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J Appl Physiol 99: 141-153, 2005. First published October 15, 2004; doi:10.1152/japplphysiol.00494.2004
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Neck muscle fatigue and spatial orientation during stepping in place in humans

Micaela Schmid1 and Marco Schieppati1,2

1Human Movement Laboratory, Centro Studi Attività Motorie, Fondazione Salvatore Maugeri, Scientific Institute of Pavia, and 2Department of Experimental Medicine, Section of Human Physiology, University of Pavia, Pavia, Italy

Submitted 10 May 2004 ; accepted in final form 10 August 2004


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Neck proprioceptive input, as elicited by muscle vibration, can produce destabilizing effects on stance and locomotion. Neck muscle fatigue produces destabilizing effects on stance, too. Our aim was to assess whether neck muscle fatigue can also perturb the orientation in space during a walking task. Direction and amplitude of the path covered during stepping in place were measured in 10 blindfolded subjects, who performed five 30-s stepping trials before and after a 5-min period of isometric dorsal neck muscle contraction against a load. Neck muscle electromyogram amplitude and median frequency during the head extensor effort were used to compute a fatigue index. Head and body kinematics were recorded by an optoelectronic system, and stepping cadence was measured by sensorized insoles. Before the contraction period, subjects normally stepped on the spot or drifted forward. After contraction, some subjects reproduced the same behavior, whereas others reduced their forward progression or even stepped backward. The former subjects showed minimal signs of fatigue and the latter ones marked signs of fatigue, as quantified by the dorsal neck electromyogram index. Head position and cadence were unaffected in either group of subjects. We argue that the abnormal fatigue-induced afferent input originating in the receptors transducing the neck muscle metabolic state can modulate the egocentric spatial reference frame. Notably, the effects of neck muscle fatigue on orientation are opposite to those produced by neck proprioception. The neck represents a complex source of inputs capable of modifying our orientation in space during a locomotor task.

locomotion; reference frame

AN IMPRESSIVE NUMBER OF PAPERS have recently appeared about the multifarious roles of the neck muscle proprioceptive input on the perception of body segment position and body orientation in space. A clear example of the relevance of neck input for the subject's reference frame comes from studies of neck vibration after cortical lesions leading to neglect of the contralateral space and/or body. These studies clearly show that neck vibratory treatment improves neglect symptomatology. This clear superiority over other treatments might result from the partial (re)activation of a distributed, multisensory network in the lesioned hemisphere (Ref. 36; for a review, see Ref. 39) that is triggered by the spindle afferent input activated by the vibration. Most likely, the parietal cortex plays a role in the egocentric representation of space and its calibration, since many of its areas receive signals from the neck muscles and the labyrinth (2).

Less amazing, but certainly nonnegligible, effects can be produced by neck muscle vibration in normal subjects, in particular on body segment orientation and body sway during quiet stance and on walking features. In standing subjects, neck muscle vibration induces body tilt and increases sway, suggesting that posture is organized with respect to a "body schema," to the construction of which the spindle input from the neck contributes together with eye and skeletal muscle (15, 23, 32, 38, 44, 54, 55). During stepping in place, bilateral vibration of the dorsal neck muscles produces an involuntary forward stepping without modifying the stepping frequency and in treadmill locomotion produces an involuntary steplike increase of walking speed (33). One-sided lateral neck muscle vibration, in the absence of vision, produces deviation of the trajectory during normal walking (3) and body rotation during stepping in place (4); under both conditions, the deviation is opposite to the vibrated site. On a different vein, Goodwin et al. (20) originally described proprioceptive illusions induced by muscle vibration. It was later shown that neck muscle vibration also elicits apparent motion of a stationary visual target and deviation of the perceived "straight ahead," possibly by producing a change in the egocentric body-centered coordinate system (1, 37, 62).

Muscle vibration is certainly an artificial situation, with its major advantage being the good selectivity of its effects on the muscle spindles' primary terminations (11). Are there "natural" stimuli able to elicit similar effects, e.g., changes in length of the neck muscles connected with head posture? Head and eyes systematically deviate toward the future direction of the curved trajectory (21), suggesting an anticipatory role of the neck muscle for body steering while walking. Body sway increases when subjects stand with their heads turned or extended and their eyes closed (5, 58). Early observations suggested that cervical proprioceptive input could affect the direction of body sway by acting on the central vestibular system (28). More recently, it has been shown that neck input has an influence on the direction of body displacement induced by galvanic vestibular stimulation (18). Moreover, natural proprioceptive stimulation (head rotation) affects the perception of the head position, object localization, and movement in the visual space (46, 48). It has also been shown that vestibular-proprioceptive interactions play a role in self-motion perception in addition to postural control (47).

On the other hand, disturbances of the neck musculature could bring about dizziness or unsteadiness, the so-called cervicogenic dizziness (6). A report by Schieppati et al. (56) showed that prolonged contraction of dorsal neck muscles, bilaterally, can alter balance control through a mechanism connected to fatigue-induced afferent inflow. Strong and prolonged neck muscle contractions have also been recently shown to produce postural responses (14). Fatigue-related sensory input may be the result of an increased outflow from the free nerve endings as a consequence of ionic or metabolic changes (elevated interstitial potassium concentration or insufficient oxygen availability due to reduced blood flow) (19, 52). Muscle fatigue can indeed affect joint position sense (Refs. 12, 57, 60; for a recent review, see Ref. 63), and abnormal cervical pain-related input is able to significantly alter postural control (35).

In this study, we have tested the hypothesis that dorsal neck muscle fatigue could affect the reference system for the orientation of body position in space. In particular, the effects of a fatiguing contraction have been tested on the capacity of stepping in place. This task reproduces several features of normal walking (8), such as the cyclic single-leg support of the body and the need for accurate control of balance. It can also be more easily captured by a movement-analysis system for extended periods of time than by normal locomotion. As such, this task should be at least as sensitive as normal floor walking to possible disorientation-producing stimuli. Perhaps, it could be even more sensible than normal walking, because, contrary to the latter, it lacks the advantage given by the kinetic energy of the body progressing in one direction. The stepping-in-place task has been previously employed as a test for vestibular deficits and balance problems, even if its reliability in this context has been repeatedly challenged (50). Because the isometric contraction of the dorsal neck muscles was bilateral and symmetrical, we assumed that postcontraction changes in the body position during the stepping-in-place test could be detected along the subject's sagittal plane, much like it occurred as a consequence of bilateral dorsal neck muscle vibration, which induced an increased velocity in the stepping progression along the straight-ahead direction (32).


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects.   Ten healthy subjects (9 men and 1 women, mean age 26.2 yr, range 22–33 yr) volunteered to participate. No subject had a history of neck pain or cervical column disease or had suffered head trauma or whiplash injury. Informed consent was obtained according to the Declaration of Helsinki. The local Ethics Committee approved the investigation and experimental procedures.

Procedures.   Subjects were asked to step in place at a self-selected pace, blindfolded in a dim-lighted room. Before the start of the acquisition session, subjects were free to step in place with eyes open to feel confident with the maneuver. Then four blocks of stepping trials were acquired, each composed of five successive trials. Each trial lasted 30 s. After each trial, the subjects were repositioned at the starting point by one experimenter before the next trial began. It was checked that, at the beginning of each trial, the subjects started from the same initial standing position, with the orientation of feet, trunk, and head aligned. The starting signal was given by the experimenter after a verbal warning signal. The four blocks were the control, postcontraction 1, recovery, and postcontraction 2 blocks. After the control and recovery blocks, subjects performed a 5-min-long tonic isometric bilateral contraction of the dorsal neck muscles against a load (see Isometric contraction of dorsal neck muscles) while standing on the starting spot. At the end of this period, subjects immediately started the first trial of the postcontraction (1 or 2) block. A rest period of ~30 min separated the postcontraction 1 block from the recovery block. The subjects' preparation with the markers and electrodes took ~30 min. The entire stepping session lasted ~1 h. The same subjects have also been recruited in an additional session, in a different day, when they were asked to step in place and again perform four blocks of five subsequent stepping trials each, but without tonic isometric contraction of the dorsal neck muscles (no-load session). This procedure was performed as a control experiment to check that the repetition of the stepping trials per se produced no effect on body displacement and to help in interpreting highly variable data.

Isometric contraction of dorsal neck muscles.   A large belt was passed around the head just above the ears, and a cable was fixed to it frontally and medially in correspondence with the forehead. The cable passed through a pulley fixed at a 1-m distance at head height. The pulley was part of a versatile gym training column placed in front of the subject. Its vertical position was adjustable so that the line of the pulling action was horizontal. The other end of the cable was fixed to an adjustable mass. The thorax of the subject leaned against a padded vertical support firmly fixed to the cable column so that the action of the mass did not displace the trunk and overall body posture. No contraction of the body extensor muscle chain below the support level was required, since there was no need to push the trunk or whole body backward, owing to the thorax support, which nullified the body forward-pulling action of the mass. Therefore, the muscle action was broadly limited to the neck extensors, and the subject counteracted the head-flexor torque exerted by the mass by contracting the dorsal neck muscles. The subjects had visual feedback of the head position by way of a target fixed to the cable, which had to remain coplanar with a reference fixed to the column. This was sufficient enough to ensure negligible head pitch during the head extensor effort against the head-flexor torque produced by the mass. For each subject, the mass was chosen so that it represented about one-third of the maximal voluntary contraction (MVC; 25.5 ± 8.5 kg), i.e., 9.5 ± 2.0 kg, equal to 34.9 ± 9.5% of MVC. MVC was the highest force value exerted during a 10-s period of neck extension, during which the subject was encouraged to produce the strongest possible effort. This was measured by means of a mechanical dynamometer placed in series between the head belt and the pulley. During the fatiguing periods, the subject had to counteract the applied mass for 5 min. At the end of this period, the mass and the padded support were quickly disconnected and removed.

Electromyogram recording and processing.   Electrical activity of the dorsal neck (splenius) and ventral neck (sternocleidomastoid) muscles (from both right and left side) was recorded using bipolar prejelled surface electrodes, with a longitudinal distance of 1 cm between the recording spots. The electrode pairs were placed on the bellies of the dorsal neck muscles, 2 cm from the midline and 4 cm below the cranial insertion, and on the belly of the sternocleidomastoid, about halfway from its proximal and distal insertion points. The electrodes were left in place during the entire recording session. The signals were differentially amplified (x1,000), filtered (cutoff frequency of 500 Hz), and acquired at a sampling frequency of 1 kHz. Data were recorded by the Telemg Multichannel Electromyograph System (Bioengineering Technology Systems). The signals were acquired for the initial 10-s period of each minute of the 5-min contraction period. The analysis of the electromyogram (EMG) was performed with the Acknowledge software (Biopac), and the EMG amplitude (AMP) of the filtered and integrated signal and the signal's median power frequency (MF) were calculated over the recorded epochs (49). The EMG activity plots of the splenius and sternocleidomastoid muscles, during the 10 s of minute 1 and the 10 s of minute 5, are shown in Fig. 1.



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  		Fig. 1. Examples of traces of surface electromyogram (EMG), recorded from a dorsal [splenius (SPL), left] and anterior [sternocleidomastoid (SCM), right] neck muscle in one subject. The raw traces have been recorded during the first (top) and last minute (bottom) of the 5-min tonic isometric bilateral contraction of the dorsal neck muscles against a load. The selectivity of the contraction is witnessed by the silence of the anterior flexor muscle (SCM, right), both at the beginning and the end of the contraction period. The development of fatigue is accompanied by an increase in amplitude of the SPL EMG from the first to the last minute of contraction (compare top and bottom) and by a shift toward lower frequency values of the median frequency (MDF) in the power spectrum of the EMG (middle) observed at minute 5 of contraction.

 
Procedure of quantification of muscle fatigue based on EMG signal.   Based on the changes in the AMP and MF between the beginning and end of the contracting period, an EMG index of fatigue was calculated for each subject using the following formula: index of fatigue = ratio of AMP/ratio of MF, where the ratio of AMP = (AMP of the 10-s period of minute 5/AMP of the 10-s period of minute 1) and the ratio of MF = (MF of the 10-s period of minute 5/MF of the 10-s perod of minute 1).

This index is influenced by two variables that are known to be affected by the fatigue phenomenon (49). To check that both variables were influenced by fatigue in the present population, we plotted the EMG median frequency vs. amplitude for each subject and for each minute of the 5-min period of tonic contraction. Figure 2A shows four examples of these relationships and the best-fit line for each of them. In two cases, when the median frequency decreased, the amplitude increased. In the other two cases, the best-fit line was less steep or flat. The angular coefficients of the best-fit lines were thus calculated for each subject and plotted against the corresponding indexes of fatigue. In Fig. 2B, the result of this procedure is reported. The strong linearity of this scatter [y = –3.56x + 3.66; r2 = 0.91; F(1,8) = 87.035; P = 0.00001] is in favor of the appropriateness of the use of an index that combines both EMG variables.



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  		Fig. 2. A: EMG amplitude vs. EMG median frequency for each successive minute of the 5-min period of tonic contraction. These relationships are shown for 4 subjects, and the best-fit line for each of them is plotted. For 2 subjects (solid symbols), when the median frequency decreased, the amplitude increased. For the other subjects (open symbols), the best-fit line was less steep or flat. B: angular coefficients of the best-fit lines calculated for all subjects are plotted against the corresponding indexes of fatigue. For A and B, the equations of the best-fit lines are reported.

 
Cluster analysis (K means) was performed on the EMG data of all subjects by including in the analysis both amplitude and median frequency changes, with each being computed as the ratio of the last and first minute of tonic contraction. When n = 2 clusters were imposed to the algorithm, the analysis divided the subjects into two equal-size groups. It turned out that the two groups had values smaller or larger than 1.5. For simplicity, we will label the groups as fatigue and no-fatigue groups, respectively, even if the range of the indexes of the latter group is from 0.98 and 1.45, meaning that some subjects of this group showed minimal EMG signs of fatigue.

For each group, intermediate indexes of fatigue were also calculated by means of the above formula for the successive minutes, where the minute 5 data were sequentially changed with the data of minutes 2, 3, and 4. Figure 3A reports the results for the fatigue group, and Fig. 3B reports results for the no-fatigue group. It can be appreciated that, in the former group, the intermediate EMG indexes of fatigue monotonically increased from the first to the last minute of the contraction period, whereas the same indexes remained stationary in the latter group.



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  		Fig. 3. Indexes of fatigue calculated from the EMG variables (amplitude and median frequency) for each successive minute of the isometric neck muscle contraction. The mean indexes are reported for the subjects showing (A) and not showing (B) signs of fatigue. It can be seen that, in the former group, there was a progressive increase in the index values during the contraction period. The same mean indexes remained stationary in the latter group.

 
To further validate the EMG index of fatigue against an independent measure of fatigue, we measured the MVC of the dorsal neck muscles before and after the tonic contraction period. Then, we plotted the value of MVC after the tonic contraction (as percentage) of the initial MVC) against the EMG fatigue index. To this aim, 7 of the 10 subjects performed the two MVCs on a different day, the former before and the latter immediately after a 5-min period of dorsal neck tonic isometric contraction, against the same load they sustained in the first experimental session. On average, the MVC recorded during the former trial was not different from that measured during the first experimental session (n = 7; MVC = 26.4 ± 5.9 kg). Because three of the original subjects could not participate in this evaluation, to strengthen the validation procedure we increased the population by recruiting six additional subjects (n = 6; MVC = 28.1 ± 2.4 kg). These subjects were subjected to the same procedure for measurement of MVC and EMG as the original subjects, and the load was chosen to be in the same range (11.3 ± 1.4 kg). Figure 4 shows that the percent drop in MVC induced by the tonic contraction significantly increased [y = –0.12x + 1.08; r2 = 0.43; F(1,11) = 8, 16; P = 0.015] with the increase in the EMG fatigue index.



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  		Fig. 4. Percent drop in maximal voluntary contraction (MVC) induced by the tonic contraction (MVC immediately after contraction divided by MVC before contraction period) plotted against the fatigue index for 13 subjects. Despite great variability, the regression was significant. The best-fit line is plotted, and its equation is reported.

 
The index was then used for further analysis of the fatigue effects on stepping behavior, assuming that changes in the EMG index correlated with peripheral fatigue (29).

Kinematic recording and processing.   Body movement was recorded by the ELITE System (Bioengineering Technology and Systems) with eight infrared cameras. The reflective spherical markers were attached to the skin on the right and left anterior-superior iliac spine and to an adjustable helmet in these following positions: vertex of the head, forehead (the central point between the two temples), and lateral left and lateral right positions (the left and right temples, respectively). The helmet was removed during the fatiguing procedure and then repositioned, always in the same position, during the stepping trials. Before the helmet was removed, a sign of its position was made on the skin.

The markers' positions were sampled at a frequency of 100 Hz. The body movement was obtained by computing the midpoint (average of the coordinates) between the left and the right anterior-superior iliac spine marker positions. The resulting point, which was labeled body midpoint, could be considered a good approximation of the displacements of the center of mass. In the working space, subjects were positioned at the starting point with their mediolateral (M-L) body axis along the working space x-axis and their anteroposterior (A-P) body along the y-axis. Figure 5A shows an example of body midpoint path in the working field during a stepping-in-place trial. The x values of the body midpoint path vs. time and the y values vs. time were fitted with a polynomial function, the order of which minimized the mean squared error (Fig. 5B). In most cases, the algorithm chose a 10th-order polynomial as the best fit. By plotting the x vs. y interpolating polynomials, we obtained the interpolated path. In Fig. 5A, this is superimposed on the acquired body midpoint path. The mean squared errors have been taken as a measure of the body midpoint sway (in the x- and y-axes) around the main direction of displacement. The displacement of the subjects in the working space was quantified by the A-P and the M-L displacement of the body midpoint on the x-y plane. A-P displacements were calculated as the differences between the y coordinates of the body midpoint at the starting point and at the final point, whereas the M-L displacements were the differences between the x coordinates of the same points.



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  		Fig. 5. A: example of body midpoint path in the working field for one trial of one subject during the stepping in place with eyes closed under control condition. In this case, the subject showed a forward progression of ~1 m during the 30-s stepping trial. The step-by-step body midpoint mediolateral (M-L) oscillation of <10 cm is clearly evident along the x-axis. The gray line, superimposed on the body midpoint path, is the interpolated curve that minimized the squared mean error. B: projections of the instantaneous positions of the body midpoint on the M-L (top) and anteroposterior (A-P; bottom) plane. Superimposed on these projections are the respective interpolated curves.

 
To compare the postcontraction displacement changes across the subjects despite the possible different directions (forward or backward) of the postcontraction paths, an A-P index of displacement was calculated. For each subject, it was defined as the A-P displacement of the first trial of the first postcontraction trial (postcontraction 1) minus the mean value of the A-P displacement of the control trials, divided by the sum of the absolute values of these two numbers. This procedure weights the differences against the absolute magnitude of the traveled paths. A positive sign of the index meant A-P forward displacement, and a negative sign meant A-P backward displacement.

Head movements were computed on the basis of the angle between the line joining the helmet vertex to the helmet frontal marker and the vertical axis versor (head pitch), and on the basis of the angle between the line joining the helmet lateral right marker to the helmet lateral left marker and the vertical axis versor (head roll).

Cadence recording.   The cadence was recorded by the PedarMobile Insole System (Novel, München, Germany). The analog signal provided by the insole sensors was sampled at a frequency of 50 Hz, and the data were stored in the memory card to leave a subject free to move without cable constraints. After each acquisition block, the data were stored on a personal computer. The cadence was computed from the number of stance phases over time.

Statistical analysis.   To test the significance of the differences in the computed variables and parameters across the stepping trials of the control block (before isometric contraction), the postcontraction 1 block, the recovery block, and the postcontraction 2 block, a two-way repeated-measures ANOVA (blocks and trials) was used. This analysis was separately performed on the two groups of subjects (fatigue and no-fatigue groups), divided on the cluster analysis mentioned before. To check for a significant main effect of fatigue on A-P displacement for group, both groups were analyzed together in a three-way ANOVA (fatigue vs. no-fatigue group, blocks and trials). A two-way repeated-measures ANOVA (blocks and trials) was used to test for repetition effects on A-P displacement during stepping in place in the no-load trials; all subjects collapsed. A three-way repeated-measure ANOVA (load vs no-load, blocks and trials) in the group of five subjects who showed the highest EMG fatigue indexes was used for assessing possible repetition effects, as opposed to fatiguing tonic contraction effects, on A-P displacement. When appropriate, the Newman-Keuls test was used for post hoc comparisons. Between the two groups, the mean indexes of fatigue and the corresponding mean indexes of A-P displacement were compared by means of the Student's nonpaired t-test. When necessary, a linear regression analysis was carried out. The level of significance at which the null hypothesis was rejected was always equal to P < 0.05.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Body midpoint path under control condition.   The covered path during the stepping-in-place trials was quite variable from subject to subject, even during the block of control trials. Nevertheless, it was possible to identify two dominant behaviors. Some subjects moved forward some distance along their sagittal plane (Fig. 6, subject A). Other subjects remained almost in place, and the movement of their body midpoint generated a winding line covering a circumscribed area around the starting point (Fig. 6, subject B). The behavior of each subject was quite consistent within the trials of the control block. The sway of the body midpoint, which was connected to the pelvis movement during the shift of the body weight from one foot to the other, was evident in all subjects and trials. This was filtered out by the interpolating procedure that gave the body midpoint path along the heading direction. Across the subjects, large A-P displacements corresponded to long interpolated paths. This denotes that during the stepping-in-place trials the predominant movement was along the A-P plane, since, if a trial were characterized by conspicuous shifts of the body midpoint from the straight-ahead direction, the length of its interpolated path would be greater than the mean distance of its A-P displacement. When all the control trials from all subjects were gathered into two groups, one showing and one not showing EMG signs of fatigue (on the basis of the fatigue index) and separately averaged, the mean value of the A-P distance covered in the forward direction was equal to 48.7 ± 19.3 and 34.5 ± 17.2 cm (means ± SE; no-fatigue and fatigue groups, P = 0.56).



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  		Fig. 6. Examples of different body midpoint displacements taken from 2 subjects, different from that of Fig. 5, during the stepping in place under control condition. Although subject A (A) exhibited a forward progression of ~40 cm, subject B (B) almost stepped on the spot throughout the 30-s trial. {circ}, Starting point (at y = –140 cm and x = 30 cm).

 
Qualitative effects of the isometric contraction of dorsal neck muscles on the body midpoint path.   The isometric contraction of the dorsal neck muscles did not produce the same changes in the body midpoint path in all the subjects. During the trials performed in the period after the first contraction (postcontraction 1), some subjects basically reproduced the same path already seen during the control blocks. It turned out that, in these subjects, the neck muscle EMG signals during the isometric contraction showed no or negligible signs of fatigue and so did the index of fatigue. On the contrary, other subjects showed a different body midpoint path from that of the control block trials. Figure 7 shows the paths of the first and the fifth trial of each block for two representative subjects (subjects A and B), in whom the neck muscle EMG during the isometric contraction showed clear-cut signs of fatigue. The graphs of the first trial after the contraction period (postcontraction 1) showed different paths between the first and fifth trial of the control block. In particular, the subject who, during the control trials, moved forward (subject A) in this first trial remained roughly in place, just behind the starting point. During the trials after the rest period (recovery block), the paths tended to recuperate the feature of the control trials without really reproducing it. This means that, even after a rest period of 30 min, this subject was unable to reach a complete recovery. On the other hand, the subject who during the control trials remained in place (subject B) moved backward after contraction, taking away from the starting point. The effects of the isometric contraction were also reproduced in the first trial of the period after the second contraction (postcontraction 2). As shown in the bottom graphs of Fig. 7, both subjects moved backward, farther from the starting point.



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  		Fig. 7. Examples of body midpoint paths in the working field for 2 subjects (A and B) during the stepping in place with closed eyes under each of the 4 experimental conditions (from top to bottom: control, postcontraction 1, recovery, and postcontraction 2). For each condition, the 2 columns correspond to the first and last (5th) stepping trials of each subject. Under all conditions, the stepping trials began at the same spot (open circle in each graph at x = 30 and y = –140 cm). Subject A reversed his forward displacement in the first trial after the first period of isometric dorsal neck muscle contraction; in the first trial after the second contraction period, his displacement was directed backward. At the 5th stepping trial of postcontraction 2, the backward displacement disappeared. Subject B moved backward from the beginning, but his backward displacement was much larger in the first trials of the postcontraction blocks 1 and 2. Also in this case, the last trials of the postcontraction blocks were similar to the control trials.

 
Mean A-P displacement of body midpoint in the two groups of subjects: the effect of fatigue.   The mean differences in the A-P displacement and in the traveling direction (forward or backward) were separately analyzed in the subjects showing and not showing signs of fatigue based on the magnitude of the EMG index of fatigue (see METHODS). The subjects could in fact be clustered into two groups, which had significantly different mean indexes of fatigue (fatigue group, index of fatigue of >1.5, 2.302 ± 0.31; no-fatigue group, index of fatigue of <1.5, 1.146 ± 0.19; P < 0.001).

The corresponding mean indexes of displacement (A-P index) were for the fatigue group –0.49 ± 0.33 and for the no-fatigue group 0.0 ± 0.17 (P < 0.05). Figure 8 shows the A-P indexes calculated for the first stepping trial after the first isometric contraction period vs. the fatigue index of each subject. It is possible to appreciate that, when the fatigue index assumed values lower than 1.5, the A-P index was very close to zero, whereas when the fatigue index was greater than 1.5, the A-P index assumed much lower, negative values. It can also be seen that, despite a considerable variability, there was a significant inverse relationship between the two indexes [the equation of the best-fit line was y = –0.41x + 0.46; R2 = 0.56; F(1,8) = 10.473; P = 0.011].



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  		Fig. 8. For each subject, the A-P index has been plotted vs. the fatigue index (see METHODS). An A-P index equal to zero indicates no changes in the displacement along the A-P axis, whereas a negative value indicates a backward displacement after the first isometric contraction period. Across the subjects, the A-P indexes showed greater negative values as a function of increasing fatigue indexes. {bullet}, Subjects of the no-fatigue group; {blacksquare}, subjects of the fatigue group.

 
Figure 9 shows the mean values of the body midpoint A-P displacements of the fatigue (Fig. 9A) and no-fatigue groups (Fig. 9B) for each of the successive stepping trials. When both groups were analyzed together in a three-way ANOVA (fatigue vs. no-fatigue group, blocks and trials) to check for a significant main effect on A-P displacement for group, no significant differences were found between groups [F(1) = 0.66; P = 0.44]. There was no effect for trials [F(4) = 0.79; P = 0.54] and a marginal effect for blocks [F(3) = 2.65; P = 0.07]. However, there was an interaction between blocks and trials [F(12) = 2.44; P = 0.008] and between groups, blocks, and trials [F(12) = 1.88; P = 0.045]. In particular, the post hoc test showed no difference between the trials of the control blocks of the two groups (P > 0.02 for all comparisons). But there were significant differences between the two groups in the first trials of the second blocks (postcontraction 1, P = 0.031) and in the first trials of the fourth blocks (postcontraction 2, P = 0.0017).



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  		Fig. 9. A and B: mean values (+SE) of the body midpoint A-P displacements for all subjects of the fatigue (A) and no-fatigue (B) group for each of all successive stepping trials under all experimental conditions. Reduction of the A-P displacement is obvious in the first trials of the postcontraction periods 1 and 2 (Post C1 and Post C2, respectively; shaded bars) in the fatigue but not in the no-fatigue group. C and D: mean values (+SE) of the body midpoint M-L displacements for all the subjects, grouped as above. M-L displacements were not affected by the contraction periods 1 and 2 in either group. E and F: neither the first nor second contraction period produced significant M-L deviations of the path, as assessed by the SD (along the x-axis) of the interpolated path. Contr, control condition.

 
The fatigue group was characterized by a reduced A-P displacement in some postcontraction 1 trials as well as in some postcontraction 2 trials with respect to the control trials. Two-way ANOVA showed that, although there were no differences between blocks [F(3) = 1.999; P = 0.168] or between trials [F(4) = 0.313; P = 0.865], there was an interaction between blocks and trials [F(12) = 2.319; P = 0.019]. The post hoc test showed that the significant reduction in A-P displacement was present for the mean values of the first trials of the postcontraction 1 (compared with all control trials) and 2 (compared with all control and recovery trials) blocks (P < 0.03 for all comparisons). The successive trials of postcontractions 1 and 2 showed a progressive but incomplete recovery toward control mean values.

In the subjects showing only mild or no sign of fatigue, the A-P displacements remained unchanged across the different blocks and trials [2-way ANOVA; blocks, F(3) = 0.849, P = 0.493; trials, F(4) = 0.775, P = 0.557]. There was a significant interaction between blocks and trials [F(12) = 2.029; P = 0.042]: the post hoc test showed a significant effect limited to the difference between the first trial of the last block (postcontraction 2 blocks) and the last trial of the control block (P = 0.030).

A-P displacement of body midpoint under no-load condition.   When the same subjects stepped in place (4 blocks of 5 subsequent stepping trials each), but this time without any interposed period of head extensor effort (no-load session), no effect of the repetition of the stepping trials on the body A-P displacement was seen. The two-way ANOVA applied to the A-P displacement of all block and trials in all subjects collapsed (n = 10) gave neither a significant main effect [blocks, F(3) = 2.295, P = 0.100; trials, F(4) = 1.116, P = 0.364] nor a significant interaction [F(12) = 1.05; P = 0.409]. The ANOVA was then applied to the subjects belonging to the fatigue group alone, with the aim of comparing their A-P displacement between the two experimental conditions (isometric contraction vs. no load). The three-way ANOVA (condition, block, trial) gave no significant effect for conditions [F(1) = 0.008; P = 0.932] and trials [F(4) = 0.213; P = 0.930] but a main effects for blocks [F(3) = 3.603; P = 0.028]. There was a significant interaction (condition, block, trial) [F(12) = 1.983; P = 0.034]. In particular, the post hoc test indicated that the first trials of the second and fourth block of the load condition exhibited a smaller A-P displacement (second block, P = 0.049; fourth block, P = 0.001) than the corresponding trials of the no-load condition.

Mean M-L displacement of body midpoint in the two groups of subjects: the effect of fatigue.   The M-L displacements, computed as the difference between the x coordinates of the starting and final points, were always small in the control trials in the two groups. This behavior remained unchanged in all subsequent trials, independently of the experimental condition and group (Fig. 9, C and D). The two-way ANOVA applied to the fatigue group gave neither significant main effects [blocks, F(3) = 0.631, P = 0.609; trials, F(4) = 0.573, P = 0.686] nor significant interaction [F(12) = 1.903; P = 0.058]. The two-way ANOVA applied to the no-fatigue group gave neither significant main effects [blocks, F(3) = 1.603, P = 0.240; trials, F(4) = 1.835, P = 0.172] nor significant interaction [F(12) = 0.342; P = 0.977]. To make sure that the subjects did not proceed along a winding trajectory during the stepping-in-place trials to eventually stop at a point lying along the initial straight-ahead line, the mean standard deviation of the interpolated path was computed. As shown in Fig. 9, E and F, neither contraction condition produced significant changes in the mean standard deviation. The two-way ANOVA applied to the mean standard deviation values of the interpolated path in the fatigue group gave neither significant main effects [blocks, F(3) = 0.205, P = 0.891; trials, F(4) = 0.176, P = 0.947] nor significant interaction [F(12) = 0.417; P = 0.949]. The two-way ANOVA applied to the no-fatigue group gave neither significant main effects [blocks, F(3) = 1.23, P = 0.341; trials, F(4) = 2.146, P = 0.122] nor significant interaction [F(12) = 1.949; P = 0.513]. Therefore, we conclude that subjects did not significantly deviate from a straight pathway under any experimental condition.

Body sway during stepping in place.   There were no a priori reasons for excluding the possibility that fatigue increased the body sway during stepping in place and that such instability, in turn, could be at least in part be responsible for the observed changes in the path of the postcontraction stepping trials. The body midpoint sway around the main body midpoint direction of displacement was evaluated on the basis of the mean squared error made by the path interpolation. This parameter estimated how much the actual path differed from the interpolated path and, therefore, to what extent the subjects swayed on the spot by moving the body weight from one foot to the other during stepping in place. As shown in Fig. 10, A and B, fatigue did not increase body sway, neither in the A-P axis nor on the M-L axis. The two-way ANOVA applied to the A-P data of the fatigue group gave neither significant main effects [blocks, F(3) = 0.404, P = 0.753; trials, F(4) = 0.786, P = 0.551] nor significant interaction [F(12) = 0.779; P = 0.668]. The two-way ANOVA applied to the M-L data of the fatigue group gave neither significant main effects [blocks, F(3) = 2.013, P = 0.166; trials, F(4) = 1.013, P = 0.430] nor significant interaction [F(12) = 1.907; P = 0.057].



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  		Fig. 10. Body midpoint sway around the main body midpoint direction of displacement was obtained by the interpolation of the actual path and the computation of its mean squared error (MSE). The average value (+SE) of MSE is shown for all trials of the subjects belonging to the fatigue group. Fatigue (either Post C1 or Post C2 trials; shaded bars) did not increase body sway either in the A-P (A) or M-L axis (B).

 
Head position during stepping in place.   The position of the head was measured to check whether the isometric contraction of the dorsal neck muscles provoked flexion or extension of the head, since these modifications could be one of the possible causes of the fatigue-induced variations of the path. The mean values of pitch angle as well as roll angle did not show differences among the trials (Fig. 11). The two-way ANOVA applied to the pitch angle data of the fatigue group gave neither significant main effects [blocks, F(3) = 1.715, P = 0.217; trials, F(4) = 1.68, P = 0.951] nor significant interaction [F(12) = 1.041; P = 0.428]. The two-way ANOVA applied to the pitch angle data of the no-fatigue group gave neither significant main effects [blocks, F(3) = 1.749, P = 0.210; trials, F(4) = 0.647, P = 0.637] nor significant interaction [F(12) = 1.037; P = 0.432]. The two-way ANOVA applied to the roll angle data of the fatigue group gave neither significant main effects [blocks, F(3) = 1.780, P = 0.204; trials, F(4) = 0.309, P = 0.867] nor significant interaction [F(12) = 0.547; P = 0.872]. The two-way ANOVA applied to the roll angle data of the no-fatigue group gave neither significant main effects [blocks, F(3) = 0.508, P = 0.684; trials, F(4) = 0.201, P = 0.934] nor significant interaction [F(12) = 1.952; P = 0.051]. Therefore, the isometric contraction of the dorsal neck muscles, even when it reached a fatiguing level, did not affect the position of the head during stepping in place.



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  		Fig. 11. Mean values (+SE) of the head pitch angle (A and B) and head roll angle (C and D) for all the subjects of the fatigue (A and C) and no-fatigue (B and D) groups for each of all successive stepping trials under all experimental conditions. The mean angles were not different among the trials of either group.

 
Stepping-in-place cadence.   The mean stepping cadence under control conditions was not significantly different between the fatigue and the no-fatigue groups (54.0 ± 3.5 and 59.3 ± 5.2 steps/min, respectively). There were minor effects of isometric neck muscle contraction on stepping cadence. The two-way ANOVA applied to the fatigue group gave neither significant main effects [blocks, F(3) = 2.172, P = 0.144; trials, F(4) = 0.185, P = 0.943] nor significant interaction [F(12) = 1.645; P = 0.111]. The two-way ANOVA applied to the no-fatigue group gave a significant main effects for trials [blocks, F(3) = 0.217, P = 0.883; trials, F(4) = 3.347, P = 0.036] but no significant interaction [F(12) = 0.849; P = 0.602]. The significant changes between trials in cadence in the no-fatigue group were due to a very minor augmentation from the first to the last trials (from 59.7 to 60.3 steps/min, all blocks collapsed), i.e., to less than one additional step over the entire period (30 s) of acquisition. To further check that even any nonsignificant variation in cadence in the fatigue group could be one of the possible causes of the path alteration and of the A-P displacement reduction during the first trial of postcontraction 1 and postcontraction 2, the A-P index was plotted vs. the percent cadence change in the first trial after fatigue (with respect to the mean cadence in the 5 control trials) for each subject of the fatigue group. The regression analysis gave no significant relationship [R2 = 0.0002; F(1,3) = 0.00067; P = 0.981].


   DISCUSSION
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During stepping in place, before the prolonged head extensor effort, the subjects presented a substantial variability in their behavior. Most of them had a tendency to slowly proceed along the subject's sagittal plane, and some showed a mild M-L displacement. Only a few subjects really did step in place. Across the subjects, the mean progression of the body midpoint was in the forward direction, whereas the displacement in the M-L direction was, on average, close to zero. In all cases, no subject was aware of his or her displacement in the walking space. The extent of the forward progression of the subjects changed significantly after the 5-min period of tonic contraction of the dorsal neck muscles. In turn, the extent of this change depended on the degree to which the contraction produced muscle fatigue in the neck muscles.

Because the EMG can furnish an indirect measure of fatigue in the muscle of interest under conditions of controlled isometric contraction (64), an EMG index was used to quantify the muscle contraction level across the subjects. This index depended on EMG changes in both amplitude and median frequency occurring during the period of isometric dorsal neck muscle contraction. Indeed, the changes in these two variables were highly correlated within several subjects of our population, regardless of gender and weight, whereby the EMG amplitude gradually increased together with a gradual decrease in EMG median frequency during the contraction period. In other subjects, this correlation was not evident, since EMG amplitude and median frequency showed no sizeable changes during the contraction period. The relationship between EMG index and fatigue was also shown by the significant regression, across 13 subjects, between the percent decrease in MVC produced by the tonic contraction and the fatigue index. On these bases, we assumed that the EMG index was a good marker of muscle fatigue, and we used it for dividing all our subjects into two subgroups.

In the subjects showing EMG signs of neck muscle fatigue, the forward displacement during the stepping-in-place trials proved to be much reduced (to 32%, on average) immediately after the 5-min period of tonic contraction with respect to the stepping trials performed under control conditions. Some subjects even stepped in the backward direction. This behavior was obvious only in the first trial immediately after the fatiguing period, a sign of relatively rapid recovery from the fatigue effects, in keeping with recent reports from other investigations (16). However, it was reproduced and even enhanced in the first trial of the second series of the stepping trials performed after the second fatiguing session, where the average displacement was in the backward direction. This would point to a residual effect of the first fatiguing contraction that had not completely vanished at the end of the recovery period of 30 min and added to the effects of the second fatiguing contraction (67). Shorter bouts of back muscle fatiguing contraction recover earlier (41). This behavior was not obvious in those subjects for whom dorsal neck muscle contraction did not show or showed only minor EMG signs of fatigue.

All subjects also participated in an additional session, when they were asked to step in place and perform the same sequence of blocks and trials but without the tonic isometric contraction of the dorsal neck muscles (no-load session). The repetition of the stepping trials per se did not produce significant effects on the body displacement. This strengthens the notion that the cause of the observed reduced forward progression or backward displacement was the neck muscle contraction rather than some process connected with the repetition of the trials or with the feedback received by subjects being repositioned at the starting point after each trial.

When we searched for a graded change in the body progression along the sagittal plane by plotting the A-P index of displacement against the EMG index of fatigue, it turned out that, despite a considerable variability (likely connected to individual anthropometric characteristics, to peculiarity of the stepping task, and to the magnifying effects of the ratios used for computing the indexes), the relevant changes in the displacements along the sagittal plane after contraction were again evident only in the subjects in whom the contraction produced clear-cut EMG signs of fatigue. This finding is also in favor of a rather selective role of fatigue, rather than prolonged contraction per se, in producing the effects and also strengthens the EMG criteria for separating the subjects into two groups.

Body unsteadiness during stepping?   Dorsal neck muscle contraction, be it fatiguing or not, did not produce abnormal oscillations around the interpolated stepping path of the body midpoint during stepping, which would happen if a subject's body midpoint became unusually unsteady around the mean position. This might have been assumed on the basis of a previous study, in which dorsal neck muscle fatigue was able to produce moderate but significant increases in body sway during quiet stance (4). It should be noted, however, that the increase in body sway during quiet stance that was described in that paper was not associated with any major change in the center of foot pressure (forward, backward, or sideways), which might have entrained directional effect in the body displacement during the stepping in place. However, any correspondence between body oscillations under static (quiet bipedal stance) and dynamic condition (stepping in place) must be considered with caution, because in the latter case balance control heavily depends on the alternate shift of the body weight on a single support.

The fatigue-induced changes in the A-P displacement during the stepping-in-place task were not dependent on changes in head posture. In fact, head position did not change postcontraction, either in pitch or roll angle, either with or without signs of fatigue. The fact that the head remained in place despite the fatigue of the head extensor muscles was likely dependent on the very low level of force necessary to counteract the gravity-dependent head flexion, a level of force easily produced even by heavily fatigued muscles. Possibly, the production of the appropriate dorsal neck muscle tone was also aided by a mechanism of minimization of the change in the discharge from the gravito-inertial labyrinthine receptors. Certainly, vision could not help, since the subjects were blindfolded during the stepping phase. In turn, the absence of excessive body midpoint oscillations during stepping could be favored by a mechanism of head-referenced body stabilization, the importance of which in the postural control system and inertial guidance of locomotion has been already emphasized by Pozzo and coworkers (53).

Putative neural mechanisms.   Neck muscles are surely central in the construction of a reference frame for movement in space. Such a role is apparently not played by the leg muscles involved in the production of body movement, at least as indicated by the minor effect of bilateral triceps surae vibration during walking (13). It is therefore in that light that we would like to propose an explanation of the observed phenomenon. In so doing, it seems useful to discuss the present data, together with those of the studies describing the effects of dorsal neck muscle vibration, in the line of the process of multisensory fusion that leads to egocentric space representation.

During stepping in place, neck vibration produces involuntary forward stepping at about 0.3 m/s without modifying the stepping frequency (32). In our case, neck muscle fatigue instead induced an involuntary smaller forward progression or even backward progression. The difference between the effects of fatigue and vibration cannot be ascribed to the more aspecific distribution of fatigue, since the concurrent EMG recording from the anterior neck muscles showed no sign of activation of these muscles. Similar to vibration, the stepping cadence did not undergo major changes as a consequence of neck muscle fatigue. The small changes in cadence observed were unrelated to the distance or direction of body displacement during the stepping. Apparently, the central effects of both vibration and fatigue do not influence the rhythmic outflow from the central pattern generators implicated in this automatic locomotor-like stepping activity.

Perhaps, the changes in body progression along the sagittal plane should be attributed to the outflow from the neck muscles to the brain centers responsible for building the body spatial reference frame. Vibration and fatigue both produce modifications in joint position sense (for vibration, see Refs. 9, 20, 22, 30, 31; for fatigue, see Refs. 12, 16, 24, 26, 57, 59). This testifies of the capacity of the afferent input from dorsal neck muscles of accessing the central nervous system and altering the perception of the position of the segments in space. However, the fatigue state and vibration effects dramatically diverge as far as the modification in the presumed reference frame for controlling locomotion is concerned. Fatigue reduces the forward distance reached by subjects who normally exhibit a forward progression and pushes clearly backward those who stepped in place.

This would speak in favor of a different set of receptors and afferent fibers under vibration and fatiguing contraction conditions, indirectly or directly responsible for the modulation of the reference frame. In particular, the receptors responsible for the "shrinkage" of our imagined space in the forward direction or for the "backward displacement" of the body position reference after fatigue would be different from those possibly activated by muscle contraction per se (like tendon organs or muscle spindles). Rat experiments have shown that fatigue activates small-fiber receptors, the same that are activated by capsicine (52). Small-fiber sensory input may be the result of an increased inflow from the free nerve endings as a consequence of ionic or metabolic changes (elevated interstitial potassium concentration or insufficient oxygen availability due to reduced blood flow) (19, 52). This input, in addition to inhibiting muscle spindle afferent activity during fatigue (10), could also directly access the brain centers responsible for shaping our reference frames for navigation. Interestingly, abnormal conditions of the neck muscle (tension neck) can disrupt the normal postural response to neck muscle vibration (40), pointing to a susceptibility of the reference system to abnormal fatigue-related inputs of neck muscle origin.

Admittedly, fatigue can affect the discharge of many sensory receptors, including muscle spindles (27, 34, 63, 64, 67). In turn, spindle discharge could be modulated by fatigue-induced alterations in gamma-motoneuron discharge (43, 51). Such abnormal muscle spindle inflow could possibly perturb and deteriorate postural control through an action on the central nervous system (19). However, one may note that there was no neck muscle contraction during the stepping trials and presumably little spindle discharge, since the latter should not outlast previous contraction, contrary to the discharge of the receptors sensitive to fatigue-induced intramuscular changes. Any modulation of a scarce proprioceptive input would therefore hardly produce the gross effects shown here in body progression, emphasizing a direct effect of fatigue-related input as a cause of the abnormal progression after the fatiguing contraction.

Neck muscle fatigue effects on locomotion.   Stepping in place with closed eyes and without acoustic cues is a nonoptimal definition for a locomotor task and presents itself with peculiar characteristics from subject to subject (7). The drift from the starting position is a sign of unreliable feedback during stepping in place (61). Most likely, many sensory modalities normally able to convey velocity and direction information, such as the foot sole receptors and their central integration, are below the threshold under these circumstances, or the central mechanisms for calculating the mismatch between the successive positions of the two leg can be fooled by the minimal differences of their positions between steps. The gravito-inertial receptors would also be of no use, given that the successive head and body up and down movements do not seem to be influenced by the body progression and that the linear body velocity in the midsagittal plane is negligible even when it reaches its maximum value (~3 cm/s) (25). Certainly, no subject was aware of his or her displacement in the working space, either before or after the fatigue-induced effects. And this comes as no surprise, since much larger body displacement produced by lateral neck muscle vibration during stepping in place went completely unnoticed by the subjects (4). Therefore, the body displacement would be the expression of the spontaneous drift in the activity of the brain centers controlling the body position in space. This command center, although numb to the afferent sensory input from the evolving movement, is, however, sensible to other afferent inputs like that from fatigued neck muscles. Despite the highly variable body displacement across subjects, the relative consistency of this displacement in the different trials within a subject could be taken as an indication that the subjects' reference for the stepping position can be relatively stable. It seems, therefore, that stepping in place after neck muscle fatigue is being performed with respect to a reference system and modified in the same sense by the fatigue-induced input in every subject. Such a modification could be reminiscent of an error of parallax, as if the brain would incorporate depth information when it updates its stored representations of space after the neck muscle fatiguing contraction (45).


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ACKNOWLEDGMENTS
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This work was supported by grants from the Italian Ministry of Health (Ricerca Finalizzata 2002) and Ministry of University and Research (Progetto Ricerca Interesse Nazionale 2003, Fondo Investimenti Ricerca di Base 2002).


   ACKNOWLEDGMENTS
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
The help of M. V. Beretta and A. M. De Nunzio during data collection is gratefully acknowledged. We thank two unknown referees for critical reading and detailed suggestions.


   FOOTNOTES
 

Address for reprint requests and other correspondence: M. Schieppati, Centro Studi Attività Motorie (CSAM), Fondazione Salvatore Maugeri (IRCCS), Istituto Scientifico di Pavia, Via Ferrata 8, I-27100 Pavia, Italy (E-mail: mschieppati{at}fsm.it)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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 REFERENCES
 

  1. Biguer B, Donaldson IM, Hein A, and Jeannerod M. Neck muscle vibration modifies the representation of visual motion and direction in man. Brain 111: 1405–1424, 1988.[Abstract/Free Full Text]
  2. Bottini G, Karnath HO, Vallar G, Sterzi R, Frith CD, Frackowiak RS, and Paulesu E. Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration. Brain 124: 1182–1196, 2001.[Abstract/Free Full Text]
  3. Bove M, Diverio M, Pozzo T, and Schieppati M. Neck muscle vibration disrupts steering of locomotion. J Appl Physiol 91: 581–588, 2001.[Abstract/Free Full Text]
  4. Bove M, Courtine G, and Schieppati M. Neck muscle vibration and spatial orientation during stepping in place in humans. J Neurophysiol 88: 2232–2241, 2002.[Abstract/Free Full Text]
  5. Brandt T, Krafzcyk S, and Malsbended I. Postural imbalance with head extension: improvement by training as a model for ataxia therapy. Ann NY Acad Sci 374: 636–649, 1981.[Web of Science][Medline]
  6. Brandt T and Bronstein AM. Cervical vertigo. J Neurol Neurosurg Psychiatry 71: 8–12, 2001.[Free Full Text]
  7. Brenière Y. Why we walk the way we do. J Mot Behav 28: 291–298, 1996.[Web of Science][Medline]
  8. Brenière Y and Ribreau C. A double-inverted pendulum model for studying the adaptability of postural control to frequency during human stepping in place. Biol Cybern 79: 337–345, 1998.[CrossRef][Web of Science][Medline]
  9. Brumagne S, Lysens R, Swinnen S, and Verschueren S. Effect of paraspinal muscle vibration on position sense of the lumbosacral spine. Spine 24: 1328–1331, 1999.[CrossRef][Web of Science][Medline]
  10. Brunetti O, Della Torre G, Lucchi ML, Chiocchetti R, Bortolami R, and Pettorossi VE. Inhibition of muscle spindle afferent activity during masseter muscle fatigue in the rat. Exp Brain Res 152: 251–262, 2003.[CrossRef][Web of Science][Medline]
  11. Burke D, Hagbarth KE, Lofstedt L, and Wallin BG. The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol 261: 673–693, 1976.[Abstract/Free Full Text]
  12. Carpenter JE, Blasier RB, and Pellizzon GG. The effects of muscle fatigue on shoulder joint position sense. Am J Sports Med 26: 262–265, 1998.[Abstract/Free Full Text]
  13. Courtine G, Pozzo T, Lucas B, and Schieppati M. Continuous, bilateral Achilles' tendon vibration is not detrimental to human walk. Brain Res Bull 55: 107–115, 2001.[CrossRef][Web of Science][Medline]
  14. Duclos C, Roll R, Kavounoudias A, and Roll JP. Long-lasting body leanings following neck muscle isometric contractions. Exp Brain Res 158: 58–66, 2004.[Web of Science][Medline]
  15. Eklund G. General features of vibration-induced effects on balance. Ups J Med Sci 77: 112–124, 1972.[Web of Science][Medline]
  16. Elfving B, Liljequist D, Dedering A, and Nemeth G. Recovery of electromyograph median frequency after lumbar muscle fatigue analysed using an exponential time dependence model. Eur J Appl Physiol 88: 85–93, 2002.[CrossRef][Web of Science][Medline]
  17. Forestier N, Teasdale N, and Nougier V. Alteration of the position sense at the ankle induced by muscular fatigue in humans. Med Sci Sports Exerc 34: 117–122, 2002.[CrossRef][Web of Science][Medline]
  18. Fransson PA, Karlberg M, Sterner T, and Magnusson M. Direction of galvanically-induced vestibulo-postural responses during active and passive neck torsion. Acta Otolaryngol (Stockh) 120: 500–503, 2000.
  19. Garland SJ. Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol 435: 547–558, 1991.[Abstract/Free Full Text]
  20. Goodwin GM, McCloskey DI, and Matthews PB. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 175: 1382–1384, 1972.[Abstract/Free Full Text]
  21. Grasso R, Prevost P, Ivanenko YP, and Berthoz A. Eye-head coordination for the steering of locomotion in humans: an anticipatory synergy. Neurosci Lett 253: 115–118, 1998.[CrossRef][Web of Science][Medline]
  22. Gregory JE, Morgan DL, and Proske U. Aftereffects in the responses of cat muscle spindles and errors of limb position sense in man. J Neurophysiol 59: 1220–1230, 1988.[Abstract/Free Full Text]
  23. Gurfinkel VS, Ivanenko YP, and Levik YS. The influence of head rotation on human upright posture during balanced bilateral vibration. Neuroreport 7: 137–140, 1995.[Web of Science][Medline]
  24. Hardin JA. The effects of muscle fatigue on shoulder joint position sense. Am J Sports Med 26: 262–265, 1998.[Abstract/Free Full Text]
  25. Harris LR, Jenkin M, and Zikovitz DC. Visual and non-visual cues in the perception of linear self-motion. Exp Brain Res 135: 12–21, 2000.[CrossRef][Web of Science][Medline]
  26. Hiemstra LA, Lo IK, and Fowler PJ. Effect of fatigue on knee proprioception: implications for dynamic stabilization. J Orthop Sports Phys Ther 31: 598–605, 2001.[Web of Science][Medline]
  27. Hill JM. Increase in the discharge of muscle spindles during diaphragm fatigue. Brain Res 918: 166–170, 2001.[CrossRef][Web of Science][Medline]
  28. Holtmann S, Clarke A, and Scherer H. Cervical receptors and the direction of body sway. Arch Otorhinolaryngol 246: 61–64, 1989.[CrossRef][Medline]
  29. Horita T and Ishiko T. Relationships between muscle lactate accumulation and surface EMG activities during isokinetic contractions in man. Eur J Appl Physiol Occup Physiol 56: 18–23, 1987.[CrossRef][Web of Science][Medline]
  30. Inglis JT and Frank JS. The effect of agonist/antagonist muscle vibration on human position sense. Exp Brain Res 81: 573–580, 1990.[CrossRef][Web of Science][Medline]
  31. Inglis JT, Frank JS, and Inglis B. The effect of muscle vibration on human position sense during movements controlled by lengthening muscle contraction. Exp Brain Res 84: 631–634, 1991.[Web of Science][Medline]
  32. Ivanenko YP, Talis VL, and Kazennikov OV. Support stability influences postural responses to muscle vibration in humans. Eur J Neurosci 11: 647–654, 1999.[CrossRef][Web of Science][Medline]
  33. Ivanenko YP, Grasso R, and Lacquaniti F. Neck muscle vibration makes walking humans accelerate in the direction of gaze. J Physiol 525: 803–814, 2000.[Abstract/Free Full Text]
  34. Johansson H and Sojka P. Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: a hypothesis. Med Hypotheses 35: 196–203, 1991.[CrossRef][Web of Science][Medline]
  35. Karlberg M, Persson L, and Magnusson M. Impaired postural control in patients with cervico-brachial pain. Acta Otolaryngol Suppl (Stockh) 520: 440–442, 1995.
  36. Karnath HO, Christ K, and Hartje W. Decrease of contralateral neglect by neck muscle vibration and spatial orientation of trunk midline. Brain 116: 383–396, 1993.[Abstract/Free Full Text]
  37. Karnath HO, Sievering D, and Fetter M. The interactive contribution of neck muscle proprioception and vestibular stimulation to subjective "straight ahead" orientation in man. Exp Brain Res 101: 140–146, 1994.[Web of Science][Medline]
  38. Kavounoudias A, Roll R, and Roll JP. Specific whole-body shifts induced by frequency-modulated vibrations of human plantar soles. Neurosci Lett 266: 181–184, 1999.[CrossRef][Web of Science][Medline]
  39. Kerkhoff G. Modulation and rehabilitation of spatial neglect by sensory stimulation. Prog Brain Res 142: 257–271, 2003.[Medline]
  40. Koskimies K, Sutinen P, Aalto H, Starck J, Toppila E, Hirvonen T, Kaksonen R, Ishizaki H, Alaranta H, and Pyykko I. Postural stability, neck proprioception and tension neck. Acta Otolaryngol Suppl (Stockh) 529: 95–97, 1997.
  41. Lariviere C, Gravel D, Arsenault AB, Gagnon D, and Loisel P. Muscle recovery from a short fatigue test and consequence on the reliability of EMG indices of fatigue. Eur J Appl Physiol 89: 171–176, 2003.[CrossRef][Web of Science][Medline]
  42. Lekhel H, Popov K, Anastasopoulos D, Bronstein A, Bhatia K, Marsden CD, and Gresty M. Postural responses to vibration of neck muscles in patients with idiopathic torticollis. Brain 120: 583–591, 1997.[Abstract/Free Full Text]
  43. Ljubisavljevic M and Anastasijevic R. Fusimotor system in muscle fatigue. J Peripher Nerv Syst 1: 83–96, 1996.[Medline]
  44. Lund S. Postural effects of neck muscle vibration in man. Experientia 36: 1398, 1980.[CrossRef][Web of Science][Medline]
  45. Medendorp WP, Tweed DB, and Crawford JD. Motion parallax is computed in the updating of human spatial memory. J Neurosci 23: 8135–8142, 2003.[Abstract/Free Full Text]
  46. Mergner T, Siebold C, Schweigart G, and Becker W. Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res 85: 389–404, 1991.[Web of Science][Medline]
  47. Mergner T, Huber W, and Becker W. Vestibular-neck interaction and transformation of sensory coordinates. J Vestib Res 7: 347–367, 1997.[CrossRef][Web of Science][Medline]
  48. Mergner T, Nasios G, Maurer C, and Becker W. Visual object localisation in space. Interaction of retinal, eye position, vestibular and neck proprioceptive information. Exp Brain Res 141: 33–51, 2001.[CrossRef][Web of Science][Medline]
  49. Merletti R and Lo Conte LR. Surface EMG signal processing during isometric contractions. J Electromyogr Kinesiol 7: 241–250, 1997.[CrossRef][Web of Science][Medline]
  50. Norre ME, Forrez G, and Beckers A. Clinical application of vestibulospinal reflex tests in peripheral vestibular disorders. Acta Otolaryngol Suppl 468: 337–339, 1989.[Medline]
  51. Pedersen J, Ljubisavljevic M, Bergenheim M, and Johansson H. Alterations in information transmission in ensembles of primary muscle spindle afferents after muscle fatigue in heteronymous muscle. Neuroscience 84: 953–959, 1998.[CrossRef][Web of Science][Medline]
  52. Pettorossi VE, Della Torre G, Bortolami R, and Brunetti O. The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat. J Physiol 515: 599–607, 1999.[Abstract/Free Full Text]
  53. Pozzo T, Berthoz A, and Lefort L. Head stabilization during various locomotor tasks in humans. I. Normal subjects. Exp Brain Res 82: 97–106, 1990.[Web of Science][Medline]
  54. Pyykko I, Enbom H, Magnusson M, and Schalen L. Effect of proprioceptor stimulation on postural stability in patients with peripheral or central vestibular lesion. Acta Otolaryngol (Stockh) 111: 27–35, 1991.
  55. Roll JP, Vedel JP, and Roll R. Eye, head and skeletal muscle spindle feedback in the elaboration of body references. Prog Brain Res 80: 113–123, 1989.[Web of Science][Medline]
  56. Schieppati M, Nardone A, and Schmid M. Neck muscle fatigue affects postural control in man. Neuroscience 121: 277–285, 2003.[CrossRef][Web of Science][Medline]
  57. Sharpe MH and Miles TS. Position sense at the elbow after fatiguing contractions. Exp Brain Res 94: 179–182, 1993.[Web of Science][Medline]
  58. Simoneau GG, Leibowitz HW, Ulbrecht JS, Tyrrell RA, and Cavanagh PR. The effects of visual factors and head orientation on postural steadiness in women 55 to 70 years of age. J Gerontol 47: 151–181, 1992.
  59. Skinner HB, Wyatt MP, Hodgdon JA, Conard DW, and Barrack RL. Effect of fatigue on joint position sense of the knee. J Orthop Res 4: 112–118, 1986.[CrossRef][Web of Science][Medline]
  60. Sterner RL, Pincivero DM, and Lephart SM. The effects of muscular fatigue on shoulder proprioception. Clin J Sport Med 8: 96–101, 1998.[Web of Science][Medline]
  61. St.-Onge N and Feldman AG. Referent configuration of the body: a global factor in the control of multiple skeletal muscles. Exp Brain Res 155: 291–300, 2004.[CrossRef][Web of Science][Medline]
  62. Taylor JL and McCloskey DI. Illusions of head and visual target displacement induced by vibration of neck muscles. Brain 114: 755–759, 1991.[Abstract/Free Full Text]
  63. Taylor JL, Butler JE, and Gandevia SC. Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 83: 106–115, 2000.[CrossRef][Web of Science][Medline]
  64. Vøllestad NK. Measurement of human muscle fatigue. J Neurosci Methods 74: 219–227, 1997.[CrossRef][Web of Science][Medline]
  65. Weerakkody NS, Whitehead NP, Canny BJ, Gregory JE, and Proske U. Large-fiber mechanoreceptors contribute to muscle soreness after eccentric exercise. J Pain 2: 209–219, 2001.[CrossRef][Web of Science][Medline]
  66. Weerakkody N, Percival P, Morgan DL, Gregory JE, and Proske U. Matching different levels of isometric torque in elbow flexor muscles after eccentric exercise. Exp Brain Res 149: 141–150, 2003.[Web of Science][Medline]
  67. Yaggie JA and McGregor SJ. Effects of isokinetic ankle fatigue on the maintenance of balance and postural limits. Arch Phys Med Rehabil 83: 224–228, 2002.[CrossRef][Web of Science][Medline]
  68. Yoshitake Y, Ue H, Miyazaki M, and Moritani T. Assessment of lower-back muscle fatigue using electromyography, mechanomyography, and near-infrared spectroscopy. Eur J Appl Physiol 84: 174–179, 2001.[CrossRef][Web of Science][Medline]
  69. Zhang LQ and Rymer WZ. Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86: 1086–1094, 2001.[Abstract/Free Full Text]



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