Posture control after prolonged exercise

Eur J Appl Physiol (1997) 76: 55 ± 61
Ó Springer-Verlag 1997
ORIGINAL ARTICLE
Romuald Lepers á Andre X. Bigard á Jean-Pierre Diard
Jean-FrancËois Gouteyron á Charles Y. Guezennec
Posture control after prolonged exercise
Accepted: 10 January 1997
Abstract The perturbations of equilibrium after prolonged exercise were investigated by dynamic posturography on nine well-trained subjects (four athletes and
®ve triathletes). A sensory organization test, where the
platform and visual surround were either stable or referenced to the subject's sway with eyes open or closed,
was performed before and after a 25-km run (average
time 1h 44 min) by the nine subjects. In addition, the same
test was performed on the ®ve triathletes only, before and
after ergocycle exercise of identical duration (i.e. ergocycle time = running time). The results showed that the
ability to maintain postural stability during con¯icting
sensory conditions decreased after exercise, with some
di€erences depending on the kind of exercise. Sensory
analysis revealed that the subjects made less e€ective use
of vestibular inputs after running than after cycling
(P < 0.05). Adaptation to prolonged stimulation of
proprioceptive, vestibular and visual inputs had probably
occurred in the integrating centres during exercise. This
adaptation was maintained during the recovery period
and could explain the postexercise balance disorders.
Other mechanisms such as impairment of motor e€erents
or haemodynamic changes should not be excluded.
Key words Equilibrium á Dynamic posturography á
Sensory inputs á Prolonged exercise á Running
Introduction
The maintenance and control of posture and balance,
whether under static or dynamic conditions, are essential
requirements for physical and daily activities. The
R. Lepers (&) á A.X. Bigard á C.Y. Guezennec
DeÂpartement de Neurophysiologie, Institut de MeÂdecine
AeÂrospatiale du Service de Sante des ArmeÂes,
BP 73, F-91223 BreÂtigny-sur-Orge Cedex, France
J.P. Diard á J.F. Gouteyron
Centre Principal d'Expertise MeÂdicale du Personnel Navigant,
Percy-Clamart, France
maintenance of equilibrium is achieved by using orientation information derived from three independent sensory sources: somatosensory, vestibular and visual
inputs. The a€erent information is processed in the
brainstem and cerebellum, and then motor commands
are initiated. The three sensory systems all contribute to
postural control, and damage to any of them, or to the
brainstem or cerebellum, will in¯uence the overall output of the postural system.
It has been shown that the contribution of individual
sensory inputs to equilibrium can be quanti®ed by
measuring the equilibrium adjustments of standing
subjects deprived of vision and/or input from the support surface, the environment thus presenting the subjects with con¯icting visual, proprioceptive and
vestibular stimuli (Nashner et al. 1982; Nashner 1983).
In such an experiment, called ``dynamic posturography'', the various con¯icting sensory conditions are
created by rotating the surface platform and/or the visual surround in proportion to the subject's postural
sway, thus making these sources of sensory information
inappropriate for the postural task. This method for
assessing human balance and posture has been extensively used in clinical practice for assessing and di€erentiating disturbances of vestibular, visual, and proprioceptive functions, as well as central co-ordination.
Dynamic posturography has been found to be versatile
in assessing equilibrium e€ects of anaesthesia (Gupta
et al. 1991), acute and chronic e€ects of alcohol (Ledin
and OÈdkvist 1991), and solvents (Ledin et al. 1991).
Decreased postural stability has been studied in aged
persons (Era and Heikkinen 1985; Straube et al. 1988;
Teasdale et al. 1993), patients with vestibular de®cits
(Nashner et al. 1982; Black and Nashner 1983), cerebral
palsy (Nashner et al. 1983) or Parkinson's disease (Allum et al. 1988; Bloem 1992; Beckley et al. 1995) and
many other diseases. Studies of human posture and
equilibrium control in normal subjects and patients have
provided much information on the capacity of the central nervous system to regulate posture. The decreased
stability associated with postural sway can be related to
56
reduced peripheral sensibility in the visual, vestibular, or
proprioceptive systems, and also to a defect or a slowing
of the central integrative mechanisms responsible for
con®guring the postural control system.
From observations of the postural instability of
runners after the end of a race, it would seem correct to
assume that the equilibrium has been impaired by exhausting physical exercise. Sensory inputs are highly
stimulated during a run: it has been demonstrated that
muscle spindles, tendon organs, joint receptors and cutaneous a€erents on the sole of the feet are activated at
each stride (Merton 1964), the vestibular system is sensitive to each head acceleration (Kornhuber 1974), and
the eyes are stimulated by the motion of the visual ®elds
(Lestienne et al. 1977). Whereas the e€ects of long distance running on the cardiovascular and musculoskeletal systems are well known, the e€ects on the
neurosensory system and therefore on the maintenance
of equilibrium remain unknown. Nevertheless, there are
some situations especially in sport where postural and
balance requirements follow physical exercise (for example, cross-country skiing and shooting in the biathlon). To our knowledge, no study has yet quanti®ed the
importance of postural instability after physical exercise.
The present study was conducted in order to evaluate
and quantify the equilibrium performance before and
after long-distance running on well-trained subjects
(triathletes and running specialists). To verify the importance of the movement of visual ®eld and the stimulation of face pressure receptors on the mechanisms of
balance control, we also examined and quanti®ed the
e€ects of a cycle ergometer exercise of similar duration
and intensity.
long-duration exercise and none had any history of vestibular or
neurological disease. The experimental procedure was approved by
the local Ethics Commission.
Platform test procedures
Procedures involved the use of an instrumented platform system
(Equitest, Neurocom Int. Inc., Clackamas, Oregon, USA), which
has been used in previous studies (Nashner et al. 1982; Ledin and
OÈdkvist 1993; Beckley et al. 1995). The system included two
movable support surfaces (one for each foot; each could independently move horizontally and rotate around an axis colinear to the
ankle joints) and a movable visual surround (a 1-m square enclosure open at the back and bottom which rotated around an axis
colinear to the ankle joints). Strain gauges within each platform
measured the torsional forces and the total vertical force exerted by
the foot resting upon its surface.
Sensory organisation test
Each subject stood quietly on the platform within the visual surround for three periods of 20 s (3-s rest inbetween) during six
di€erent test conditions (Fig. 1). During the ®rst three test conditions, the platform support surface remained ®xed with respect to
the earth horizontal, but the visual surrounds were (1) ®xed with
Methods
Subjects
Nine well-trained subjects whose physical characteristics are shown
in Table 1, volunteered to participate in this study. Five of them
were competitive triathletes, who trained on average 12±15 h a
week, three times in each discipline: swimming, cycling and running. The four other subjects were competitive runners, who
trained around 6±8 h a week. Every subject was familiarized with
Table 1 Physical characteristics
of the subjects
Fig. 1 The six conditions of the sensory organisation test. During the
®rst three conditions 1, 2 and 3, the platform support surface was ®xed
relative to earth horizontal. During the next three conditions 4, 5 and
6, the platform support surface was moved proportional to the
subject's anteroposterior body sway. The three visual conditions were
repeated in sequence, ®rst with the platform earth-®xed; second with
the platform perceptually stabilized. The three visual conditions were
repeated: 1 and 4 eyes open with a ®xed ®eld of vision 2 and 5 eyes
closed, and 3 and 6 ®eld of vision moved in relation to body sway
Subject
Speciality
Age
(years)
Height
(cm)
Body
mass
(kg)
25-km
Time
(h-min)
Maximal O2
uptake cycling
(ml á min)1 á kg)1)
A
B
C
D
E
F
G
H
I
Run
Run
Run
Run
Triathlon
Triathlon
Triathlon
Triathlon
Triathlon
44
27
32
29
41
23
40
27
44
172
178
175
180
183
174
176
183
171
60
66
61
59
73
55
66
74
60
1
1
1
1
1
1
1
1
1
±
±
±
±
66
60
68
72
62
Mean
SEM
34
3
176.8
1.4
63.8
2.2
1 h 44
0 h 03
h
h
h
h
h
h
h
h
h
43
32
51
50
41
57
34
40
51
65.6
2.1
57
respect to the earth vertical, (2) the subjects eyes were closed, and
(3) in proportional to anteroposterior (AP) body sway (visual
stabilization). It has been found that during this third condition,
the visual enclosure sways in direct proportion to the changes in AP
orientation, so that the relative orientation of the subject and his
surround remains ®xed Nashner 1983. During the three other
conditions (4), (5) and (6), the platform support surfaces rotated in
proportional to AP body sway (support surface stabilization) and
the ®rst three visual conditions were repeated. During these last
three conditions, the relative orientation of the subject and the
support surface was ®xed as has been described by Nashner (1971).
During both support surface and visual stabilization procedures,
the gain of surface motion relative to that of the body sway could
be set at any level ranging from 1 (surface and body motions in
direct proportion) to 2 (surface motions being double that of body
motions).
For each test an equilibrium score re¯ected the extent to which
the subject's AP sway movements approached the limits of stability
for the feet together stance, during each of the 20-s trials. A score
between 0 (12.5° sway range, or falling) and 100 (no sway motion)
was measured using the system of Nashner et al. (1990). The scores
of the three successive 20-s trials of each test were averaged to give
the test equilibrium score. The degree of ankle and hip movements
were estimated by a strategy score (100: no horizontal AP forces,
i.e. full ankle strategy 0: shear force of 110 N estimated to be the
maximum possible, i.e. full hip strategy; Horak and Nashner 1986).
Protocol
The sensory organisation test (SOT) (Fig. 1) was performed on
each subject, three times (runner specialists) or ®ve times (triathletes). A trial sequence was always performed a few days before the
day of the test run, to familarize the subjects with the procedure and
to reduce the learning e€ects. The other sequences were carried out
just before (PRE) and immediately after (POST) the long-distance
run and cycle exercise. Because disorientation and instability were
possible during the assessment of fatigued subjects, sensory conditions were imposed to increase the diculty during the SOT. The
®rst three SOT quanti®ed the performance of each subject during
three di€erent visual conditions (normal, eyes closed and stabilized
vision) when they were provided with a ®xed support surface. The
three tests were repeated for the three di€erent visual conditions,
except that then the subjects stood with the support surface stabilized. Because the subjects showed good balance (preliminary test),
stabilization gains during these trials were set at 2.
Sensory analysis was accomplished by computing sensory ratios
among the average equilibrium scores on speci®c pairs of sensory
test conditions, as shown in Table 2.
All the subjects ®rst performed the long distance run and the
triathletes, at least 1 week later the cycle exercise. All the tests were
performed in the morning.
Long distance run
The nine subjects were invited to run, at a speed close to their personal record, for 25 km outside on a generally ¯at route which had
been measured. The subjects were followed during the entire run by
Table 2 Sensory analysis. For
de®nitions of conditions 1±6
see Fig. 1
a cyclist, who gave them information about distance and time.
Water was provided on demand by the cyclist without restriction.
Stationary cycle exercise
Because the competitive runners were not trained cyclists, the second part of the experiment was conducted only with the triathletes.
Triathletes were asked to cycle on an ergometer (Orion, Toulouse,
France) at a power corresponding to approximately 65%±70% of
their maximal oxygen uptake (determined during previous laboratory incremental tests) for a time equal to that of their 25-km run.
Statistics
Statistical di€erences between PRE and POST conditions of the
same exercise (run or cycle) and between POST conditions (run
versus cycle) were determined by the nonparametric Mann Whitney
test, for each sensory condition of SOT and for each sensory ratio
of the sensory analysis.
Results
The subjects ran 25-km in times ranging from 1 h 32 min
to 1 h 57 min with an average of 1 h 44 min (Table 1).
Dynamic posturography after the 25-km run
Figure 2a and b illustrates the average (and SEM)
equilibrium scores and strategy scores during the six
di€erent sensory conditions, before and after the 25-km
run for the nine subjects, respectively. The equilibrium
scores, which re¯ected the subject's ability to maintain
his balance, decreased after the run, except in condition 1. In the two other ®xed support surface conditions,
stability performance was lower after the run than before. Strategy scores remained high during these three
conditions, suggesting that the ankle strategy prevailed
during ®xed support surface conditions.
During the three stabilized support surface conditions, stability performance was lower and particularly
altered in conditions 5 and 6 after the run. Equilibrium
scores decreased signi®cantly postexercise (P < 0.05) in
the stabilized surface condition 4. In condition 5, the
average equilibrium score was reduced from 71 (3.6°
body sway angle range) before the run to 52 (6° body
sway angle range) after the run. In conditions 5 and 6
lower performance and greater variability resulted from
the loss of balance (i.e. score 0) of one subject in 5 and two
Ratio Name
Ratio Pair
Somatosensory
Condition
Condition
Condition
Condition
Condition
Condition
Condition
Condition
Visual
Vestibular
Visual Preference
Question
2
1
4
1
5
1
(3+6)
(2+5)
Does sway increase when visual cues are
removed?
Does sway increase when somatosensory cues
are inaccurate?
Does sway increase when visual cues are
removed and somatosensory cues are inaccurate?
Do inaccurate visual cues result in increased
sway compared to no visual cues?
58
Fig. 2a Comparison of equilibrium scores before (PRE ) and
after (POST ) a 25-km run
(n=9). Signi®cance level
*P < 0.05 b Comparison of
strategy score before (PRE ) and
after (POST ) a 25-km run
(n = 9). Signi®cance level:
*P < 0.05. For de®nitions of
conditions 1±6 see Fig. 1
subjects in 6. Under the three stabilized support surface
conditions, strategy scores were lower after exercise, re¯ecting a preferential use of hip strategy to control balance. This decrease was signi®cantly di€erent in conditions 4 (P < 0.05) and 5 (P < 0.05) after the run.
Comparison of dynamic posturography
after ergometer exercise versus the run
Figure 3a and b illustrates respectively the average and
SEM equilibrium scores and strategy scores during the
six di€erent sensory conditions before and after the
25-km run and the ergocycle exercise for the ®ve triathletes.
During ®xed support surface conditions, equilibrium
scores were very similar either after the run or after
cycling in 1, but present in 2 and 3 condition values
which were lower postrun than after the ergometer exercise. Strategy scores did not show signi®cant di€erences during the ®xed support surface conditions.
During stabilized support surface conditions, the alterations of performances were similar with ®xed (4) or
stabilized vision (6) either after the run or the cycle exercise. A di€erence appeared nevertheless during the
eyes closed condition when the scores tended to be
substantially lower after running than after cycling, even
though it was not statistically signi®cant. Strategy scores
decreased similarly, being independent of the kind of
exercise during stabilized support surface conditions.
Sensory analysis
Figure 4 illustrates the changes in sensory ratios. The
sensory ratio of condition 2:1 remained unchanged
59
Fig. 3a Comparison of equilibrium
scores before (PRE ) and after
(POST ) a 25-km run and the same
duration ergometer exercise (n = 5).
Signi®cance levels *P < 0.05,
**P < 0.01. b Comparison of strategy scores before (PRE ) and after
(POST ) a 25-km run and the same
duration ergometer exercise
(n = 5). Signi®cance level
*P < 0.05, **P < 0.01. For de®nitions of conditions 1±6
see Fig. 1
whereas the sensory ratios for both conditions 4:1 and
5:1 decreased postexercise. In the absence of a stable
surface, the subjects did not make e€ective use of either
vestibular or visual inputs after prolonged exercise.
Vestibular input seems to have been more a€ected by the
run than by the ergometer exercise (P < 0.05). Visual
preference values remained unchanged postexercise.
Discussion
Fig. 4 Comparison of sensory ratios before (PRE ) and after (POST )
a 25-km run (n = 9) and the same duration ergometer exercise (n =
5). SOM somatosensory (condition 2/condition 1), VIS visual
(condition 4/condition 1), VEST vestibular (condition 5/condition
1), VIS PREF visual preference (condition 3+6/condition 2+5).
Signi®cantly di€erent from PRE-exercise condition aP < 0.05, bP <
0.01. Signi®cantly di€erent from POST-RUN condition cP<0.05
The results showed that the subjects' abilities to maintain their balance under con¯icting sensory conditions
were altered by prolonged exercise with some di€erences
between the run and ergometer exercise. Estimation of
human balancing ability by tradition has been limited to
static test conditions, i.e. the person standing on a stable
60
support surface during the test. Static posturography
limits the possibilities of the investigator to study external in¯uences. The e€ects of vision (Romberg test)
may be tested easily, but the role of the concurrent
systems were not studied. The SOT procedure represents
a substantial improvement in the study of the equilibrium system as a control system. It must also be remembered that this method has drawbacks; it is not
speci®c to any of the systems involved, it is also heavily
in¯uenced by motivation and concentration.
Whether a learning e€ect interfered with the equilibrium performances during the test may be questioned.
Before the experimental measurements, one sequence
was devoted to familarizing the subjects with the SOT
procedure. However, no statistical di€erences appeared
between the equilibrium and strategy scores in the different sensory conditions of the prerun and the prebike
situations. Moreover, the subjects performed their best
scores during the second SOT procedure i.e. prerun test.
It may thus be hypothesized that a learning e€ect did not
signi®cantly a€ect the results.
The post-tests were performed immediately after the
end of the exercise, it corresponded then to a period of
transition from exercise perturbation to a rest condition.
The maintenance of equilibrium was appreciated here
during the recovery time when the sensory stimulations
of the exercise had stopped. However, it may be hypothesized that the mechanisms of postural regulation
were impaired by the previous exercise. This observation
raises the problem of the di€erent mechanisms which
could explain this impairment of balance control.
In the sensory conditions 5 and 6 of SOT, when both
the support surface and visual references were made simultaneously inaccurate, leaving vestibular input as the
only potentially accurate orientation reference for postural control, the regulation of erect stance was more
dicult after exercise, especially after the run. The increased sway under these conditions was typical of patients with reduced vestibular function (see Black and
Nashner 1983). During the run, a continuous stimulation of the otholitic system, which is sensitive to linear
head acceleration, would have occurred. In response to
the prolonged stimulation during the run, the integrator
centres of vestibular information could have decreased
their sensibility threshold. Consequently, the vestibular
omission resulting from an adaptation to running
movement, which probably persisted during the beginning of the recovery, could in part explain the perturbations of postural control postexercise.
In the same way, we cannot exclude an adaptation to
the visual information by the integrator centres. Visually
guided behaviour such as locomotion and postural stabilization have been shown to depend on visual information mediated by the peripheral visual inputs
(Lestienne et al. 1977). During the run, in contrast to a
stationary cycle exercise, the visual input was continuously stimulated by the moving ®eld of vision. Visual
movement by itself could have given the perception of
body sway and caused postural compensations, even
when somatosensory and vestibular information did not
signal the sway. Such a prolonged stimulation of the
visual input, and the adaptation which resulted, could
also have in¯uenced the maintenance of balance during
the post running equilibrium test.
The third input which was highly stimulated during
such prolonged exercise was the somatosensation. Under normal circumstances, it has been demonstrated that
an individual is more reliant on somatosensation than
on visual inputs in correcting for body sway (Nashner
and Berthoz 1978). During running, eccentric contractions alternate with concentric ones and muscle damage
does occur. The tendons, the joint receptors and the
cutaneous mechanoreceptors of the sole of the foot are
then greatly and repetitively stimulated. All these receptors play an important role in the maintenance of
balance. A loss of somatosensory information from the
lower limbs, resulting from a disease or an experimental
manipulation, has been shown to induce postural control abnormalities (Diener et al. 1984; Horak et al. 1990).
Moreover, muscular fatigue associated with local glycogen depletion, metabolite accumulation and muscle
damage probably occured in the ankle extensors and
¯exors during the run. A decrease of the e€ector system
eciency due in part to muscle fatigue, and changes in
the proprioceptive information and/or in their integration could probably impair the postural regulation loop.
This hypothesis has been supported by previous observations showing that stretch-re¯ex sensitivity was reduced after exhausting exercise (Hortobagyi et al. 1991;
Nicol et al. 1996). This phenomenon can be attributed to
several factors associated with metabolic fatigue, neuromuscular spindle sensitivity or muscle damage. In our
conditions, we did not make a direct measurement of
muscle fatigue so that it was not possible to relate postural control changes with fatigue. Further studies are
needed to obtain a reliable index of fatigue which could
be compared to postural changes. The changes of postural strategies postexercise, especially the increase of
hip movements to control postural stability, could be
attributed to such an adaptative process.
The di€erences in equilibrium scores in some sensory
conditions of SOT between the postrun and the
postcycling situations would suggest that running exercise could have speci®c e€ects on equilibrium maintenance. The vestibular system, in particular the otholitic
organs, were less stimulated during the ergometer exercise than during the run. It should nevertheless be
pointed out that the sensitivity threshold of otholitic
organs to linear accelerations was very low (5 cm á s)2),
and the head oscillations during the ergometer exercise
should be taken into consideration, but to a lesser extent. The ergometer exercise also suppressed the moving
®eld of vision thus reducing the stimulations of the visual input. Finally, the lower leg muscle recruitment and
the stimulations of joint and tendon receptors, but also
of cutaneous mechanoreceptors, were di€erent, with
smaller mechanical constraints. Such di€erences in
proprioceptive requirements between running and cy-
61
cling could explain the lower equilibrium score obtained
after the run compared to cycling in condition 3 of SOT
± ®xed support surface, stabilized vision ± when the
central system would have used essentially the proprioceptive information to regulate balance.
The changes of sensory information integration
postexercise are nevertheless not the only hypothesis to
explain the equilibrium perturbations. During exercise,
the peripheral blood volume can only be returned to the
central circulation by continual activation of the skeletal
muscle pump, as occurs with running or cycling.
Therefore, the sudden stop in exercise would have immediately promoted peripheral blood pooling, which
could have transiently perturbated vestibular vascularization in the ®rst minutes of the test. Thus, as has been
suggested a perturbation in blood ¯ow parameters at the
vestibular level could perhaps impair the sensory input
even if the cerebellar blood ¯ow seems to be preserved
during exercise (Jorgensen et al. 1992). To test this hypothesis, an audiogram with detection of auditory
thresholds, for example, should be performed after exercise. Haemodynamic changes resulting from progressive dehydration, as often occurs during prolonged
exercise, should also be taken into consideration.
Conclusion
The main result of this study was that the subjects'
ability to maintain their balance in a dynamic environment was altered by prolonged exercise. Such alterations
probably resulted from an adaptation by the integrator
centres to the hyperstimulation of sensory inputs during
exercise, which persisted during the recovery period.
Nevertheless other parameters, such as impairment of
motor e€erents and haemodynamic changes, could also
have been involved in the disturbance of equilibrium
postexercise. The lesser stimulation of vestibular and
visual inputs during the cycle ergometer exercise than
during the run could explain the lesser alteration of
postural control after the cycle ergometer exercise.
Acknowledgements The authors wish to thank Mr. G. Porcheron
for the English language revision of the manuscript.
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