Optimization model predictions for postural coordination ... - Research

equilibrium constraint. In conclusion, the optimization technique is well suited for the prediction of postural modes of coordination and seems to offer many ...
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Journal of Biomechanics 39 (2006) 170–176 www.elsevier.com/locate/jbiomech www.JBiomech.com

Optimization model predictions for postural coordination modes Luc Martina,, Violaine Cahoue¨ta, Myriam Ferrya, Florent Fouqueb a

b

Laboratoire Sport et Performance Motrice EA 597, UFRAPS Universite´ Joseph Fourier, 38041 Grenoble cedex 9, France Laboratoire Motricite´-Plasticite´ INSERM/ERIT-M 207, UFRSTAPS, Universite´ de Bourgogne BP 27877, 21078 Dijon, France Accepted 13 October 2004

Abstract This paper examines the ability of the dynamic optimization model to predict changes between in-phase and anti-phase postural modes of coordination and to evaluate influence of two particular environmental and intentional constraints on postural strategy. The task studied was based on an experimental paradigm that consisted in tracking a target motion with the head. An original optimal procedure was developed for cyclic problems to calculate hip and ankle angular trajectories during postural sway with a minimum torque change criterion. Optimization results give a good description of the sudden bifurcation phase between in-phase and anti-phase postural coordination modes in visual target tracking. Transition frequency and predicted effects of environmental and intentional constraints are also in line with experimental observations described in existing literature. In particular, these investigations pointed out that postural planning process can be related to the minimization of a dynamic cost criterion with an equilibrium constraint. In conclusion, the optimization technique is well suited for the prediction of postural modes of coordination and seems to offer many opportunities for better comprehension of neuromuscular movement control. r 2004 Elsevier Ltd. All rights reserved. Keywords: Dynamic optimization; Postural coordination; Trajectory planning; Minimum torque change criterion

1. Introduction A classic assumption on movement planning is that human beings perform a motion according to certain optimal criteria, i.e. movement control can be related to a problem of cost function minimization. Over the years, several researchers have used such optimization principles for different biomechanical motion predictions, for example, arm pointing (Uno et al., 1989; Alexander, 1997; Wada et al., 2001), manual lifting (Lin et al., 1999; Chang et al., 2001), pedaling (Kautz and Hull, 1995; Raasch et al., 1997) and walking (Anderson and Pandy, 2001). There are various approaches to investigating human planning strategies by which trajectories are selected depending on the choice of a cost functional. Some authors have suggested a planning strategy at a Corresponding author. Tel.: +33 3 76 63 50 83; fax: +33 3 76 51 44 69. E-mail address: [email protected] (L. Martin).

0021-9290/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2004.10.039

kinematic level with the minimum jerk model (Flash and Hogan, 1985). A more reliable approach, when comparing with experimental data, is to relate movement strategies to intrinsic parameters with a human body dynamics-based criterion. For example Uno et al. (1989) suggested that arm-pointing movements were organized such that the time integral of the square sum of muscular joint moment changes is minimal. Many other authors focused on joint moments since they are often associated with physical stress or metabolic energy (Kautz and Hull, 1995; Lin et al., 1999; Alexander, 1997). These models are objectively and experimentally examinable because of their quantitative predictions but none have been used to examine postural strategy in standing. Human stance requires the control of different body segments that can be organized in many ways. Nashner and McCollum (1985) have described two preferential postural strategies: hip and ankle strategies. In the first strategy, the body oscillates around the ankle joint

ARTICLE IN PRESS L. Martin et al. / Journal of Biomechanics 39 (2006) 170–176

whereas in the second, postural equilibrium is regulated by tilting the torso forward or backward. This definition is confusing because it is widely accepted that hip strategy may include ankle rotation and several studies have reported that hip rotation was often apparent in ankle strategy (Horack and Nashner, 1986; Nashner and McCollum, 1985). These observations suggested that it was not the involvement of these different joints that determined the type of postural organization adopted, but rather the way in which the movements of the different joints were coordinated. Accordingly, Bardy et al. (2002,1999) analyzed the relative phase (Frel ) between hips and ankles in standing participants who were stressed to track a visual target with the head. Participants were found to switch suddenly from inphase mode (the ankles and the hips moving simultaneously in the same direction, Frel close to 01) to antiphase mode (the ankles and hips rotating simultaneously in opposite directions, Frel close to 1801) as a result of constraints acting on the system. Newell (1986) distinguished three categories of constraints which influenced observed coordination modes: environmental constraints (i.e. support surface properties), intrinsic constraints (i.e. height of the center of mass, length of the feet) and intentional constraints (or task constraint, i.e. the instruction to track target motion). The aims of this paper are to investigate the ability of dynamic optimization model to predict in-phase and anti-phase postural modes of coordination and to evaluate influence of two particular environmental (length of support base) and intentional (amplitude of head displacement) constraints on postural strategy. The studied task was based on the experimental paradigm widely used in literature (Bardy et al., 2002; Oullier et al., 2002; Marin et al., 1999a) consisting in tracking a target motion with the head. An original optimal procedure was developed for cyclic problems to calculate hip and ankle angular trajectories during postural sway with a minimum torque change criterion.

2. Method 2.1. Biomechanical model During postural sway, the human body was modeled as a two-dimensional system comprising three rigid segments representing the feet (segment 0), the lower limbs (segment 1) and the upper part of the body (segment 2) which were linked by two articulations, ankle and hip joints (Fig. 1) modeled as frictionless hinges. The feet were assumed to remain at rest, in static contact with the floor. Assuming that the ligaments and bone-on-bone contact forces were negligible, the inverse dynamics of the body-system was used to expressed muscular net joint moments at ankle

171

.

G2

θ2

O2 G1 O1

ρ

y

d

θ1

x

O1

(a)

Xa

M1 Fy G0

Fx

CoP X CoP Xb

(b)

Fig. 1. Two-dimensional human body system (a) and mechanical characteristics of the feet (b).

and hip joints as a function of segmental kinematics at each time t: M 1 ¼ ðI 1 þ I 2 þ l 21 m2 þ 2m2 l 1 r2 cos y2 Þy€ 1 þ ðI 2 þ m2 l 1 r2 cos y2 Þy€ 2  ðm2 l 1 r2 sin y2 Þ 2  ðy_ 2 þ 2y_ 1 y_ 2 Þ þ gðm1 r1 cos y1

þ m2 ðl 1 cos y1 þ r2 cosðy1 þ y2 ÞÞÞ;

ð1Þ 2

M 2 ¼ ðI 2 þ m2 l 1 r2 cos y2 Þy€ 1 þ I 2 y€ 2 þ ðm2 l 1 r2 sin y2 Þy_ 1 þ gðm2 r2 cosðy1 þ y2 ÞÞ;

ð2Þ

where, for i ¼ 1; 2 : M i was the net muscular torque at joint i, yi ; y_ i and y€ i were respectively angular position, velocity and acceleration of joint i as defined in Fig. 1. For each segment i ¼ 1; 2 : l i and mi were, respectively, the length and the mass, Gi the center of mass, ri the distance between Gi and joint i and Ii, the moment of inertia with respect to the axis ðOi ; zÞ: The maintenance of balance during postural sway depends on the horizontal anterior–posterior position of the center of pressure (CoP), which can be expressed as a function of the body kinematics. The static equilibrium of the feet segment led to X CoP ¼

ðM 1  F x d þ m0 r0 gÞ ; Fy

(3)

where Fx and Fy were respectively horizontal and vertical ground reaction force components. As regards the body pluri-articulated system, Euler’s equations could relate Fx and Fy to the rate of change of the respective horizontal and vertical linear momenta of

ARTICLE IN PRESS L. Martin et al. / Journal of Biomechanics 39 (2006) 170–176

172

the whole system at each time t (Cahoue¨t et al., 2002): F y ¼ ðm1 r1 þ m2 l 1 Þ cos y1 y€ 1 þ m2 r2 cosðy1 þ y2 Þðy€ 1 þ y€ 2 Þ 2  ðm1 r1 þ m2 l 1 Þ sin y1 y_ 1  m2 r2 sinðy1 þ y2 Þðy_ 1 þ y_ 2 Þ2

þ ðm0 þ m1 þ m2 Þg;

ð4Þ

F x ¼  ðm1 r1 þ m2 l 1 Þ sin y1 y€ 1  m2 r2 sinðy1 þ y2 Þ 2

ðy€ 1 þ y€ 2 Þ  ðm1 r1 þ m2 l 1 Þ cos y1 y_ 1  m2 r2 cosðy1 þ y2 Þðy_ 1 þ y_ 2 Þ2 :

ð5Þ

Dt ¼

2.2.1. Minimum torque change criterion The optimization model assumed that the human body performed postural sway by minimizing time derivatives of net joint moments. Considering a steady-state cyclic two-joint movement, postural activity was formulated into a mathematical optimization problem with an objective function specifying the minimization of the sum of net torque changes:  ZT c  dM 21 dM 22 þ dt; dt dt

(6)

0

where Tc was the period of the movement corresponding to the period of the target motion. The task related to the studied movement was two-fold: first, the head had to move in phase with the target (frequency ¼ fT) and with the same amplitude aT and secondly, the bodysystem had to maintain balance. This could be expressed by adding constraints in the optimization search. The head amplitude displacement was imposed to equal target one      Tc l 1 cos y1  cosðy1 ð0ÞÞ 2        Tc Tc þ l 2 cos y1 þ y2  cosðy1 ð0Þ þ y2 ð0ÞÞ 2 2 ¼ aT :

ð7Þ

The other constraint imposed in the optimization search was the maintenance of balance during oscillation. To keep the CoP antero-posterior position (3) of the subject within the base of support and feet flat on the floor, the constraint could be expressed as X a pX CoP ðtÞpX b ;

2.2.2. Time discretization and angular trajectory models Discretizing the cycle time scale of the angular trajectories, the infinite dimensional of the minimization problem (6) was converted into a finite one:  n  X dM 21 dM 22 Cn ¼ ðti Þ þ ðti Þ Dt; (9) dt dt i¼1 where n was the number of discrete time ti and Dt was the time discretization step such that

2.2. Optimal calculation for hip and ankle angular trajectories

1 C¼ 2

The associated non-linear constrained optimization problem consisted in finding cyclic joint displacements yi¼1;2 such that criterion (6) was minimized and constraints (7) and (8) were satisfied.

(8)

where Xa and Xb were the boundary positions on the CoP in respectively backward and forward directions with respect to the ankle joint to prevent toe-off or heel-off.

Tc : ðn  1Þ

Considering that angular displacements in steady-state postural sway were cyclic time functions, they could be described by a N-harmonic Fourier series: yi ðtÞ ¼

N a0i X þ ðaki cosðko0 tÞ þ bki sinðko0 tÞÞ; 2 k¼1

(10)

where aki and bki were amplitude coefficients and the fundamental frequency o0 ¼ 2p=T c : Consequently, the optimization problem could be reformulated using (10) as follows: find the 2(2N+1) coefficients of the Fourier series representing y1 and y2 ; such that C n ða01 ; . . . ; aN1 ; b11 ; . . . ; bN1 ; a02 ; . . . ; aN2 ; b12 ; . . . ; bN2 Þ was minimal and (7) and (8) were respected. This non-linear constrained optimization was solved with the sequential quadratic programming (SQP) method (Boggs and Tolle, 1996) using Matlab (Math Works Natick, MA). 2.2.3. Input data values Specific input data values were chosen to perform simulations of postural sway during head tracking task. Typical male proportions were used to determine anthropometrical parameters (Paı¨ and Patton, 1997). According to experimental observations of postural sway movements (Marin et al., 1999a), the amplitude spectra of hip and ankle position data present very little activity above the second harmonic. Consequently, the number of harmonics in the Fourier series was set to N ¼ 3 in the optimization search. All simulations were performed with the same initial solution in the optimization search, where Fourier series’ coefficients (10) were set to zero. The periods of target oscillations were varied with an increment of 0.5 s between 5 s and 1 s (corresponding to frequencies of between 0.2 and 1.0 Hz) to examine hip and ankle coordination evolution. Focusing on the transition phase, the corresponding bifurcation frequency calculation was refined with a precision of 0.01 Hz.

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0.12 0.08 0.04 0

Ankle angle (rad)

1.54 1.52 1.5 1.48

Hip angle (rad)

The influence of environmental (length of support base) and intentional (amplitude of head displacement) constraints was investigated using three different amplitudes of target motion (0.07, 0.1, 0.13 m) and three distinct lengths of support base (0.07, 0.1, 0.13 m). For each trial, angular displacement and net muscular power were estimated at the hip and ankle joints. Net joint powers, calculated at each joint using scalar product between muscular net joint moment and angular velocity, demonstrated concentric muscular action when positive and eccentric muscular action when negative. Head motion, body center of gravity (CoG) and CoP displacements were also evaluated for each trial.

Head position (m)

L. Martin et al. / Journal of Biomechanics 39 (2006) 170–176

0.1

-0.1

(a)

0.5 Hz

0.3 Hz

3. Results 5 0 -5 -10

(b) Horizontal position (m)

Two distinct stable modes of coordination appeared in the predicted joint trajectories with increasing oscillation frequencies. Typical optimal results, corresponding to in-phase (f ¼ 0:3 Hz) and anti-phase (f ¼ 0:5 Hz) coordination patterns are illustrated in Fig. 2. In in-phase mode coordination, hip and ankle joints flexed in the first part of the cycle and extended simultaneously in the second one. Conversely, the antiphase mode was characterized by hip flexion and ankle extension in the first part of the cycle and by hip extension and ankle flexion in the last one. Net joint power time histories (Fig. 2b) exhibited one eccentric and one concentric muscular action at ankle joint, and two eccentric and two concentric muscular actions appeared at hip articulation regardless of the trial. At the ankle joint, the appearance chronology of distinct muscular actions was inverted between in-phase and anti-phase coordination modes, while it remained unchanged at the hip joint. Peak-to-peak CoG displacement along the antero-posterior axis (Fig. 2c) was greater at low frequency (0.3 Hz), and conversely, CoP oscillated with greater amplitude at the higher frequency (0.5 Hz). For both trials, CoG displacements presented lower amplitude than CoP displacements. The mean antero-posterior value of CoG position observed at 0.3 Hz was located in front of the one predicted at 0.5 Hz. The bifurcation frequency corresponding to a sudden transition between coordination modes was estimated at 0.41 Hz (Fig. 3b). In-phase coordination mode corresponding to relative phase equal to zero were observed for low target motion frequencies (0.2–0.4 Hz). An antiphase pattern of coordination was obtained for higher frequencies (0.42–1 Hz), where the coordination of the ankle was 1801 out of phase with respect to the hip joint. The simulation trend exhibited angular displacement amplitudes at ankle joint that were more reduced than at the hip, regardless of frequency (Fig. 3a).

Net joint power (W)

10

ankle 0.5 Hz

hip 0.5 Hz

ankle 0.3 Hz

hip 0.3 Hz

150

200

0.1

0.05

0 0

50

100 Cycles (%)

(c) CP 0.5 Hz

CG 0.5Hza

CP 0.3Hz

CG 0.3 Hz

Fig. 2. Two typical trials (aT ¼ 0:1 m) of in-phase (0.3 Hz) and antiphase (0.5 Hz) coordination modes: horizontal head position and ankle and hip angles (a), net joint power at hip and ankle joints (b) and CoG and CoP horizontal displacements (c) are plotted as a function of the cycle proportion.

During in-phase coordination and for increasing frequencies from 0.2 to 0.35 Hz, angular displacement amplitude decreased at hip joint, while it slightly increased at ankle joint. This trend was inverted at both articulations for higher frequencies ranging from 0.35 Hz to the bifurcation frequency. During anti-phase coordination, raising motion frequency resulted in an increase in angular displacement amplitude at both joints. The model predictions are sensitive to modified environmental and/or intentional constraints (Fig. 4). In general, observed transition frequency increased with increasing base of support length, and decreased as head

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Angular amplitude (rad)

174 Ankle

Hip

0.3

0.4

0.8 0.6 0.4 0.2 0

(a)

Relative phase (°)

180

0 0.1

0.2

(b)

0.5

0.6

0.7

0.8

0.9

1

Frequencies (Hz)

Bifurcation frequency (Hz)

Fig. 3. Evolution of (a) hip and ankle angular motion amplitude and (b) relative phase evolutions with head motion frequencies increasing from 0.2 to 1.0 Hz. Bifurcation frequency (0.41 Hz) is marked with a vertical dotted line. These simulations were conducted with parameters values of base of support and head motion amplitude both set at 0.1 m.

0.5

0.3

0.1 0.05

0.07

0.09

0.11

0.13

0.15

Base of support (m) Head motion amplitude

(0.07 m)

(0.1m)

(0.13 m)

Fig. 4. Bifurcation frequencies plotted as a function of base support length and head motion amplitude.

motion amplitude was extended, except for a single trial corresponding to a base of support length of 0.13 m and a head displacement amplitude of 0.07 m.

4. Discussion The constrained optimization model we have developed, provided realistic predictions of postural sway movements during head tracking task. Considering the formulation of the optimization problem, the chosen criterion, which involves a dynamic planning control (Uno et al., 1989) satisfactorily reproduced postural experimental observations. More precisely, the use of minimum torque change criterion to

predict cyclic postural sway movements, which are of low metabolic cost, was adequate. The formulation of the criterion suggests that the planning strategy can be related to some extent, to the minimization of the central motor command variations. Therefore, this criterion, combined with a pertinent equilibrium constraint, may provide suitable predictions of all postural tasks, while associated energy expenditure remains restrained. Traditionally, joint angular velocities and accelerations are expressed as a function of angular positions using a finite difference method (Chang et al., 2001). This method is convenient but can lead to unrealistic predictions because it does not ensure that angular kinematics are continuously differentiable functions. Some alternatives are to use spline curves (Lo and Metaxas, 1999) or polynomial approximations (Wada et al., 2001; Lin et al., 1999) for angular displacements. Considering that angular displacements in steady-state postural sway are cyclic time functions, the use of Fourier series to approximate joint angular trajectory is convenient because it ensures that angular positions and velocities are continuously differentiable functions. Furthermore, it avoids enforcing supplementary constraints to ensure periodic displacements and allows better convergence of the optimization process. This study has proved the ability of the optimization model to predict two different modes of coordination in postural sway for varying frequencies with a sudden transition phase. We calculated an in-phase coordination between hip and ankle joints for low motion frequencies and anti-phase coordination for higher frequencies. These results are consistent with observations related to similar experimental paradigms, i.e. head tracking, found in existing literature (Bardy et al., 2002; Marin et al., 1999a,b; Oullier et al., 2002). Examining the optimization process, it appears that the sudden bifurcation emerges from both equilibrium constraint and cost minimization. For low frequencies (below 0.35 Hz), the predicted CoP displacement which minimizes the cost functional is naturally inside base of support boundaries and equilibrium constraint is not active in the optimization search. The predicted in-phase coordination is the less expensive strategy with regard to the chosen criterion. Increasing oscillation frequency leads to augmented CoP displacement amplitude, which imperils balance. Consequently, the equilibrium constraint becomes active in the minimization search. In these conditions, optimal process do not predict the less expensive strategy but the one that can ensure equilibrium conditions while minimizing the cost functional. The activation of equilibrium constraint in the optimal search also leads to a modification in angular amplitude evolution at hip and ankle joint, as observed in Fig. 3 for frequency values comprised between 0.35 Hz and bifurcation frequency. For frequencies above 0.41 Hz, anti-phase coordination mode appears because, in these

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conditions, balance cannot be maintained anymore using in-phase strategy. Observation of typical trials of in-phase and antiphase coordination modes (Fig. 2b) showed that the four-component pattern of net muscular power present at hip joint was maintained in each mode of coordination. As regards the ankle joint, the observed bi-phasic muscular action pattern was inverted between in-phase mode (eccentric followed by concentric actions) and anti-phase mode (concentric followed by eccentric actions). Consequently, the ankle extensor group remained agonist for the whole flexion and extension motion, regardless of the coordination mode. These observations are strongly dependant on the base of support characteristic values used in the model and have to be confirmed by further experiments. For all studied target velocities, CoP displacements remained in phase with respect to CoG movement. This trend has already been widely observed in quiet standing (Winter et al., 1998). The optimal process also predicted opposite influence of motion velocity on CoP and CoG displacement amplitudes. Peak-to-peak CoG oscillations were reduced as head motion frequency was increased (Fig. 2c). This result is in accordance with those obtained by Pozzo et al. (2002) during whole body pointing movements for different execution velocities. The sensitivity of the predictive model to modified environmental and intentional constraints was explored by manipulating the value of the length of the support base and the amplitude of the head motion. In general, increased base support length resulted in increased bifurcation frequency estimates (Fig. 4). This result is in accordance with the experimental tendency described by Marin et al. (1999a). The optimal model also predicted decreasing transition frequency for increased head motion amplitude (Fig. 4). This tendency is qualitatively in line with the experimental observations of Marin et al. (1999b); for a given motion frequency, in-phase coordination mode measured with a small target motion amplitude was changed into anti-phase coordination with larger amplitude. It can be observed in Fig. 4 that results from a single trial, corresponding to a support length of 0.13 m and head motion amplitude of 0.07 m, were inconsistent with these general tendencies. For this trial, the optimal model predicted exaggerated trunk bending. This does not correspond to a realistic position that can be observed in this kind of visual target tracking experimental paradigm and can be explained by the fact that only horizontal head displacements were constrained in the optimal search. Adding some constraints in the optimal process to better express intentional constraint and limit head vertical motion should improve the reproduction of the experimental task. In general, this study brings to light the role of the CoP position, which seems to be of crucial importance in the postural coordination planning. Indeed, it appears

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from our results that this parameter is of prime importance in the modification of the postural strategy. Moreover, since pressure receptors are located under the feet, proprioceptive information reflecting CoP position can be directly available to the system and, hence, involved in the motor command elaboration. In conclusion, the study has proved that the optimization technique is well suited for the prediction of postural coordination. The original formulation developed for cyclic angular displacement is efficient and could be successfully applied to the simulation of all periodic tasks such as pedaling or walking. In general, these investigations pointed out that postural planning process can be related to a dynamic cost criterion minimization coupled with an equilibrium constraint expressed by confining CoP displacement. Particularly, optimal predictions are consistent with the hypothesis that multi-segment coordination in postural control emerges from interactions between constraints imposed by the support surface and those imposed by the task. Possibilities for future studies include the examination of the influence of modified intrinsic constraints (as limited moment strength) on coordination modes and the simulation of other postural tasks, i.e. postural perturbation effect observations (Runge et al., 1999) or oscillating plate-form paradigm (Buchanan and Horak, 1999; Corna et al., 1999; Ko et al., 2001). The optimization model approach also seems to offer opportunities to allow a better comprehension of neuromuscular movement control.

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