B) for all five subjects. The 4 s period prior to time zero shows frequency-specific coherence as subjects were braced on top of the platform and balanced its body-like load with their feet. Time zero represents the transition point from human-controlled balancing of the platform to a computer-controlled rotation of the platform along a predetermined path, which lasted for 4 s (between the vertical lines), before subjects regained control of the platform. The mean of the coherence from 0 to 25 Hz at each time point is shown across the bottom panel. Non-significant data points have been removed so that zero coherence represents the values below the threshold of the 99% confidence limit; 0.046 for the single subject and 0.0093 for the group mean data.