1Department of Biomedical Engineering, Oregon Health and Science University, 2UCL Institute of Neurology, Queen Square, 3Department of Neurology, Oregon Health and Science University
Gurfinkel, V. S., Cacciatore, T. W., Cordo, P. J., Horak, F. B. Method to Measure Tone of Axial and Proximal Muscle. J. Vis. Exp. (58), e3677, doi:10.3791/3677 (2011).
The control of tonic muscular activity remains poorly understood. While abnormal tone is commonly assessed clinically by measuring the passive resistance of relaxed limbs1, no systems are available to study tonic muscle control in a natural, active state of antigravity support. We have developed a device (Twister) to study tonic regulation of axial and proximal muscles during active postural maintenance (i.e. postural tone). Twister rotates axial body regions relative to each other about the vertical axis during stance, so as to twist the neck, trunk or hip regions. This twisting imposes length changes on axial muscles without changing the body's relationship to gravity. Because Twister does not provide postural support, tone must be regulated to counteract gravitational torques. We quantify this tonic regulation by the restive torque to twisting, which reflects the state of all muscles undergoing length changes, as well as by electromyography of relevant muscles. Because tone is characterized by long-lasting low-level muscle activity, tonic control is studied with slow movements that produce "tonic" changes in muscle length, without evoking fast "phasic" responses. Twister can be reconfigured to study various aspects of muscle tone, such as co-contraction, tonic modulation to postural changes, tonic interactions across body segments, as well as perceptual thresholds to slow axial rotation. Twister can also be used to provide a quantitative measurement of the effects of disease on axial and proximal postural tone and assess the efficacy of intervention.
Twister is a servo-controlled device for quantifying postural tone in axial and proximal body regions during active, upright stance. The original device was constructed at Oregon Health & Science University and a similar device is under construction for the University of Southampton, UK. In this report, we describe the function and rationale for Twister and its various uses. We then provide a detailed description to facilitate its reproduction and show how it can be used to investigate the control of postural tone.
Twister consists of a rigid steel frame, rotating platform, torque sensor, counterbalanced suspension system, upper and lower fixations, and body attachments (Fig 1), as well as a servo control system for regulating platform rotation. Twister quantifies postural tone in standing subjects by rotating lower body segments about the vertical axis relative to upper segments. This twists the region in between, changing the length of muscles within. Upper and lower fixations can be attached to impart twisting to the neck, trunk or hip regions (Fig 2). Because Twister does not provide postural support, tonic activity of skeletal muscle is necessary to counteract gravitational torques. This tonic regulation is studied by the torsional resistance to twisting as well as electromyography from relevant muscles. Resistance to twisting is assessed by a torque sensor within the upper fixation and reflects the state of all muscles undergoing length changes. Twister uses several different platform rotation profiles to study tonic control, including a triangle profile, step profile, and triangle profile of increasing magnitude (Fig 3). These rotate the platform at a constant slow velocity, which minimizes inertial effects on the subject and measurement.
We use a twisting perturbation about the vertical axis because it: 1) changes the length of axial and proximal muscles, as these structures are oriented obliquely and have broad anatomic origins and insertions; 2) does not alter the relationship of the whole body and its parts to gravity; 3) rotates the body around an axis of minimal moment of inertia2; 4) corresponds to a neutral zone3,4, so that resistance from small displacements from the forward facing position reflects muscular rather than osteo-ligamentous forces; and 5) naturally occurs in everyday activities3,5.
Twister is a flexible device that can be used to address various aspects of tonic control. These include: 1) stiffness related to tonic activity6-8; 2) tonic responses to muscular length changes6,8. 3) the effect of twisting on remote body regions; 4) tonic effects from kinesthetic information9; 5) the effects of disease on postural tone7,10; and 6) perceptual thresholds to slow rotation11.
3. Detailed description of device
We detail the components of Twister below.
4. Experimental protocol
A typical experimental is run as follows:
5. Representative results
Resistive torque typically increases with platform excursion, however the increase slows with larger excursion. Overall resistance is typically quantified by peak-to-peak torque, averaged across cycles. Fig 5A shows single trial responses across subjects for torsional resistance of constant speed ramp for the trunk. We have observed data reproducible over months within a subject (Fig 5B; interclass correlation coefficient = 0.89). Mean resistance to twisting differs across body segments, and has been reported to be 0.54 ± 0.24 Nm for the neck, 5.11 ± 1.94 Nm for the trunk and 3.23 ± 1.67 Nm for the hips6 (Fig 6). It is important that platform rotation is smooth and there is no lash. Absence of lash is indicated by smooth changes in torque during directional changes and a rapid change in torque at the onset, presumably due to short-range stiffness of muscle (see Fig 3A in Gurfinkel et al.6).
The measured torque reflects both the dynamic changes in tone with twisting as well as the distribution of baseline tonic activity (which includes co-contraction). Because of the slow speed of twisting, the increase in torque per degree is equivalent to intrinsic stiffness12 only when muscle activity is constant. Note that because active structures contribute to the measured resistance Twister technically assesses pseudostiffness.
In general, two types of responses are observed that correspond to constant or modulated tonic activity within the twisted region. The former is characterized by low cycle-to-cycle variation in torque, high peak-to-peak torque magnitude, and relatively constant EMG. In contrast, dynamic modulation is characterized by high cycle-to-cycle variability, low torsional resistance and EMG modulation coherent with twisting. On angle vs. torque plots unmodulated subjects exhibit a regular hysteresis loop while modulated subjects have an irregular pattern that can reverse direction (see Fig 3A in Gurfinkel et al.6 Dynamic modulation generally consists of increasing tonic activity during muscle shortening and decreasing activity during lengthening (i.e. Sherrington's lengthening and shortening reactions13), which are opposite in sign to the stretch reflex. An integrative measure of the extent of modulation can be obtained by the shift in a subject's neutral (zero-torque) position within a cycle, referred to as torque phase advance6,8.
Figure 1. Schematic of Twister from the side. Components are labeled as follows: 1) rotating platform; 2) telescoping bar for lower fixation; 3) hinge joint between lower telescoping bar and rotating platform; 4) helmet attached to upper fixation; 5) torque sensor and counterbalanced suspension system; 6) locking vertical linear bearing; 7) external fixation for measuring induced torque; 8) hinge joint analogous to 3; 9) rigid frame; 10) diagonal cross bracing for rigid frame.
Figure 2. Twisting applied to axial and proximal levels. Subjects stand on a rotating platform (yellow) with upper and lower body attachments affixed to impart twisting to the desired body region. The upper attachment is connected via a suspension system (zigzag lines) to the torque sensor (T), which is fixed with regard to rotation around the vertical axis. The lower attachment connects to the rotating platform via a hinge joint (black circle) that allows rotation in the sagittal plane of the subject. A: Neck twisting is achieved by attaching a helmet to the torque sensor and the shoulders to the platform. B: Trunk twisting is achieved by attaching the shoulders to the torque sensor and the pelvis to the platform. C: Hip twisting is achieved by attaching the pelvis to the torque sensor.
Figure 3. Different twisting profiles. Various profiles can be used to study specific aspects of tonic control. The output of the optical encoder specifying platform rotation is shown in Volts. Upward deflection corresponds to counter-clockwise platform rotation when viewed from above. 1) Triangle profile: In this case the rotational velocity, maximum excursion and number of cycles are specified. Two cycles of 12° are shown. 2) Discontinuous, step profile: Amplitude, velocity, and holding time a step are specified. Two cycles 12° rotations, consisting of four, 3° deg steps are shown. 3) Increasing amplitude triangle waves: two cycles of each of 3°, 6° and 9° rotations are shown. In this example the rate of platform rotation is constant for all conditions.
Figure 4. Photograph of Twister from the side. A: Configuration for trunk twisting with components labeled as follows: 1) rotating platform; 2) motor and servo-control assembly; 3) hinge joint between lower telescoping bar and the rotating platform; 4) lower fixation and pelvis orthotic; 5) upper fixation and shoulder harness; 6) bar connecting suspension to upper fixation; 7) torque sensor and counterbalanced suspension system; 8) external fixation for measuring induced torque; 9) rigid frame. B: Closeup of torque sensor and suspension system labeled as follows: 1) torque sensor; 2-5) lightweight hinged aluminum plates. The hinge between plates 2 and 3 rotates about the anterior-posterior axis, while the hinge between plates 4 and 5 is oriented around the mediolateral axis. 8) locking vertical linear bearing; 9) lightweight helmet and upper attachment. C: Configuration for twisting the trunk but measuring the torsional effect on the neck. In this configuration the pelvis is fixed to the rotating platform (1) and the shoulders are connected to the external fixation (2), which prevents the shoulders, neck and head from rotating, restricting twisting to the trunk. The head is also attached to the upper fixation (3) so that any induced neck torque is applied to the torque sensor.
Figure 5. Torsional resistance of the trunk. A) Torque traces from individual trials from different subjects. Three cycles of 10°, 1°/s triangle waves were used. Subjects have consistent torque behavior across cycles, with large variation in resistance between subjects. Traces with highest resistance are typical of unmodulated behavior, while traces with least resistance are typical of high modulation. B) Inter-subject repeatability in torsional resistance across time. Two measurements from 7 subjects separated by one month. Peak-to-peak trunk torque shows consistent within-subject behavior across testing sessions but wide inter-subject variation.
Figure 6. Restive torque from different axial levels. The resistive torque to 10°, 1°/s triangle waves for the neck, trunk and hip levels. Single trials from a representative subject are shown. Note the different magnitude and timecorse across levels.
Figure 7. Schematic of servo-control. The control loop consists of a PID (proportional, integral, derivative) controller, which receives input from an optical encoder attached to the platform shaft. The controller determines the motor drive current. Custom software running on a PC is used for selecting the desired platform trajectory, which then downloads this information to the controller.
It is our opinion that Twister can be used address many questions in tonic control. To date, Twister has lead to 7 such publications6-11,14. Probably the most important feature of Twister is that it provides an integrated, kinetic measure of tone. This torque measure of tone is not provided by kinematic, inverse dynamics or electromyographic approaches, and is necessary to answer many questions regarding tone. Also, Twister is unique in not substantially interfering with natural antigravity or postural behavior, and provides a tonic, rather than a phasic perturbation.
One potential use of twister is the quantification of the tonic effects of disease on postural tone. While the intrinsic and reflex stiffness has been well studied for many neurological and musculoskeletal conditions using fast perturbations, the quantitative effect of many diseases on postural tone not well characterized. In particular, Twister can be used to quantify the effects of disorders such as rigidity7,10,14, hypotonia, dystonia, and back and neck pain on the magnitude, distribution and symmetry of postural tone along the body axis. It can also be used to measure axial kinesthesis, eg; perception of body rotation based on muscle proprioceptors and11 perceptuomotor symmetry, eg; representation of straight ahead during axial twisting14. Finally, Twister can be used to study the effect of intervention on these measures of axial postural tone8.
We estimate the cost of hiring an engineering firm to fabricate Twister is approximately $30,000 US. This device can likely be manufactured in-house for a fraction of this cost, as the price of raw materials is low, but significant fabrication is required. Throughout its use, Twister has evolved significantly and continues to do so. There are many basic questions that can be addressed with Twister. We hope that this report will help other investigators build Twisting devices or otherwise stimulate research into this fundamental but poorly understood area.
The authors have nothing to disclose.
We would like to thank Eugene Gurfinkel and Mark Chapman for their roles in the design and fabrication of Twister. The development of Twister was funded by National Institutes of Health grants R01 AR-31017 to P. Cordo and V. Gurfinkel and F32 HD-008520 to T. Cacciatore. T. Cacciatore would also like to acknowledge the Medical Research Council, UK for support to write this manuscript.