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Direction-dependent neck and trunk postural reactions during sitting
Journal of Electromyography and Kinesiology 21 (2011) 904–912
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Direction-dependent neck and trunk postural reactions during sitting Nancy St-Onge a,b,c,⇑, Julie N. Côté c,d, Richard A. Preuss b,e, Isabelle Patenaude c,d, Joyce Fung c,e a
Department of Exercise Science, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, Canada H4B 1R6 Constance-Lethbridge Rehabilitation Center, Montreal Center for Interdisciplinary Research in Rehabilitation (CRIR), 7005 Maisonneuve W., Montreal, QC, Canada H4B 1T3 c Feil & Oberfeld/CRIR Research Centre, Jewish Rehabilitation Hospital, 3205 Place Alton Goldbloom, Laval, QC, Canada H7V 1R2 d Department of Kinesiology and Physical Education, McGill University, 475 Pine Avenue West, Montreal, QC, Canada H2W 1S4 e School of Physical and Occupational Therapy, McGill University, 3654 Promenade Sir William Osler, Montreal, QC, Canada H3G 1Y5 b
a r t i c l e
i n f o
Article history: Received 29 October 2010 Received in revised form 27 July 2011 Accepted 27 July 2011
Keywords: Postural reactions Muscle activity Kinematics Kinetics
a b s t r a c t Postural reactions in healthy individuals in the seated position have previously been described and have been shown to depend on the direction of the perturbation; however the neck response following forward and backward translations has not been compared. The overall objective of the present study was to compare neck and trunk kinematic, kinetic and electromyographic (EMG) stabilization patterns of seated healthy individuals to forward and backward translations. Ten healthy individuals, seated on a chair fixed onto a movable platform, were exposed to forward and backward translations (distance = 0.15 m, peak acceleration = 1.2 m/s2). The head and trunk kinematics as well as the EMG activity of 16 neck and trunk muscles were recorded. Neck and trunk angular displacements were computed in the sagittal plane. The centers of mass (COMs) of the head (HEAD), upper thorax (UPTX), lower thorax (LOWTX) and abdomen (ABDO) segments were also computed. Moments of force at the C7-T1 and L5S1 levels were calculated using a top-down, inverse dynamics approach. Forward translations provoked greater overall COM peak displacements. The first peak of moment of force was also reached earlier following forward translations which may have played a role in preventing the trunk from leaning backwards. These responses can be explained by the higher postural threat imposed by a forward translation. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction Human postural stabilization strategies can be investigated using mechanical perturbation protocols, which are typically performed by inducing sudden displacements of the support surface on which a person stands or sits. Many investigators have studied the effects of support surface perturbations in standing healthy participants to describe the actions of the postural control system in maintaining postural stability (Diener et al., 1988; Henry et al., 1998a,b, 2001; Horak and Nashner, 1986; Nashner, 1983; Runge et al., 1999). For instance, in response to support surface translations in different directions, stereotypical patterns have been shown to occur in the leg and trunk muscles to restore postural stability. One of these patterns is characterized by activation of muscles in a distal-to-proximal progression. Henry et al. (1998a,b) have shown some muscle responses to be direction-specific and organized in synergies, suggesting that muscles are not necessarily activated when stretched but when functionally relevant in maintaining standing equilibrium. Although ⇑ Corresponding author at: Department of Exercise Science, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, Canada H4B 1R6. Tel.: +1 514 848 2424x5805; fax: +1 514 848 8681. E-mail address: [email protected] (N. St-Onge). 1050-6411/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2011.07.016
the direction of perturbation did not affect the distal-to-proximal progression of body segment movement, responses to anterior translations resulted in smaller movements of the trunk and larger displacements of the thigh in comparison to posterior and lateral translations. The direction of the perturbation was also shown not to affect peak COM displacement; however, the difference between center of pressure and COM peak displacements was larger for lateral than for forward and backward translations, suggesting greater postural instability in this direction following the same perturbation. Other studies have characterized the response patterns to perturbations in seated individuals (Blouin et al., 2003; Brault et al., 2000; Forssberg and Hirschfeld, 1994; Keshner, 2003; Preuss and Fung, 2008; Siegmund et al., 2002, 2003a,b; Vibert et al., 2001; Zedka et al., 1998). In general, studies on seated postural perturbations have consistently identified that trunk and neck muscles are activated when they are stretched. Similar to perturbations in the standing position, perturbations in the sitting position have been shown to produce a caudo-cranial progression of body segment movement (Côté et al., 2009; Forssberg and Hirschfeld, 1994; Keshner, 2003; Vibert et al., 2001). Postural responses have also been reported to be direction-specific in the sitting position (Preuss and Fung, 2008; Vibert et al., 2001). For example, although the amplitude of the head, arms and trunk COM displacement was
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smaller following antero-posterior perturbations as compared to lateral perturbations, the caudo-cranial delay in the progression of trunk segment COMs was shown to be more evident with anterior–posterior perturbations than with lateral perturbations (Preuss and Fung, 2008). Although postural reactions in healthy individuals in the seated position have previously been described and have been shown to depend on the direction of the perturbation, the neck response following forward and backward translations has not been compared. Preuss and Fung (2008) studied several directions but have not reported the neck angular displacements or the response of neck musculature. They also did not compare the effect of forward and backward translations on the timing of postural reactions. Vibert et al. (2001) studied the response of the trunk and the neck; however, they compared antero-posterior perturbations to lateral perturbations but did not compare perturbations in the same plane (i.e., forward vs. backward perturbations). The objectives of the present study were thus to characterize neck and trunk kinematic, kinetic and EMG stabilization patterns of seated healthy individuals; and to compare these stabilization patterns between forward and backward translations.
2. Methods 2.1. Participants A group of ten healthy individuals aged 21–46 years (five women, five men; body mass: 55–88 kg; body height: 157– 184.5 cm) participated in this study. Participants previously diagnosed with any neck or back, musculoskeletal or neurological problems were excluded. Participants signed an informed consent form approved by the institutional ethics committee before participating in the study. 2.2. Experimental protocol Participants sat on an experimental chair equipped with lateral support frames for the pelvis and the knees (Preuss and Fung, 2008, Fig. 1). The chair design served to standardize the hip and knee angles. A seat belt was buckled around the thighs to stabilize the legs; the trunk was free to move in all planes. The chair was fixed to a platform servo-controlled by electrohydraulic actuators. The participants were instructed to cross their arms on their torso, keep their eyes open, look ahead and stay relaxed throughout trials. Three static trials were first recorded (3 s each). Participants were then subjected to a randomized sequence of a total of 15 trials (five forward, five backward and five unperturbed trials). The perturbation parameters (distance = 0.15 m, peak velocity = 0.3 m/s, peak acceleration = 1.2 m/s2) were selected from a previous study that aimed at determining the lowest intensity translation to elicit a postural stabilization reaction (St-Onge et al., 2009). The total duration of the perturbation including the acceleration and deceleration phases was 1.5 s. Participants were informed prior to each trial (‘‘Ready? One, two, three, go!’’); however they were not told if the trial would be forward, backward, or static. After the perturbation sequence, three static trials were recorded. 2.3. Data acquisition Motion of the platform, head, arms and trunk was recorded (sampling frequency = 120 Hz) using a six-camera Vicon 512 Motion Analysis System (Vicon Peak, UK). Passive reflective markers were placed on 25 anatomical landmarks (see Fig. 1) and on each corner of the movable platform. To allow the computation of the
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COMs, anthropometric measurements were taken: trunk depth at T1, T4, T10, and L3 levels; body height and body mass. The EMG activity of 16 muscles of the neck and trunk were acquired (sampling frequency = 1800 Hz) using the Telemyo 900 EMG system (Noraxon, USA). After preparing the skin following standard procedures, bipolar surface Ag/AgCl electrodes (Ambu, DE) were placed on the skin overlying the right and left scalenus (SCA), sternocleidomastoid (SCM), cervical paraspinals (CP), upper trapezius (UT), erector spinae (thoracic level; TES), erector spinae (lumbar level; LES), rectus abdominis (RA), and external obliques (EO). A ground electrode was placed on the greater tubercle of the humerus. Electrode placement is defined in Table 1. 2.4. Data analysis Kinematic data were low-pass filtered (zero-phase lag fourth order Butterworth filter, 6 Hz). The head segment was defined using the four head markers and the trunk segment was defined using markers on S1 and both left and right T1 transverse processes. Trunk angular displacements were computed by quantifying the orientation of the trunk segment relative to the global space using Euler xyz rotations. Neck angular displacements were computed as the orientation of the head segment relative to a segment defined using the markers on the sternal notch and both left and right T1 transverse processes using Euler yxz rotations, therefore representing the position of the head relative to the base of the neck. The COMs of the head, upper thorax (T1-T6, including the arms), lower thorax (T6-L1) and abdomen (L1-S1) segments were computed using segmental measurements and standard anthropometric tables (de Leva, 1996; Pearsall et al., 1996). Platform displacement was computed by averaging the position of the four markers positioned on its corners. Platform onset was taken as the time when the velocity of its center surpassed 2% of its maximal velocity, while angle and COM onsets were identified as the time when their velocities first surpassed 5% of the respective maximum velocities. At the neck level, some participants displayed a small movement in the opposite direction in the beginning before moving in the main direction. For example, although in response to forward translations the main motion of the neck was in extension, some participants displayed a small amount of flexion before moving into extension. To allow for more consistency, the onset of motion was selected in the direction for which most of the displacement occurred. Amplitude of the first peak angle and time to first peak angle were also computed for neck and trunk. The peak COM displacement (maximum position reached from beginning to end of motion – initial position) was computed for each segmental COM. Kinematic onsets and timeto-peak angle were reported relative to platform onset. Estimates of the net moments of force at the neck (C7-T1) and trunk (L5-S1) levels were calculated using a linked segment model, assuming segment rigidity. The position of the C7-T1 and L5-S1 joint centers, and the resulting segment kinematics (head and trunk, including arms), were derived from the kinematic model described above. A 3-dimensional, top-down, inverse dynamics approach (Kingma et al., 1996) was used to estimate the net moments of force, using anthropometric variables adapted from de Leva (1996) and Pearsall et al. (1996), similar to the approach described by Preuss and Fung (2008). Results were low-pass filtered at 2.5 Hz using a zero-phase lag 2nd order Butterworth filter. A lower filter frequency (2.5 Hz vs. 6 Hz) was used for the inverse dynamic model because the velocity and acceleration of the segments is needed for these calculations. Any high frequency noise in the position data produces large spikes in the derivatives (rapid change in slope), which can amplify this noise in the results of the kinetic analysis. This may obscure the true data, and make interpretation of the findings difficult. The frequency was chosen based
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Fig. 1. Reflective markers were placed on the following anatomical landmarks: left and right front head, left and right back head, C7 spinous process, right scapula, left and right T1 transverse processes, T6 spinous process, left and right T8 transverse processes, T12 spinous process, left and right L1 transverse processes, S1, left and right posterosuperior iliac spines, apex of sacrum, sternal notch, left and right acromia, left and right lateral epicondyles, left and right head of third metacarpals.
Table 1 Electrode placement. Muscle
Electrode position
SCA SCM CP UT TES LES RA EO
Just above the clavicle, posterior to the SCM and anterior to the UT Halfway between the mastoid process and the sternal notch At the level of C4, 2 cm from the midline Halfway between C7 and the acromion At the level of T9, 3 cm from the midline At the level of L3, 3 cm from the midline 3 cm lateral to the umbilicus 8–12 cm lateral to the umbilicus
on the findings from Moorhouse and Granata (2005). This study found the natural frequency of the trunk following perturbation to be below 2 Hz. As such, the 2.5-Hz cutoff is unlikely to eliminate any relevant data from the kinematics. Kinetic onsets were identified as the time when their first derivatives first surpassed 5% of the respective maximum velocities. Time to first peak was also computed. Onsets and time-to-peak are reported relative to platform onset. The EMG signals were first amplified (2000). For each EMG signal, any contamination by the electrocardiogram was removed by first visually defining the initiation and end of a heartbeat. The selected heartbeat was then filtered out from the EMG signal using a 40-Hz low-pass 2nd order Butterworth filter on the part of the signal where it occurred. The beginning of all heartbeats was visually defined and the filtered-out heartbeat was subsequently subtracted from the EMG signal at every position where a heartbeat was defined. Signals were then band-pass filtered (zero-phase lag 4th order Butterworth filter, 10–350 Hz) and fullwave rectified. The mean and the standard deviation (SD) of each baseline EMG signal were calculated using the data from 300 to 100 ms before platform onset. EMG envelopes were then computed using a 20-Hz zero-phase lag 4th order Butterworth lowpass filter. The first burst that surpassed two SDs above the
baseline mean for at least 25 ms was detected on each EMG envelope. The onset of the EMG burst was identified by following the signal back until the point when the signal decreased under the baseline mean. EMG onsets are reported relative to platform onset. All analyses were performed using Matlab (The MathWorks Inc., Natick, MA, USA).
2.5. Statistical analysis Trials with missing markers which made points of interest (onsets, peaks, ..) not available were discarded. Data were first averaged over trials for each participant when at least three trials were available. For COM variables (onset, peak), kinematic variables (onset, time-to-peak, and amplitude), and kinetic variable (onset, time-to-peak) the data were analyzed using a two-way repeated-measures analysis of variance (ANOVA) with two within factors: direction (forward, backward) and segment (angles: neck and trunk; COMs: head, upper thorax, lower thorax and abdomen). When a significant main effect or interaction was found, post hoc analyses were performed using Tukey tests of comparisons. All statistical tests were performed using Statistica, v. 7 (Statsoft, Tulsa, OK, USA) and statistical significance was set at p < 0.05.
3. Results 3.1. Kinematics Fig. 2 displays the angular displacement sequence following forward and backward perturbations. For forward translations, the neck first moved in flexion in most participants, but motion reversed to extension and most of the displacement occurred in extension. The trunk first moved into extension and then reversed into flexion. The opposite pattern was observed following backward translations. The average neck and trunk angle onsets, times
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Fig. 2. Neck (upper panels) and trunk (lower panels) angular flexion (+)/extension ( ) following forward (left panels) and backward (right panels) perturbations. Thick lines: group means; thin lines: one standard deviation above and below means; dashed lines: platform motion. Vertical lines mark onsets (dashed) and time-to-peak (solid).
to the first peak angle, and amplitude of first peak are displayed in Fig. 3. For angle onsets, there was a significant segment effect (F(1, 7) = 1147.7, p < 0.001), with onsets occurring earlier for the trunk (96 ms) than for the neck (596 ms). No significant direction or interaction effect was observed (direction: F(1, 7) = 0.1, p = 0.794; interaction: F(1, 7) = 0.003, p = 0.955). For the time to the first peak angle (extension for forward perturbations, flexion for backward perturbations), there was also a significant effect of segment (F(1,7) = 49.1, p < 0.001) with peak angle occurring earlier for the trunk (711 ms) compared to the neck (1099 ms), and no significant direction or interaction effect (direction: F(1, 7) = 3.0, p = 0.126; interaction: F(1, 7) = 0.1, p = 0.724). For the amplitude of the first peak, there was no segment, direction, or interaction effect
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(segment: F(1, 6) = 0.6, p = 0.475; direction: F(1, 6) = 1.7, p = 0.245; interaction: F(1,6) = 5.7, p = 0.055). Both perturbation directions provoked COM displacements that followed a caudo-cranial temporal sequence (Fig. 4). Average COM onset times and peaks are displayed in Fig. 3. There was a significant segment effect for onset times (F(3, 18) = 76.8, p < 0.001). All four COM onsets were significantly different from each other, except those of the UPTX and LOWTX, with later onsets at the upper level COMs (HEAD: 444 ms; UPTX: 257 ms; LOWTX: 197 ms; ABDO: 133 ms). There was no perturbation direction effect and no interaction effect for COM onsets (direction: F(1, 6) = 0.4, p = 0.541; interaction: F(3, 18) = 1.8, p = 0.188). There were a significant direction effect and a significant segment effect for the COM peak displacements (direction: F(1,
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Fig. 3. Histograms displaying group means for angle onset, time-to-peak angle, peak angle, COM onset, COM peak amplitude, moment onset, time-to-peak moment following forward (black bars) and backward (grey bars) perturbations. See text for significant differences and interactions.
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Fig. 4. Head, upper thorax (UPTX), lower thorax (LOWTX) and abdomen (ABDO) center of mass displacement following forward and backward perturbations. Thick lines: group means; thin lines: one standard deviation above and below means; dashed lines: platform motion. Vertical dashed lines mark onsets.
5) = 7.0, p = 0.046; segment: F(3, 15) = 23.4, p < 0.001). Forward translations produced larger COM amplitudes (177 mm) than backward translations (163 mm). All COM peak displacements were significantly different from each other, except UPTX vs. LOWTX and LOWTX vs ABDO (HEAD: 183 mm; UPTX: 172 mm; LOWTX: 166 mm; ABDO: 160 mm). There was also a significant segment x direction interaction effect for the COM peak displacements, with forward perturbations creating greater between-COM differences (F(3, 15) = 3.3, p = 0.050).
3.2. Kinetics Fig. 5 displays moments of force and powers at the trunk and neck levels following forward and backward perturbations. For forward translations, moments of force at the trunk and neck were initially flexion moments followed by extension moments, while for backward translations, they were initially extension moments followed by flexion moments. Both forward and backward translations thus provoked mainly eccentric contractions, with flexion moments when segments move in extension, and extension moments when segments move in flexion. It can also be seen that contractions were eccentric from the negative trunk and neck powers
(see Fig. 5, lower panels). The average trunk and neck moment of force onsets and times to the first peak are displayed in Fig. 3. For onsets, there was a significant segment effect (F(1, 8) = 24.8, p = 0.001), with onsets occurring earlier for the trunk (130 ms) than for the neck (232 ms). No significant direction effect or interaction was observed (direction: F(1, 8) = 4.6, p = 0.063; interaction: F(1, 8) = 2.5, p = 0.155). For time-to-peak, there was a significant segment effect (F(1, 8) = 45.9, p < 0.001), with peak occurring earlier for the trunk (639 ms) than for the neck (702 ms). There was also a direction effect (F(1, 8) = 21.7, p = 0.002) with peak occurring earlier following forward translations (forward: 645 ms; backward: 696 ms). No significant interaction was observed (F(1, 8) = 0.5, p = 0.506). 3.3. EMG Fig. 6 displays rectified signals for SCM, CP, RA, and LES for one forward trial and one backward trial in one participant, while Table 2 shows mean EMG onset values across participants. For forward perturbations, neck and trunk flexor muscles were activated first, followed by the extensor muscles. For backward perturbations, extensor muscles were activated first, followed by flexors. As can be seen in Table 2, neck muscles were not activated
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Fig. 5. Neck and trunk flexion (+)/extension ( ) moments of force (upper four panels) and powers (lower four panels) following forward and backward perturbations. Thick lines: group means; thin lines: one standard deviation above and below means; dashed lines: platform motion. Vertical lines mark onsets (dashed) and time-to-peak (solid).
as consistently as trunk muscles. Moreover, UT was never activated in any of the participants for both forward and backward translations. Also, forward perturbations elicited muscle activation more frequently than backward perturbations. 4. Discussion In characterizing the kinematic, kinetic and EMG stabilization patterns of seated healthy individuals, we showed that forward and backward translations provoke postural reactions which display an opposite flexion/extension pattern that are qualitatively similar. However, we observed some quantitative differences in postural reactions depending on the direction of the perturbation. 4.1. Postural response to perturbations Forward translations led to head and trunk segments responding first by extension, and then reversing into flexion. However, many participants displayed a small neck movement in the opposite direction (flexion) in the beginning. Neck and trunk flexor
muscles were activated first, followed by the extensor muscles. The opposite pattern was observed following backward translations with head and trunk segments first responding by flexion, and extensors being activated first in most participants. A similar pattern of head and trunk segments initially moving in the direction opposite to that of the support surface has been reported by other groups (Blouin et al., 2003; Brault et al., 2000; Forssberg and Hirschfeld, 1994; Siegmund et al., 2002, 2003a,b; Vibert et al., 2001). The pattern of muscle recruitment observed in our study has also been previously reported in participants subjected to forward translations and legs-up rotations (Brault et al., 2000; Forssberg and Hirschfeld, 1994; Zedka et al., 1998). Our kinetic results suggest that forward and backward translations both provoked mainly eccentric contractions throughout the entire response. The motion of the trunk and neck is therefore not actively produced by muscle contraction, but rather is due to the inertial properties of the trunk and head not following motion of the platform instantly. Our results are similar to previous findings (Preuss and Fung, 2008) that revealed eccentrically controlled extension of lumbo-sacral, thoraco-lumbar, and mid-thoracic inter-segments following anterior-rightward translations.
N. St-Onge et al. / Journal of Electromyography and Kinesiology 21 (2011) 904–912 FORWARD
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Fig. 6. EMG traces for sternocleidomastoid (SCM), cervical paraspinal (CP), rectus abdominis (RA), and lumbar erector spinae (LES) in one participant following forward and backward perturbations. Data were normalized using maximal activation reached across trials. Dashed lines: platform motion. Vertical dashed lines mark onsets.
Table 2 Mean (SD) EMG onsets. Forward Right SCA SCM CP UT RA EO TES LES
349 (71) 340 (60) 800 (78) 325 (60) 307 (72) 685 (85) 663 (128)
Backward n
Left
n
Right
n
Left
n
9 7 3 0 9 10 4 8
362 (84) 324 (39) 662
6 7 1 0 8 7 6 8
510 (77) 578 (6) 375 (75)
2 2 3 0 1 3 3 9
614 509 (105) 377 (65)
1 2 5 0 4 1 6 7
347 355 690 681
(66) (85) (113) (121)
631 558 (137) 309 (62) 299 (72)
518 (106) 413 368 (95) 286 (62)
n = Number of subjects for which a burst was detected.
4.2. Caudo-cranial sequence of postural response Although the amplitude of movement was similar for both neck and trunk, the trunk segment started moving earlier and reached its first peak earlier than the neck. This caudo-cranial progression of body segment movement following perturbations in the sitting position has been previously reported by our team as well as by other groups (Côté et al., 2009; Forssberg and Hirschfeld, 1994; Keshner, 2003; Vibert et al., 2001). In our study, the caudo-cranial sequence of segments was also reflected in upper body COM movement. Upper segments started moving later than lower segments due to segment rotation and length between segments. A similar caudo-cranial sequence has been observed in both the sitting and standing postures (Preuss and Fung (2008)). 4.3. Effect of perturbation direction on timing of postural reactions Similar to Preuss and Fung (2008) who compared translations in the frontal plane to translations in the sagittal plane, the direction of the perturbation in the present study did not affect the caudocranial sequence of segmental COMs. In our study, the direction of the perturbation neither affected the caudo-cranial sequence nor the onsets of segmental COMs displacements. However, Preuss and Fung (2008) reported that the caudo-cranial delay in the progression of trunk segment COMs was shown to be more evident
with anterior–posterior perturbations than with lateral perturbations. Preuss and Fung’s results may be due to the greater compliance of the trunk in the sagittal than in the frontal plane. Although our results cannot rule out a different compliance in the forward and backward directions, this possible difference appears not to be important enough to affect onsets of segmental COMs displacements. Our results also show that the direction of perturbation does not affect timing of neck and trunk angular displacements. Again it appears that the possible difference in compliance in the forward and backward directions is not important enough to affect onsets of angular displacements. Our results do not allow comparing different planes of motion. However, according to the results from Vibert’s study, it appears that there may be a greater compliance of the head and trunk in the sagittal than in the frontal plane (Vibert et al., 2001). They indeed reported perturbations in the antero-posterior direction to result in an earlier onset of trunk and head motion as well as a shorter latency to the peaks of head rotation and head translation as compared to sideways perturbations. Our results show that the first peak of moment of force is reached earlier following forward translations. To our knowledge, the influence of perturbation direction on timing of moment of force profiles has never been reported. The faster increase in moment of force provoked by anterior translations may be due to differences in muscle coordination and recruitment, and may prevent the trunk from leaning backward following forward perturbations. This response can be explained by the higher postural threat imposed by a forward translation. Although the participants were strapped to the chair, being positioned with the upper body COM behind the seat during forward translations may put them in a more uncomfortable and threatening position than being positioned with the upper body COM above the seat and lower limbs during backward translations. 4.4. Effect of perturbation direction on amplitude of postural reactions In our study, the direction of perturbation did not affect the amplitude of angular displacement at the neck and trunk levels. However, Henry et al. (1998a) observed differences in angular
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displacements when comparing forward translations to backward and lateral translations in standing. Discordance between those results and ours may be attributed to different biomechanical constraints in sitting and standing. Indeed, Preuss and Fung (2008) demonstrated that the postural response in the trunk following movement of the support surface differs between the standing and sitting postures due to the compliance and damping provided by the lower limbs in standing. Note however, that we found a trend in the segment x direction interaction. This trend suggests that backward translations led to a greater angular displacement of the trunk than forward translations, implying a greater compliance of the trunk in flexion. The current study provides a more indepth analysis of the trunk response in sitting, and the effect that this has on head movement. We observed greater COM peak displacements provoked by forward translations than backward perturbations, suggesting that the trunk follows the platform motion more closely instead of leaning backward. This response can be explained by the higher postural threat in a forward translation. The fact that the first peak of moment of force is reached earlier following forward translations may play a role in preventing the trunk from leaning backward. Similarly, Preuss and Fung (2008) also reported COM displacement to be direction specific, with anterior and posterior perturbations producing the smallest displacements. According to the authors, this finding may be explained by the greater compliance of the trunk in the sagittal plane as compared to the frontal plane. Following the same rationale, our results suggest a smaller compliance of the trunk in the backward direction than in the forward direction. In the present study, there was also a significant interaction with forward perturbations creating greater betweenCOM differences. This finding suggests a greater displacement of upper segments in response to forward perturbations, allowing a more forward position of the upper body and thus the COM to be more centered relative to the base of support. 4.5. Effect of perturbation direction on electromyographic response In the present study, forward perturbations elicited observable bursts of muscle activation more frequently than backward perturbations. Activating muscles in reaction to a forward perturbation may be more important in order to prevent the trunk from leaning backward. Faster activation of stretched muscles may have contributed to the faster increase in moment of force provoked by anterior translations and to the trunk following the platform motion more closely instead of leaning backward. Henry et al. (1998a,b) have reported that, although latencies of shank and thigh muscles were similar for all directions of perturbation, some distal muscles were recruited either earlier or later depending on the direction of the perturbation. Modifications of parameters such as length of the support surface or velocity of displacement have also been shown to lead to a reorganisation of muscle recruitment (Horak and Nashner, 1986; Runge et al., 1999). The fact that extensor muscles are not necessarily activated in response to a backward perturbation although they are stretched may be due to differences in reflex gain and/or delay. Findings by Stokes et al. (2000) that pre-activation is associated with lower muscle responses suggest that muscles activate in response to perturbations only to provide required stiffness. In the present study, initial stiffness may have been sufficient to stabilize the upper body following backward perturbations but not following forward perturbations. 5. Conclusions We showed that forward and backward translations in the sitting position provoke postural reactions that display an opposite
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flexion/extension pattern but are qualitatively similar. However, we observed some quantitative differences in postural reactions depending on the direction of the perturbation. Differences may be due to the trunk being more compliant in flexion. Also, reaching the first peak of moment of force earlier may prevent the trunk from leaning backward following forward perturbations. The fact that COM displacement is greater following forward translations suggests that the trunk follows the platform motion more closely instead of leaning backward and possibly bringing the upper body COM behind the seat.
Conflict of interest statement No author has financial or personal conflicts of interest that could inappropriately influence their work. Acknowledgements N.S. was supported by a MENTOR post-doctoral scholarship, R.P. was supported by an FRSQ post-doctoral fellowship, and I.P. was supported by a MENTOR and an NSERC M.Sc. scholarship. J.F. holds a William Dawson Research Chair at McGill University. The infrastructure for this research was supported by the Canada Foundation for Innovation, CRIR and the JRH Foundation. References Blouin JS, Descarreaux M, Belanger-Gravel A, Simoneau M, Teasdale N. Attenuation of human neck muscle activity following repeated imposed trunk-forward linear acceleration. Experimental Brain Research 2003;150:458–64. Brault JR, Siegmund GP, Wheeler JB. Cervical muscle response during whiplash: evidence of a lengthening muscle contraction. Clinical Biomechanics (Bristol, Avon) 2000;15:426–35. Côté JN, Patenaude I, St-Onge N, Fung J. Whiplash-associated disorders affect postural reactions to antero-posterior support surface translations during sitting. Gait and Posture 2009;29:603–11. de Leva P. Adjustments to Zatsiorsky-Seluyanov’s segment inertia parameters. Journal of Biomechanics 1996;29:1223–30. Diener HC, Horak FB, Nashner LM. Influence of stimulus parameters on human postural responses. Journal of Neurophysiology 1988;59:1888–905. Forssberg H, Hirschfeld H. Postural adjustments in sitting humans following external perturbations: muscle activity and kinematics. Experimental Brain Research 1994;97:515–27. Henry SM, Fung J, Horak FB. Control of stance during lateral and anterior/posterior surface translations. IEEE Transactions on Rehabilitation Engineering 1998a;6:32–42. Henry SM, Fung J, Horak FB. EMG responses to maintain stance during multidirectional surface translations. Journal of Neurophysiology 1998b;80:1939–50. Henry SM, Fung J, Horak FB. Effect of stance width on multidirectional postural responses. Journal of Neurophysiology 2001;85:559–70. Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. Journal of Neurophysiology 1986;55:1369–81. Keshner EA. Head-trunk coordination during linear anterior–posterior translations. Journal of Neurophysiology 2003;89:1891–901. Kingma I, de Looze M, Toussaint H, Klijnsma H, Bruijnen T. Validation of a full body 3-D dynamic linked segment model. Human Movement Science 1996;15:833–60. Moorhouse KM, Granata KP. Trunk stiffness and dynamics during active extension exertions. Journal of Biomechanics 2005;38:2000–7. Nashner LM. Analysis of movement control in man using the movable platform. Advances in Neurology 1983;39:607–19. Pearsall DJ, Reid JG, Livingston LA. Segmental inertial parameters of the human trunk as determined from computed tomography. Annals of Biomedical Engineering 1996;24:198–210. Preuss R, Fung J. Musculature and biomechanics of the trunk in the maintenance of upright posture. Journal of Electromyography and Kinesiology 2008;18:815–28. Runge CF, Shupert CL, Horak FB, Zajac FE. Ankle and hip postural strategies defined by joint torques. Gait and Posture 1999;10:161–70. Siegmund GP, Sanderson DJ, Inglis JT. The effect of perturbation acceleration and advance warning on the neck postural responses of seated subjects. Experimental Brain Research 2002;144:314–21. Siegmund GP, Sanderson DJ, Myers BS, Inglis JT. Awareness affects the response of human subjects exposed to a single whiplash-like perturbation. Spine 2003a;28:671–9.
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Siegmund GP, Sanderson DJ, Myers BS, Inglis JT. Rapid neck muscle adaptation alters the head kinematics of aware and unaware subjects undergoing multiple whiplash-like perturbations. Journal of Biomechanics 2003b;36:473–82. St-Onge N, Cote JN, Patenaude I, Fung JA. Paradigm to assess postural responses triggered by anteroposterior translations in healthy seated individuals. Gait and Posture 2009;30:417–23. Stokes IA, Gardner-Morse M, Henry SM, Badger GJ. Decrease in trunk muscular response to perturbation with preactivation of lumbar spinal musculature. Spine (Phila Pa 1976) 2000;25:1957–64. Vibert N, MacDougall HG, de Waele C, Gilchrist DP, Burgess AM, Sidis A, et al. Variability in the control of head movements in seated humans: a link with whiplash injuries? Journal of Physiology 2001;532:851–68. Zedka M, Kumar S, Narayan Y. Electromyographic response of the trunk muscles to postural perturbation in sitting subjects. Journal of Electromyography and Kinesiology 1998;8:3–10.
Nancy St-Onge, Ph.D., is an Assistant Professor of the Department of Exercise Science at Concordia University and Researcher of the Constance-Lethbridge Rehabilitation Center and PERFORM Center. Her main research interest is to understand the synergistic actions of lowerlimb joints in the control of upright posture, balance, and movement regulation. She studies muscle activity, forces, and motion in situations that challenge posture in healthy and impaired populations. She explores models of instability and weakness such as injuries and muscle fatigue to better understand the participation of various components of the system to stability.
Julie N. Côté, Ph.D., is an Associate Professor at the Department of Kinesiology and Physical Education of McGill University, and a research scholar Junior 2 of the Fonds de la recherche en santé du Québec (FRSQ). She directs the Occupational Biomechanics and Ergonomics Laboratory of the Jewish Rehabilitation Hospital Feil & Oberfeld Research Center (http://www.mcg-ill.ca/edukpe/facilities/obel/), site of the CRIR. She is the co-lead of the Musculoskeletal Disorder research axis of the RRSSTQ and is a board member of the REPAR. Her research focuses on the mechanisms of muscular fatigue and posture-movement adaptations to musculoskeletal injuries, with focus on neck-shoulder disorders.
Richard A. Preuss holds a B.Sc. in Physical Therapy from McGill University, an M.Sc. in Kinesiology (Biomechanics) from the University of Waterloo, a Ph.D. in Rehabilitation Science from McGill, and has completed postdoctoral training at the Toronto Rehabilitation Institute/University of Toronto. He is currently an Assistant Professor in the School of Physical and Occupational Therapy at McGill University and a researcher at the Centre de recherche interdisciplinaire en réadaptation du Montréal métropolitain. His research focuses on biomechanical and neuromuscular factors in low back pain and other neuro – musculoskeletal conditions.
Isabelle Patenaude holds a B.Sc. in Biochemistry from the Université de Montréal, an M.Sc. in Kinesiology (Biomechanics) from McGill University and a B.Sc. in Physical Therapy from the Université de Montréal. She is currently a physical therapist working at the Clinique de physiothérapie Pierre-Boucher. For her Master’s degree, she studied postural reactions and kinematic responses in healthy and injured indiviuals to better understand injury mechanisms and more appropriate treatments. She now concentrates her work on clinical evidence-based practice of physical therapy.
Joyce Fung, PT, Ph.D., is an Associate Professor and William Dawson Scholar at the School of Physical and Occupational Therapy at McGill University. She is also the Director of Research at the Feil & Oberfeld Research Centre of the Jewish Rehabilitation Hospital, a research site of the Montreal Centre for Interdisciplinary Research in Rehabilitation. Her research ranges from the study of basic sensorimotor integration mechanisms in the control of posture and balance, to the application of new tools and technologies for the assessment and intervention of balance and mobility disorders. Her research is currently supported by the Canadian Institutes of Health Research, Fonds de la recherche en Santé du Québec, and the Jewish Rehabilitation Hospital Foundation.
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Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Direction-dependent neck and trunk postural reactions during sitting Nancy St-Onge a,b,c,⇑, Julie N. Côté c,d, Richard A. Preuss b,e, Isabelle Patenaude c,d, Joyce Fung c,e a
Department of Exercise Science, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, Canada H4B 1R6 Constance-Lethbridge Rehabilitation Center, Montreal Center for Interdisciplinary Research in Rehabilitation (CRIR), 7005 Maisonneuve W., Montreal, QC, Canada H4B 1T3 c Feil & Oberfeld/CRIR Research Centre, Jewish Rehabilitation Hospital, 3205 Place Alton Goldbloom, Laval, QC, Canada H7V 1R2 d Department of Kinesiology and Physical Education, McGill University, 475 Pine Avenue West, Montreal, QC, Canada H2W 1S4 e School of Physical and Occupational Therapy, McGill University, 3654 Promenade Sir William Osler, Montreal, QC, Canada H3G 1Y5 b
a r t i c l e
i n f o
Article history: Received 29 October 2010 Received in revised form 27 July 2011 Accepted 27 July 2011
Keywords: Postural reactions Muscle activity Kinematics Kinetics
a b s t r a c t Postural reactions in healthy individuals in the seated position have previously been described and have been shown to depend on the direction of the perturbation; however the neck response following forward and backward translations has not been compared. The overall objective of the present study was to compare neck and trunk kinematic, kinetic and electromyographic (EMG) stabilization patterns of seated healthy individuals to forward and backward translations. Ten healthy individuals, seated on a chair fixed onto a movable platform, were exposed to forward and backward translations (distance = 0.15 m, peak acceleration = 1.2 m/s2). The head and trunk kinematics as well as the EMG activity of 16 neck and trunk muscles were recorded. Neck and trunk angular displacements were computed in the sagittal plane. The centers of mass (COMs) of the head (HEAD), upper thorax (UPTX), lower thorax (LOWTX) and abdomen (ABDO) segments were also computed. Moments of force at the C7-T1 and L5S1 levels were calculated using a top-down, inverse dynamics approach. Forward translations provoked greater overall COM peak displacements. The first peak of moment of force was also reached earlier following forward translations which may have played a role in preventing the trunk from leaning backwards. These responses can be explained by the higher postural threat imposed by a forward translation. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction Human postural stabilization strategies can be investigated using mechanical perturbation protocols, which are typically performed by inducing sudden displacements of the support surface on which a person stands or sits. Many investigators have studied the effects of support surface perturbations in standing healthy participants to describe the actions of the postural control system in maintaining postural stability (Diener et al., 1988; Henry et al., 1998a,b, 2001; Horak and Nashner, 1986; Nashner, 1983; Runge et al., 1999). For instance, in response to support surface translations in different directions, stereotypical patterns have been shown to occur in the leg and trunk muscles to restore postural stability. One of these patterns is characterized by activation of muscles in a distal-to-proximal progression. Henry et al. (1998a,b) have shown some muscle responses to be direction-specific and organized in synergies, suggesting that muscles are not necessarily activated when stretched but when functionally relevant in maintaining standing equilibrium. Although ⇑ Corresponding author at: Department of Exercise Science, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, Canada H4B 1R6. Tel.: +1 514 848 2424x5805; fax: +1 514 848 8681. E-mail address: [email protected] (N. St-Onge). 1050-6411/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2011.07.016
the direction of perturbation did not affect the distal-to-proximal progression of body segment movement, responses to anterior translations resulted in smaller movements of the trunk and larger displacements of the thigh in comparison to posterior and lateral translations. The direction of the perturbation was also shown not to affect peak COM displacement; however, the difference between center of pressure and COM peak displacements was larger for lateral than for forward and backward translations, suggesting greater postural instability in this direction following the same perturbation. Other studies have characterized the response patterns to perturbations in seated individuals (Blouin et al., 2003; Brault et al., 2000; Forssberg and Hirschfeld, 1994; Keshner, 2003; Preuss and Fung, 2008; Siegmund et al., 2002, 2003a,b; Vibert et al., 2001; Zedka et al., 1998). In general, studies on seated postural perturbations have consistently identified that trunk and neck muscles are activated when they are stretched. Similar to perturbations in the standing position, perturbations in the sitting position have been shown to produce a caudo-cranial progression of body segment movement (Côté et al., 2009; Forssberg and Hirschfeld, 1994; Keshner, 2003; Vibert et al., 2001). Postural responses have also been reported to be direction-specific in the sitting position (Preuss and Fung, 2008; Vibert et al., 2001). For example, although the amplitude of the head, arms and trunk COM displacement was
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smaller following antero-posterior perturbations as compared to lateral perturbations, the caudo-cranial delay in the progression of trunk segment COMs was shown to be more evident with anterior–posterior perturbations than with lateral perturbations (Preuss and Fung, 2008). Although postural reactions in healthy individuals in the seated position have previously been described and have been shown to depend on the direction of the perturbation, the neck response following forward and backward translations has not been compared. Preuss and Fung (2008) studied several directions but have not reported the neck angular displacements or the response of neck musculature. They also did not compare the effect of forward and backward translations on the timing of postural reactions. Vibert et al. (2001) studied the response of the trunk and the neck; however, they compared antero-posterior perturbations to lateral perturbations but did not compare perturbations in the same plane (i.e., forward vs. backward perturbations). The objectives of the present study were thus to characterize neck and trunk kinematic, kinetic and EMG stabilization patterns of seated healthy individuals; and to compare these stabilization patterns between forward and backward translations.
2. Methods 2.1. Participants A group of ten healthy individuals aged 21–46 years (five women, five men; body mass: 55–88 kg; body height: 157– 184.5 cm) participated in this study. Participants previously diagnosed with any neck or back, musculoskeletal or neurological problems were excluded. Participants signed an informed consent form approved by the institutional ethics committee before participating in the study. 2.2. Experimental protocol Participants sat on an experimental chair equipped with lateral support frames for the pelvis and the knees (Preuss and Fung, 2008, Fig. 1). The chair design served to standardize the hip and knee angles. A seat belt was buckled around the thighs to stabilize the legs; the trunk was free to move in all planes. The chair was fixed to a platform servo-controlled by electrohydraulic actuators. The participants were instructed to cross their arms on their torso, keep their eyes open, look ahead and stay relaxed throughout trials. Three static trials were first recorded (3 s each). Participants were then subjected to a randomized sequence of a total of 15 trials (five forward, five backward and five unperturbed trials). The perturbation parameters (distance = 0.15 m, peak velocity = 0.3 m/s, peak acceleration = 1.2 m/s2) were selected from a previous study that aimed at determining the lowest intensity translation to elicit a postural stabilization reaction (St-Onge et al., 2009). The total duration of the perturbation including the acceleration and deceleration phases was 1.5 s. Participants were informed prior to each trial (‘‘Ready? One, two, three, go!’’); however they were not told if the trial would be forward, backward, or static. After the perturbation sequence, three static trials were recorded. 2.3. Data acquisition Motion of the platform, head, arms and trunk was recorded (sampling frequency = 120 Hz) using a six-camera Vicon 512 Motion Analysis System (Vicon Peak, UK). Passive reflective markers were placed on 25 anatomical landmarks (see Fig. 1) and on each corner of the movable platform. To allow the computation of the
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COMs, anthropometric measurements were taken: trunk depth at T1, T4, T10, and L3 levels; body height and body mass. The EMG activity of 16 muscles of the neck and trunk were acquired (sampling frequency = 1800 Hz) using the Telemyo 900 EMG system (Noraxon, USA). After preparing the skin following standard procedures, bipolar surface Ag/AgCl electrodes (Ambu, DE) were placed on the skin overlying the right and left scalenus (SCA), sternocleidomastoid (SCM), cervical paraspinals (CP), upper trapezius (UT), erector spinae (thoracic level; TES), erector spinae (lumbar level; LES), rectus abdominis (RA), and external obliques (EO). A ground electrode was placed on the greater tubercle of the humerus. Electrode placement is defined in Table 1. 2.4. Data analysis Kinematic data were low-pass filtered (zero-phase lag fourth order Butterworth filter, 6 Hz). The head segment was defined using the four head markers and the trunk segment was defined using markers on S1 and both left and right T1 transverse processes. Trunk angular displacements were computed by quantifying the orientation of the trunk segment relative to the global space using Euler xyz rotations. Neck angular displacements were computed as the orientation of the head segment relative to a segment defined using the markers on the sternal notch and both left and right T1 transverse processes using Euler yxz rotations, therefore representing the position of the head relative to the base of the neck. The COMs of the head, upper thorax (T1-T6, including the arms), lower thorax (T6-L1) and abdomen (L1-S1) segments were computed using segmental measurements and standard anthropometric tables (de Leva, 1996; Pearsall et al., 1996). Platform displacement was computed by averaging the position of the four markers positioned on its corners. Platform onset was taken as the time when the velocity of its center surpassed 2% of its maximal velocity, while angle and COM onsets were identified as the time when their velocities first surpassed 5% of the respective maximum velocities. At the neck level, some participants displayed a small movement in the opposite direction in the beginning before moving in the main direction. For example, although in response to forward translations the main motion of the neck was in extension, some participants displayed a small amount of flexion before moving into extension. To allow for more consistency, the onset of motion was selected in the direction for which most of the displacement occurred. Amplitude of the first peak angle and time to first peak angle were also computed for neck and trunk. The peak COM displacement (maximum position reached from beginning to end of motion – initial position) was computed for each segmental COM. Kinematic onsets and timeto-peak angle were reported relative to platform onset. Estimates of the net moments of force at the neck (C7-T1) and trunk (L5-S1) levels were calculated using a linked segment model, assuming segment rigidity. The position of the C7-T1 and L5-S1 joint centers, and the resulting segment kinematics (head and trunk, including arms), were derived from the kinematic model described above. A 3-dimensional, top-down, inverse dynamics approach (Kingma et al., 1996) was used to estimate the net moments of force, using anthropometric variables adapted from de Leva (1996) and Pearsall et al. (1996), similar to the approach described by Preuss and Fung (2008). Results were low-pass filtered at 2.5 Hz using a zero-phase lag 2nd order Butterworth filter. A lower filter frequency (2.5 Hz vs. 6 Hz) was used for the inverse dynamic model because the velocity and acceleration of the segments is needed for these calculations. Any high frequency noise in the position data produces large spikes in the derivatives (rapid change in slope), which can amplify this noise in the results of the kinetic analysis. This may obscure the true data, and make interpretation of the findings difficult. The frequency was chosen based
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Fig. 1. Reflective markers were placed on the following anatomical landmarks: left and right front head, left and right back head, C7 spinous process, right scapula, left and right T1 transverse processes, T6 spinous process, left and right T8 transverse processes, T12 spinous process, left and right L1 transverse processes, S1, left and right posterosuperior iliac spines, apex of sacrum, sternal notch, left and right acromia, left and right lateral epicondyles, left and right head of third metacarpals.
Table 1 Electrode placement. Muscle
Electrode position
SCA SCM CP UT TES LES RA EO
Just above the clavicle, posterior to the SCM and anterior to the UT Halfway between the mastoid process and the sternal notch At the level of C4, 2 cm from the midline Halfway between C7 and the acromion At the level of T9, 3 cm from the midline At the level of L3, 3 cm from the midline 3 cm lateral to the umbilicus 8–12 cm lateral to the umbilicus
on the findings from Moorhouse and Granata (2005). This study found the natural frequency of the trunk following perturbation to be below 2 Hz. As such, the 2.5-Hz cutoff is unlikely to eliminate any relevant data from the kinematics. Kinetic onsets were identified as the time when their first derivatives first surpassed 5% of the respective maximum velocities. Time to first peak was also computed. Onsets and time-to-peak are reported relative to platform onset. The EMG signals were first amplified (2000). For each EMG signal, any contamination by the electrocardiogram was removed by first visually defining the initiation and end of a heartbeat. The selected heartbeat was then filtered out from the EMG signal using a 40-Hz low-pass 2nd order Butterworth filter on the part of the signal where it occurred. The beginning of all heartbeats was visually defined and the filtered-out heartbeat was subsequently subtracted from the EMG signal at every position where a heartbeat was defined. Signals were then band-pass filtered (zero-phase lag 4th order Butterworth filter, 10–350 Hz) and fullwave rectified. The mean and the standard deviation (SD) of each baseline EMG signal were calculated using the data from 300 to 100 ms before platform onset. EMG envelopes were then computed using a 20-Hz zero-phase lag 4th order Butterworth lowpass filter. The first burst that surpassed two SDs above the
baseline mean for at least 25 ms was detected on each EMG envelope. The onset of the EMG burst was identified by following the signal back until the point when the signal decreased under the baseline mean. EMG onsets are reported relative to platform onset. All analyses were performed using Matlab (The MathWorks Inc., Natick, MA, USA).
2.5. Statistical analysis Trials with missing markers which made points of interest (onsets, peaks, ..) not available were discarded. Data were first averaged over trials for each participant when at least three trials were available. For COM variables (onset, peak), kinematic variables (onset, time-to-peak, and amplitude), and kinetic variable (onset, time-to-peak) the data were analyzed using a two-way repeated-measures analysis of variance (ANOVA) with two within factors: direction (forward, backward) and segment (angles: neck and trunk; COMs: head, upper thorax, lower thorax and abdomen). When a significant main effect or interaction was found, post hoc analyses were performed using Tukey tests of comparisons. All statistical tests were performed using Statistica, v. 7 (Statsoft, Tulsa, OK, USA) and statistical significance was set at p < 0.05.
3. Results 3.1. Kinematics Fig. 2 displays the angular displacement sequence following forward and backward perturbations. For forward translations, the neck first moved in flexion in most participants, but motion reversed to extension and most of the displacement occurred in extension. The trunk first moved into extension and then reversed into flexion. The opposite pattern was observed following backward translations. The average neck and trunk angle onsets, times
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to the first peak angle, and amplitude of first peak are displayed in Fig. 3. For angle onsets, there was a significant segment effect (F(1, 7) = 1147.7, p < 0.001), with onsets occurring earlier for the trunk (96 ms) than for the neck (596 ms). No significant direction or interaction effect was observed (direction: F(1, 7) = 0.1, p = 0.794; interaction: F(1, 7) = 0.003, p = 0.955). For the time to the first peak angle (extension for forward perturbations, flexion for backward perturbations), there was also a significant effect of segment (F(1,7) = 49.1, p < 0.001) with peak angle occurring earlier for the trunk (711 ms) compared to the neck (1099 ms), and no significant direction or interaction effect (direction: F(1, 7) = 3.0, p = 0.126; interaction: F(1, 7) = 0.1, p = 0.724). For the amplitude of the first peak, there was no segment, direction, or interaction effect
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(segment: F(1, 6) = 0.6, p = 0.475; direction: F(1, 6) = 1.7, p = 0.245; interaction: F(1,6) = 5.7, p = 0.055). Both perturbation directions provoked COM displacements that followed a caudo-cranial temporal sequence (Fig. 4). Average COM onset times and peaks are displayed in Fig. 3. There was a significant segment effect for onset times (F(3, 18) = 76.8, p < 0.001). All four COM onsets were significantly different from each other, except those of the UPTX and LOWTX, with later onsets at the upper level COMs (HEAD: 444 ms; UPTX: 257 ms; LOWTX: 197 ms; ABDO: 133 ms). There was no perturbation direction effect and no interaction effect for COM onsets (direction: F(1, 6) = 0.4, p = 0.541; interaction: F(3, 18) = 1.8, p = 0.188). There were a significant direction effect and a significant segment effect for the COM peak displacements (direction: F(1,
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Fig. 3. Histograms displaying group means for angle onset, time-to-peak angle, peak angle, COM onset, COM peak amplitude, moment onset, time-to-peak moment following forward (black bars) and backward (grey bars) perturbations. See text for significant differences and interactions.
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Fig. 4. Head, upper thorax (UPTX), lower thorax (LOWTX) and abdomen (ABDO) center of mass displacement following forward and backward perturbations. Thick lines: group means; thin lines: one standard deviation above and below means; dashed lines: platform motion. Vertical dashed lines mark onsets.
5) = 7.0, p = 0.046; segment: F(3, 15) = 23.4, p < 0.001). Forward translations produced larger COM amplitudes (177 mm) than backward translations (163 mm). All COM peak displacements were significantly different from each other, except UPTX vs. LOWTX and LOWTX vs ABDO (HEAD: 183 mm; UPTX: 172 mm; LOWTX: 166 mm; ABDO: 160 mm). There was also a significant segment x direction interaction effect for the COM peak displacements, with forward perturbations creating greater between-COM differences (F(3, 15) = 3.3, p = 0.050).
3.2. Kinetics Fig. 5 displays moments of force and powers at the trunk and neck levels following forward and backward perturbations. For forward translations, moments of force at the trunk and neck were initially flexion moments followed by extension moments, while for backward translations, they were initially extension moments followed by flexion moments. Both forward and backward translations thus provoked mainly eccentric contractions, with flexion moments when segments move in extension, and extension moments when segments move in flexion. It can also be seen that contractions were eccentric from the negative trunk and neck powers
(see Fig. 5, lower panels). The average trunk and neck moment of force onsets and times to the first peak are displayed in Fig. 3. For onsets, there was a significant segment effect (F(1, 8) = 24.8, p = 0.001), with onsets occurring earlier for the trunk (130 ms) than for the neck (232 ms). No significant direction effect or interaction was observed (direction: F(1, 8) = 4.6, p = 0.063; interaction: F(1, 8) = 2.5, p = 0.155). For time-to-peak, there was a significant segment effect (F(1, 8) = 45.9, p < 0.001), with peak occurring earlier for the trunk (639 ms) than for the neck (702 ms). There was also a direction effect (F(1, 8) = 21.7, p = 0.002) with peak occurring earlier following forward translations (forward: 645 ms; backward: 696 ms). No significant interaction was observed (F(1, 8) = 0.5, p = 0.506). 3.3. EMG Fig. 6 displays rectified signals for SCM, CP, RA, and LES for one forward trial and one backward trial in one participant, while Table 2 shows mean EMG onset values across participants. For forward perturbations, neck and trunk flexor muscles were activated first, followed by the extensor muscles. For backward perturbations, extensor muscles were activated first, followed by flexors. As can be seen in Table 2, neck muscles were not activated
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as consistently as trunk muscles. Moreover, UT was never activated in any of the participants for both forward and backward translations. Also, forward perturbations elicited muscle activation more frequently than backward perturbations. 4. Discussion In characterizing the kinematic, kinetic and EMG stabilization patterns of seated healthy individuals, we showed that forward and backward translations provoke postural reactions which display an opposite flexion/extension pattern that are qualitatively similar. However, we observed some quantitative differences in postural reactions depending on the direction of the perturbation. 4.1. Postural response to perturbations Forward translations led to head and trunk segments responding first by extension, and then reversing into flexion. However, many participants displayed a small neck movement in the opposite direction (flexion) in the beginning. Neck and trunk flexor
muscles were activated first, followed by the extensor muscles. The opposite pattern was observed following backward translations with head and trunk segments first responding by flexion, and extensors being activated first in most participants. A similar pattern of head and trunk segments initially moving in the direction opposite to that of the support surface has been reported by other groups (Blouin et al., 2003; Brault et al., 2000; Forssberg and Hirschfeld, 1994; Siegmund et al., 2002, 2003a,b; Vibert et al., 2001). The pattern of muscle recruitment observed in our study has also been previously reported in participants subjected to forward translations and legs-up rotations (Brault et al., 2000; Forssberg and Hirschfeld, 1994; Zedka et al., 1998). Our kinetic results suggest that forward and backward translations both provoked mainly eccentric contractions throughout the entire response. The motion of the trunk and neck is therefore not actively produced by muscle contraction, but rather is due to the inertial properties of the trunk and head not following motion of the platform instantly. Our results are similar to previous findings (Preuss and Fung, 2008) that revealed eccentrically controlled extension of lumbo-sacral, thoraco-lumbar, and mid-thoracic inter-segments following anterior-rightward translations.
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Fig. 6. EMG traces for sternocleidomastoid (SCM), cervical paraspinal (CP), rectus abdominis (RA), and lumbar erector spinae (LES) in one participant following forward and backward perturbations. Data were normalized using maximal activation reached across trials. Dashed lines: platform motion. Vertical dashed lines mark onsets.
Table 2 Mean (SD) EMG onsets. Forward Right SCA SCM CP UT RA EO TES LES
349 (71) 340 (60) 800 (78) 325 (60) 307 (72) 685 (85) 663 (128)
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510 (77) 578 (6) 375 (75)
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614 509 (105) 377 (65)
1 2 5 0 4 1 6 7
347 355 690 681
(66) (85) (113) (121)
631 558 (137) 309 (62) 299 (72)
518 (106) 413 368 (95) 286 (62)
n = Number of subjects for which a burst was detected.
4.2. Caudo-cranial sequence of postural response Although the amplitude of movement was similar for both neck and trunk, the trunk segment started moving earlier and reached its first peak earlier than the neck. This caudo-cranial progression of body segment movement following perturbations in the sitting position has been previously reported by our team as well as by other groups (Côté et al., 2009; Forssberg and Hirschfeld, 1994; Keshner, 2003; Vibert et al., 2001). In our study, the caudo-cranial sequence of segments was also reflected in upper body COM movement. Upper segments started moving later than lower segments due to segment rotation and length between segments. A similar caudo-cranial sequence has been observed in both the sitting and standing postures (Preuss and Fung (2008)). 4.3. Effect of perturbation direction on timing of postural reactions Similar to Preuss and Fung (2008) who compared translations in the frontal plane to translations in the sagittal plane, the direction of the perturbation in the present study did not affect the caudocranial sequence of segmental COMs. In our study, the direction of the perturbation neither affected the caudo-cranial sequence nor the onsets of segmental COMs displacements. However, Preuss and Fung (2008) reported that the caudo-cranial delay in the progression of trunk segment COMs was shown to be more evident
with anterior–posterior perturbations than with lateral perturbations. Preuss and Fung’s results may be due to the greater compliance of the trunk in the sagittal than in the frontal plane. Although our results cannot rule out a different compliance in the forward and backward directions, this possible difference appears not to be important enough to affect onsets of segmental COMs displacements. Our results also show that the direction of perturbation does not affect timing of neck and trunk angular displacements. Again it appears that the possible difference in compliance in the forward and backward directions is not important enough to affect onsets of angular displacements. Our results do not allow comparing different planes of motion. However, according to the results from Vibert’s study, it appears that there may be a greater compliance of the head and trunk in the sagittal than in the frontal plane (Vibert et al., 2001). They indeed reported perturbations in the antero-posterior direction to result in an earlier onset of trunk and head motion as well as a shorter latency to the peaks of head rotation and head translation as compared to sideways perturbations. Our results show that the first peak of moment of force is reached earlier following forward translations. To our knowledge, the influence of perturbation direction on timing of moment of force profiles has never been reported. The faster increase in moment of force provoked by anterior translations may be due to differences in muscle coordination and recruitment, and may prevent the trunk from leaning backward following forward perturbations. This response can be explained by the higher postural threat imposed by a forward translation. Although the participants were strapped to the chair, being positioned with the upper body COM behind the seat during forward translations may put them in a more uncomfortable and threatening position than being positioned with the upper body COM above the seat and lower limbs during backward translations. 4.4. Effect of perturbation direction on amplitude of postural reactions In our study, the direction of perturbation did not affect the amplitude of angular displacement at the neck and trunk levels. However, Henry et al. (1998a) observed differences in angular
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displacements when comparing forward translations to backward and lateral translations in standing. Discordance between those results and ours may be attributed to different biomechanical constraints in sitting and standing. Indeed, Preuss and Fung (2008) demonstrated that the postural response in the trunk following movement of the support surface differs between the standing and sitting postures due to the compliance and damping provided by the lower limbs in standing. Note however, that we found a trend in the segment x direction interaction. This trend suggests that backward translations led to a greater angular displacement of the trunk than forward translations, implying a greater compliance of the trunk in flexion. The current study provides a more indepth analysis of the trunk response in sitting, and the effect that this has on head movement. We observed greater COM peak displacements provoked by forward translations than backward perturbations, suggesting that the trunk follows the platform motion more closely instead of leaning backward. This response can be explained by the higher postural threat in a forward translation. The fact that the first peak of moment of force is reached earlier following forward translations may play a role in preventing the trunk from leaning backward. Similarly, Preuss and Fung (2008) also reported COM displacement to be direction specific, with anterior and posterior perturbations producing the smallest displacements. According to the authors, this finding may be explained by the greater compliance of the trunk in the sagittal plane as compared to the frontal plane. Following the same rationale, our results suggest a smaller compliance of the trunk in the backward direction than in the forward direction. In the present study, there was also a significant interaction with forward perturbations creating greater betweenCOM differences. This finding suggests a greater displacement of upper segments in response to forward perturbations, allowing a more forward position of the upper body and thus the COM to be more centered relative to the base of support. 4.5. Effect of perturbation direction on electromyographic response In the present study, forward perturbations elicited observable bursts of muscle activation more frequently than backward perturbations. Activating muscles in reaction to a forward perturbation may be more important in order to prevent the trunk from leaning backward. Faster activation of stretched muscles may have contributed to the faster increase in moment of force provoked by anterior translations and to the trunk following the platform motion more closely instead of leaning backward. Henry et al. (1998a,b) have reported that, although latencies of shank and thigh muscles were similar for all directions of perturbation, some distal muscles were recruited either earlier or later depending on the direction of the perturbation. Modifications of parameters such as length of the support surface or velocity of displacement have also been shown to lead to a reorganisation of muscle recruitment (Horak and Nashner, 1986; Runge et al., 1999). The fact that extensor muscles are not necessarily activated in response to a backward perturbation although they are stretched may be due to differences in reflex gain and/or delay. Findings by Stokes et al. (2000) that pre-activation is associated with lower muscle responses suggest that muscles activate in response to perturbations only to provide required stiffness. In the present study, initial stiffness may have been sufficient to stabilize the upper body following backward perturbations but not following forward perturbations. 5. Conclusions We showed that forward and backward translations in the sitting position provoke postural reactions that display an opposite
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flexion/extension pattern but are qualitatively similar. However, we observed some quantitative differences in postural reactions depending on the direction of the perturbation. Differences may be due to the trunk being more compliant in flexion. Also, reaching the first peak of moment of force earlier may prevent the trunk from leaning backward following forward perturbations. The fact that COM displacement is greater following forward translations suggests that the trunk follows the platform motion more closely instead of leaning backward and possibly bringing the upper body COM behind the seat.
Conflict of interest statement No author has financial or personal conflicts of interest that could inappropriately influence their work. Acknowledgements N.S. was supported by a MENTOR post-doctoral scholarship, R.P. was supported by an FRSQ post-doctoral fellowship, and I.P. was supported by a MENTOR and an NSERC M.Sc. scholarship. J.F. holds a William Dawson Research Chair at McGill University. The infrastructure for this research was supported by the Canada Foundation for Innovation, CRIR and the JRH Foundation. References Blouin JS, Descarreaux M, Belanger-Gravel A, Simoneau M, Teasdale N. Attenuation of human neck muscle activity following repeated imposed trunk-forward linear acceleration. Experimental Brain Research 2003;150:458–64. Brault JR, Siegmund GP, Wheeler JB. Cervical muscle response during whiplash: evidence of a lengthening muscle contraction. Clinical Biomechanics (Bristol, Avon) 2000;15:426–35. Côté JN, Patenaude I, St-Onge N, Fung J. Whiplash-associated disorders affect postural reactions to antero-posterior support surface translations during sitting. Gait and Posture 2009;29:603–11. de Leva P. Adjustments to Zatsiorsky-Seluyanov’s segment inertia parameters. Journal of Biomechanics 1996;29:1223–30. Diener HC, Horak FB, Nashner LM. Influence of stimulus parameters on human postural responses. Journal of Neurophysiology 1988;59:1888–905. Forssberg H, Hirschfeld H. Postural adjustments in sitting humans following external perturbations: muscle activity and kinematics. Experimental Brain Research 1994;97:515–27. Henry SM, Fung J, Horak FB. Control of stance during lateral and anterior/posterior surface translations. IEEE Transactions on Rehabilitation Engineering 1998a;6:32–42. Henry SM, Fung J, Horak FB. EMG responses to maintain stance during multidirectional surface translations. Journal of Neurophysiology 1998b;80:1939–50. Henry SM, Fung J, Horak FB. Effect of stance width on multidirectional postural responses. Journal of Neurophysiology 2001;85:559–70. Horak FB, Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. Journal of Neurophysiology 1986;55:1369–81. Keshner EA. Head-trunk coordination during linear anterior–posterior translations. Journal of Neurophysiology 2003;89:1891–901. Kingma I, de Looze M, Toussaint H, Klijnsma H, Bruijnen T. Validation of a full body 3-D dynamic linked segment model. Human Movement Science 1996;15:833–60. Moorhouse KM, Granata KP. Trunk stiffness and dynamics during active extension exertions. Journal of Biomechanics 2005;38:2000–7. Nashner LM. Analysis of movement control in man using the movable platform. Advances in Neurology 1983;39:607–19. Pearsall DJ, Reid JG, Livingston LA. Segmental inertial parameters of the human trunk as determined from computed tomography. Annals of Biomedical Engineering 1996;24:198–210. Preuss R, Fung J. Musculature and biomechanics of the trunk in the maintenance of upright posture. Journal of Electromyography and Kinesiology 2008;18:815–28. Runge CF, Shupert CL, Horak FB, Zajac FE. Ankle and hip postural strategies defined by joint torques. Gait and Posture 1999;10:161–70. Siegmund GP, Sanderson DJ, Inglis JT. The effect of perturbation acceleration and advance warning on the neck postural responses of seated subjects. Experimental Brain Research 2002;144:314–21. Siegmund GP, Sanderson DJ, Myers BS, Inglis JT. Awareness affects the response of human subjects exposed to a single whiplash-like perturbation. Spine 2003a;28:671–9.
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Siegmund GP, Sanderson DJ, Myers BS, Inglis JT. Rapid neck muscle adaptation alters the head kinematics of aware and unaware subjects undergoing multiple whiplash-like perturbations. Journal of Biomechanics 2003b;36:473–82. St-Onge N, Cote JN, Patenaude I, Fung JA. Paradigm to assess postural responses triggered by anteroposterior translations in healthy seated individuals. Gait and Posture 2009;30:417–23. Stokes IA, Gardner-Morse M, Henry SM, Badger GJ. Decrease in trunk muscular response to perturbation with preactivation of lumbar spinal musculature. Spine (Phila Pa 1976) 2000;25:1957–64. Vibert N, MacDougall HG, de Waele C, Gilchrist DP, Burgess AM, Sidis A, et al. Variability in the control of head movements in seated humans: a link with whiplash injuries? Journal of Physiology 2001;532:851–68. Zedka M, Kumar S, Narayan Y. Electromyographic response of the trunk muscles to postural perturbation in sitting subjects. Journal of Electromyography and Kinesiology 1998;8:3–10.
Nancy St-Onge, Ph.D., is an Assistant Professor of the Department of Exercise Science at Concordia University and Researcher of the Constance-Lethbridge Rehabilitation Center and PERFORM Center. Her main research interest is to understand the synergistic actions of lowerlimb joints in the control of upright posture, balance, and movement regulation. She studies muscle activity, forces, and motion in situations that challenge posture in healthy and impaired populations. She explores models of instability and weakness such as injuries and muscle fatigue to better understand the participation of various components of the system to stability.
Julie N. Côté, Ph.D., is an Associate Professor at the Department of Kinesiology and Physical Education of McGill University, and a research scholar Junior 2 of the Fonds de la recherche en santé du Québec (FRSQ). She directs the Occupational Biomechanics and Ergonomics Laboratory of the Jewish Rehabilitation Hospital Feil & Oberfeld Research Center (http://www.mcg-ill.ca/edukpe/facilities/obel/), site of the CRIR. She is the co-lead of the Musculoskeletal Disorder research axis of the RRSSTQ and is a board member of the REPAR. Her research focuses on the mechanisms of muscular fatigue and posture-movement adaptations to musculoskeletal injuries, with focus on neck-shoulder disorders.
Richard A. Preuss holds a B.Sc. in Physical Therapy from McGill University, an M.Sc. in Kinesiology (Biomechanics) from the University of Waterloo, a Ph.D. in Rehabilitation Science from McGill, and has completed postdoctoral training at the Toronto Rehabilitation Institute/University of Toronto. He is currently an Assistant Professor in the School of Physical and Occupational Therapy at McGill University and a researcher at the Centre de recherche interdisciplinaire en réadaptation du Montréal métropolitain. His research focuses on biomechanical and neuromuscular factors in low back pain and other neuro – musculoskeletal conditions.
Isabelle Patenaude holds a B.Sc. in Biochemistry from the Université de Montréal, an M.Sc. in Kinesiology (Biomechanics) from McGill University and a B.Sc. in Physical Therapy from the Université de Montréal. She is currently a physical therapist working at the Clinique de physiothérapie Pierre-Boucher. For her Master’s degree, she studied postural reactions and kinematic responses in healthy and injured indiviuals to better understand injury mechanisms and more appropriate treatments. She now concentrates her work on clinical evidence-based practice of physical therapy.
Joyce Fung, PT, Ph.D., is an Associate Professor and William Dawson Scholar at the School of Physical and Occupational Therapy at McGill University. She is also the Director of Research at the Feil & Oberfeld Research Centre of the Jewish Rehabilitation Hospital, a research site of the Montreal Centre for Interdisciplinary Research in Rehabilitation. Her research ranges from the study of basic sensorimotor integration mechanisms in the control of posture and balance, to the application of new tools and technologies for the assessment and intervention of balance and mobility disorders. Her research is currently supported by the Canadian Institutes of Health Research, Fonds de la recherche en Santé du Québec, and the Jewish Rehabilitation Hospital Foundation.