Force and Position Control in Humans - The Role of Augmented Feedback

Summary

Controlling an identical movement with position or force feedback results in different neural activation and motor behavior. This protocol describes how to investigate behavioral changes by looking at neuromuscular fatigue and how to evaluate motor cortical (inhibitory) activity using subthreshold TMS with respect to the interpretation of augmented feedback.

Abstract

During motor behaviour, humans interact with the environment by for example manipulating objects and this is only possible because sensory feedback is constantly integrated into the central nervous system and these sensory inputs need to be weighted in order meet the task specific goals. Additional feedback presented as augmented feedback was shown to have an impact on motor control and motor learning. A number of studies investigated whether force or position feedback has an influence on motor control and neural activation. However, as in the previous studies the presentation of the force and position feedback was always identical, a recent study assessed whether not only the content but also the interpretation of the feedback has an influence on the time to fatigue of a sustained submaximal contraction and the (inhibitory) activity of the primary motor cortex using subthreshold transcranial magnetic stimulation. This paper describes one possible way to investigate the influence of the interpretation of feedback on motor behaviour by investigating the time to fatigue of submaximal sustained contractions together with the neuromuscular adaptations that can be investigated using surface EMG. Furthermore, the current protocol also describes how motor cortical (inhibitory) activity can be investigated using subthreshold TMS, a method known to act solely on the cortical level. The results show that when participants interpret the feedback as position feedback, they display a significantly shorter time to fatigue of a submaximal sustained contraction. Furthermore, subjects also displayed an increased inhibitory activity of the primary cortex when they believed to receive position feedback compared when they believed to receive force feedback. Accordingly, the results show that interpretation of feedback results in differences on a behavioural level (time to fatigue) that is also reflected in interpretation-specific differences in the amount of inhibitory M1 activity.

Introduction

Sensory feedback is crucial to perform movements. Daily activities are hardly possible in the absence of proprioception ¹. Furthermore, motor learning is influenced by proprioceptive integration ² or cutaneous perception ³. Healthy humans with intact sensation are able to weight the sensory inputs arising from various sensory sources in order to meet situation-specific needs ⁴. This sensory weighing enables humans to perform difficult tasks with high precision even when some aspects of the sensory information are unreliable or even absent (e.g., walking in the dark or with eyes closed).

Additionally, various evidence suggests that providing augmented (or additional) feedback further improves motor control and/or motor learning. Augmented feedback provides additional information by an external source which can be added to the task intrinsic (sensory) feedback arising from the sensory system ^5,6. Especially the effect of the content of augmented feedback on motor control and learning has been of great interest in recent years. One of the questions addressed was how humans control force and position ^7,8. Initial investigations identified differences in time to fatigue of a sustained submaximal contraction using either position or force feedback and differences in load compliance (e.g., ^9-12). When subjects were provided with force feedback, the time to fatigue of the sustained contraction was significantly longer compared to when position feedback was provided. The same phenomenon was observed for a variety of different muscles and limb positions and a number of neuromuscular mechanisms, including a greater rate of motor unit recruitment and a greater decrease in H-reflex area during the position controlled contraction (for review ¹³). However, in these studies, not only the visual feedback but also the physical characteristics of the muscular contraction (i.e., the compliance of the measurement device) was altered. Therefore, we recently conducted a study not altering compliance but only augmented feedback and provided evidence that provision of force and position feedback alone during a sustained submaximal contraction can cause differences in inhibitory activity within the primary motor cortex (M1). This was shown using a stimulation technique that is known to act solely at the cortical level ¹⁴, namely subthreshold transcranial magnetic stimulation (subTMS). Unlike suprathreshold TMS, the response evoked by subTMS, is not modulated by the excitability of spinal α-motoneurons and the excitability excitatory neurons and/or cortical cells ^15-17 but solely by the excitability of inhibitory intracortical neurons. The postulated mechanism behind this stimulation technique is that it is applied at intensities below the threshold to evoke a motor evoked potential (MEP). It was shown in patients having electrodes implanted at the cervical level that this type of stimulation does not produce any descending activity but that it primarily activates inhibitory interneurons within the primary motor cortex ^14,18,19. This activation of inhibitory interneurons causes a decrease in the ongoing EMG activity and can be quantified by the amount of EMG suppression compared to the EMG activity obtained in trials without stimulation. In this respect, we showed that subjects displayed a significantly greater inhibitory activity in trials in which they received position feedback compared with trials in which force feedback was provided ²⁰. Furthermore, we also showed that not only the presentation of different feedback modalities (force vs. position control) but also the interpretation of feedback can have very similar effects on behavioural and neurophysiological data. More specifically, when we told the participants to receive position feedback (even though it was force feedback) they also not only displayed a shorter time to fatigue but also an increased level of inhibitory M1 activity ²¹. Using an approach where the same feedback but with different information about its content is always provided has the advantage that the task constraints, i.e., the presentation of the feedback, the gain of the feedback, or the compliance of the load are identical between conditions so that differences in performance and neural activity are clearly related to differences in the interpretation of the feedback and are not biased by different testing conditions. Thus, the current study investigated whether a different interpretation of one and the same feedback influences the duration of a sustained submaximal contraction and furthermore has an impact on the activation of inhibitory activity of the primary motor cortex.

Protocol

The protocol described here followed the guidelines of the ethics committee of the University of Freiburg and was in accordance with the declaration of Helsinki (1964).

1. Ethical Approval - Subject Instruction

1. Before the actual experiment, instruct all subjects about the purpose of the study and potential risk factors. When applying transcranial magnetic stimulation (TMS), there are some medical risks including any history of epileptic seizures, metal implants in eyes and/or head, diseases of the cardiovascular system and pregnancy. Exclude any subject affirming to one of these risk factors from the study.
2. Include only healthy individuals in the study. Exclude individuals with any neurological, mental and/or orthopaedic diseases.

2. Subject Preparation

1. Subject placement
   1. Throughout the entire experiment, seat subjects in a comfortable chair. Fix the head of the participant using a cast embracing the neck, ensuring a stable head position and avoiding any movements of the head relative the TMS coil.
   2. Place the right arm of the subjects in a custom-built arm rest to minimize movements of the wrist. Fix the subject's right index finger to a splint mounted to the arm of a robot. Align the axis of rotation of the robot arm with the metacarpophangeal joint of the right hand so that the joint centre matches the rotational centre of the robot.
2. Force recordings
   1. Measure the force applied by the subjects by a torquemeter mounted in the robot arm and measure the position of the robot arm (corresponding to the position of the index finger) by a potentiometer connected to the rotational axis of the robot ²².
3. Electromyography (EMG)
   1. Use a bipolar configuration of surface electrodes to measure electrophysiological responses elicited by TMS as well as muscular activation produced by the subjects.
      1. Before attaching the electrodes to the skin over the first dorsal interosseus muscle (FDI) and the abductor pollicis brevis (APB) of the right hand, shave the skin of the subjects, then slightly abrade it using sandpaper or abrading gel and disinfect it with propanol.
      2. Following this, attach self-adhesive EMG electrodes to the skin over the muscle bellies of the FDI and APB. Place an additional reference electrode on the olecranon of the same arm.
      3. Cable-connect all electrodes to an EMG amplifier and to an analogue-digital converter. Amplify the EMG signals (x 1,000), bandpass-filter (10 - 1,000 Hz) and sample at 4 kHz. Store the EMG signals for offline analysis.
4. TMS
   1. Use a figure of eight coil attached to a TMS stimulator to stimulate the contralateral motor cortical hand area.
   2. Find the optimal position of the coil relative to the scalp for eliciting motor evoked potentials (MEPs) in the FDI muscle by a mapping procedure:
      1. Place the coil approximately 0.5 cm anterior to the vertex and over the midline with the handle pointing at 45° anticlockwise relative to the sagittal plane, inducing a posterior-anterior flow of the current in the centre of the coil.
      2. At the beginning, choose a small stimulation (e.g., below 30% maximum stimulator output, MSO) intensity to get the subjects accustomed to the magnetic pulses.
      3. Subsequently, increase the stimulation intensity in small steps, for example 2 - 3% maximum stimulator output (MSO) and move the coil in the frontal-rostral and medio-lateral direction in order to find the optimal site (hotspot) for stimulating the FDI muscle. The hotspot is defined as the place where the greatest MEP can be observed at a given stimulation intensity.
   3. After finding the FDI hotspot, determine resting motor threshold (MT) as the minimum intensity required to evoke MEP peak-to-peak amplitudes in the EMG larger than 50 µV in three out of five consecutive trials ¹⁸. Inspect the size of the MEPs displayed online on the computer screen.
   4. After eliciting MEPs with 1.0*MT, constantly decrease the stimulation intensity of the TMS machine in steps of 2% MSO until the MEP can no longer be observed and an EMG suppression of the ongoing muscle activity becomes apparent.
      Note: In order to depict the TMS induced EMG suppression it is necessary to apply a high number of stimulations (see section 5. "Data Processing")

3. Feedback Presentation

1. Divide the participants into three groups (pF, fF, CON).
2. Instruct subjects from the position feedback group (pF) in half of the trials to receive feedback about the position of the index finger (position feedback) when moving the index finger by pressing against the robotic device.
3. In the other half of the trials, instruct subjects to receive feedback about the applied force while moving the robotic device (force feedback).
   Note: In reality, however, they always receive the same feedback (position feedback).
4. Instruct subjects from the force feedback group (fF) to receive force feedback in half of the trials and receive position feedback in the other half.
   Note: In fact, this group is solely provided with force feedback.
5. Do not instruct the control group (CON) about the source of the feedback. Note: The control group receives force feedback in one half of their trials and position feedback in the other half.
6. Randomly alter the order of the sessions, that is, whether trials start with force or position feedback, in all groups.
7. Visually display the force and the position feedback on a computer screen placed 1 m in front of the subjects.
8. In each condition, present a target line corresponding to 30% of the subject's individual maximal voluntary force, or the finger angle of the index finger at 30% maximally voluntary contraction (MVC), on the computer screen and instruct the subject to match the target line as closely as possible.

4. Maximal Isometric Force

1. After the subject is prepared (EMG), perform three isometric maximum voluntary contractions (MVC), consisting of a gradual increase in isometric force from zero to maximum over a 3 sec time span and the maximal force held for 2 sec ^20,21.
2. Verbally encourage the subject to achieve maximal force. After each trial, allow the subjects to rest for 90 sec to avoid fatigue.

5. Experimental Procedure

1. Fatiguing Motor Task- Sustained contractions.
   Note: The fatiguing task consists of two sustained contractions executed on separate days.
   1. Instruct the subjects to match the target line of 30% MVC for as long as possible with a line corresponding to the applied force or the position of their finger corresponding to a force level of 30% MVC.
      Note: The target line during the position feedback condition (pF-group) therefore corresponds to the finger angle when subjects match the force level of 30% MVC.
   2. Ask the subjects to hold the contractions until task failure, which is defined as the point where the subjects are no longer able to hold the target force inside a 5% window of the target force over a period of 5 sec (fF-group). For the pF-group, define task failure as when the participants are unable to maintain the finger angle within 5 % of the required target angle for 5 sec ^12,23.
   3. Ensure that the two sustained contractions are separated by at least 48 hr.
2. TMS-protocol
   Note: The subthreshold TMS experiment is carried out on separate day to the fatiguing contractions. This is important as fatigue has an influence on the EMG suppression evoked by subTMS ^24,25 so differences between force and position cannot be clearly identified. Separating the fatiguing contractions from the TMS measurements has the advantage that differences in the EMG suppression can now be clearly be attributed to the different interpretation of the feedback but has the limitation that the results can not directly be linked to the differences in the time to fatigue of the sustained contractions.
   1. Conduct the part of the experiment using TMS (see also section 3. "Feedback presentation") on a separate occasion than the fatiguing experiments. Initially, follow the exact same procedure as for the fatiguing contraction (e.g., MVC contractions) but this time, ask the subjects to hold the contractions only as long as the TMS stimulation lasts. Thus, the contractions are not fatigable and only held for approximately 100 sec during each TMS trial.
   2. Provide a break of 3 min between trials to minimize any bias of fatigue.

6. Data Processing

1. TMS
   1. Apply a total of 100 sweeps, 50 sweeps with and 50 sweeps without stimulation, with an inter-stimulus interval ranging from 0.8 to 1.1 s ^20,21,25,26. This short interstimulus interval makes sure that the subjects do not need to hold the contractions for too long so fatiguing effects can be minimized.
   2. To analyse if the TMS stimulation caused a facilitation (MEP) or an EMG suppression, subtract the rectified and then average 50 sweeps with stimulation (stimulated EMG) from the 50 sweeps without stimulation (control EMG) ^20,21,25-27.
      Note: The onset of the EMG suppression is defined as the time point where the averaged EMG for the sweeps with the stimulation is less than the control EMG for at least 4 msec in a time frame of 20 to 50 msec after the TMS pulse. The end of the suppression is defined as the instant when the stimulated EMG is greater than the control EMG for at least 1 msec and the extent of the suppression is calculated as percentage change (control-stimulated/mean_control*100).
   3. Use the sweeps without TMS stimulation for the calculation of the background EMG activation and average them over the same time window as the trials with stimulation ^20,21,25,26.
2. EMG
   1. Determine the maximal EMG activity by calculating the root-mean-square value recorded in a 0.5s time window around the peak force measured during the MVC tests ^20,21.
   2. For the sustained contractions, analyse the EMG by building 8 sec long bins where the root-mean-square of the rectified EMG is calculated and normalized to the EMG activity obtained during the MVC trials ^20,21.

Results

Interpretation of feedback

In procedure described here, subjects were instructed in a way that they believed in half of their trials to have received position feedback and in the other half of the trials to have received force feedback. In fact, they were tricked in half of their trials as they the pF-group always received position feedback and the fF-group always received force feedback.

Discussion

The present study investigated if the interpretation of augmented feedback influences the time to fatigue of a sustained submaximal contraction and the neural processing of the primary motor cortex. The results show that as soon as the participants interpreted the feedback as position feedback (compared to force feedback), the time to fatigue was significantly shorter and the inhibitory activity of the motor cortex (measured as the amount of EMG suppression caused by subTMS) is greater. As the task did not change between...

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
torquemeter	LCB 130, ME-Mebsysteme, Neuendorf, Germany		Part of robotic device built for force and position recordings
potentiometer	type 120574, Megatron, Putzbrunn, Germany		Part of robotic device built for force and position recordings
EMG electrodes	Blue sensor P, Ambu, Bad Nauheim, Germany
TMS coil	Magstim
TMS machine	Magstim Company Ltd., Whitland, UK
Recording software	Labview-Based		custom written software