Physiologically adaptive changes of the L5 afferent neurogram and of the rat soleus EMG activity during 14 days of hindlimb unloading and recovery
Laboratoire de Plasticité Neuromusculaire, EA 1032, IFR 118, Bât. SN4, Université des Sciences et Technologies de Lille, F-59655 Villeneuve d'Ascq Cedex, France
* Author for correspondence (e-mail: laurent.dedoncker{at}free.fr)
Accepted 15 October 2005
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Summary |
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Immediately after HU, the EMG activity of the soleus muscle disappeared and was associated with a decrease in the afferent neurogram. The soleus electromyographic and afferent activities remained lower than the pre-suspension levels until the sixth day of HU and were recovered between the sixth and the ninth day. On the twelfth and fourteenth days, they were increased beyond the pre-suspension levels. During the first recovery day, these activities were significantly higher than those on the fourteenth HU day and returned to the pre-suspension levels between the third and sixth recovery days.
To conclude, our study directly demonstrates that the HU conditions cannot be considered as a functional deafferentation, as suggested in the literature, but only as a reduction of afferent information at the beginning of the HU period.
Key words: rat, hindlimb unloading, neuromuscular activities
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Introduction |
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Studies on the EMG activity during HU are conflicting
(Alford et al., 1987;
Blewett and Elder, 1993
) and
few works about the recovery of EMG activity after HU are present in the
literature (Blewett and Elder,
1993
; Ohira et al.,
2002a
). Moreover, there is no direct data concerning the
physiologically adaptive changes of the L5 afferent neurogram and
of the soleus EMG perturbations during and after a HU period. Therefore, the
aim of this work was to verify, firstly, if HU conditions can be assimilated
to a functional model of deafferentation as suggested in the literature, and
secondly, if physiologically adaptive changes in L5 afferent
activation level can explain changes in activation levels of the soleus EMG
activity during and after (recovery) 14 days of HU.
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Materials and methods |
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The animals of the HU group were hindlimb unloaded by the tail for 14 days, using Morey's model (1979). Briefly, an orthopedic tape-adhesive plaster, covering less than half of the cleaned and dried tail was connected to the top of the cage where a swivel allowed 360° rotation. The rats were elevated in a head-down position (30°) so that the hindlimbs could not touch the cage floor or walls while they were able to ambulate freely on their forelimbs. The experiments and the animal housing conditions received authorization from both the Agricultural and Forest Ministry and the National Education Ministry (Veterinary Service of Health and Animal Protection, authorization 59-00980).
Electrode preparation
Electromyographic and afferent activities were recorded using bipolar
electrodes made of stainless steel wire with Teflon insulation (7 strands, AM
Systems, Cooner wire, Phymep, Paris, France).
For intramuscular electrodes, the recording surface was exposed by removing 2 mm of Teflon insulation 5 mm from one end of the stainless steel wires. To deactivate the electrode extremity, 1 mm of Teflon insulation was pulled over it.
For the L5 afferent neurogram, the recording surface was exposed by removing 2 mm of Teflon insulation 5 mm from one end of the electrode. The recording surface of bipolar electrodes was introduced into silicone tubing 3 mm in length and 1 mm in inner diameter, which was cut longitudinally. The end of the electrodes was then rolled up and stuck to the silicone tubing using silicone glue. The distance between electrodes in the silicone tubing was 1 mm (Fig. 1A). To link the electrode to a connector, 5 mm of the Teflon insulation at the other end of the electrode was removed. The ground electrode was stripped of insulation for 5 mm at each end. To obtain a simultaneous recording of the soleus muscle and afferent activities, the four recording electrodes and the ground electrode were soldered to the connector and linked with dental cement (TAB 2000, Kerr, Italy) to the connector.
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Recording and analysis
Although the EMG activity was specific to the soleus muscle, the
L5 afferent neurogram also reflected activities of neurons
innervating other hindlimb muscles (gastrocnemius, for example) affected or
not by the microgravity environment
(Peyronnard et al., 1986).
During the experimental period (pre-suspension and reloading), the animals
were placed in small cages and left alone to limit movements and to record
neuromuscular activities under postural conditions. In this study, analyzed
recordings (8090% of daily recordings) were obtained when rats were
quiet. Activity bursts produced by rat movements were not taken into account.
Within each 30 min period, only phasic-like bursts (corresponding to the
progressive recovery of the tonic EMG activity of the soleus muscle) have been
averaged, except at the beginning (D0) of HU when the hypoactivity periods
predominated over few phasic-like bursts, which were very short in duration.
The control and HU recordings began 2 and 7 days, respectively, after surgery.
The rats were recorded as control for 5 days (mean ±
S.D.) and during the first, third, sixth, ninth, twelfth
and fourteenth days of HU (D0, D3, D6, D9, D12, D14) and recovery (RD0, RD3,
RD6, RD9, RD12, RD14). The soleus EMG activity and the L5 afferent
neurogram were simultaneously recorded twice a day for 30 min each (10:00 h
and 17:00 h). The raw EMG and the afferent neurogram were amplified
(pre-amplifier model P 511, Grass Instruments, Quincy, MA, USA; Gain 10,000,
band pass 30 Hz to 3 kHz), recorded and analyzed on a personal computer
through interactive software (Spike 2, Cambridge Electronic Design, UK). This
program rectified the EMG and neurogram signals throughout the recording
periods. The mean EMG (mEMG) and the afferent neurogram were expressed as V
s1 and averaged.
We have not included in this study a separate sham-operated group of rats to monitor the evolution of the signals over the full time period. However, before recording control levels of the soleus EMG activity and of the L5 afferent neurogram, we also recorded these activities four hours (wide awake animals) after the electrode implantation. These recordings are illustrated in the Fig. 1B. No significant difference can be observed between EMG and afferent activities on the day of the surgery and 6 days later. Therefore, at least for this time period, the electrode sensitivity is not altered. We have not tested the electrode sensitivity over this time period. However, the possible decrease in the electrode sensitivity to detect signals during HU or the recovery, could account to some degree for the decreased activities during HU. Nevertheless, this decrease is not involved and cannot explain the increases in EMG and L5 afferent activities during HU and recovery. Consequently, physiologically adaptive changes of these activities cannot be attributed to alterations triggered by electrode sensitivity changes. Moreover, at the end of the experiments, the position of each electrode was checked under the dissecting microscope and was found to be as originally placed, spaced out 2 mm between intramuscular electrodes and 1 mm between electrodes into the silicon tubing. The electrode sensitivity was also verified by using electrical stimulation and was found to be the same as just after electrode implantation.
Statistical analysis
All results are expressed as means ± S.D.
Significant differences (P<0.05) between HU and its own control
were established by using a paired Student's t-test. No significant
difference in neuromuscular activities was observed between the two recording
periods (10:00 h and 17:00 h). Therefore, results have been pooled.
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Results |
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EMG activity
At rest on the floor (pre-suspension level), the EMG activity was tonic and
the mean EMG activity (mEMG) was 0.56±0.09 (V s1).
Immediately after animal hindlimbs were elevated (D0), the mEMG activity of
the soleus muscle significantly decreased by 81% (0.11±0.03 V
s1) in comparison with the pre-suspension level (Figs
2A,
3) and remained lower until the
sixth HU day (Fig. 3).
Moreover, the EMG activity of the soleus muscle was shifted from `tonic' to
`phasic-like' activity during HU (Fig.
2A). The number, amplitude and duration of EMG bursts increased
with the duration of the HU period. Although the tonic EMG activity did not
totally recover its pre-suspension level between the sixth and ninth day of HU
(Fig. 2A), mEMG bursts were
quantitatively comparable to the tonic EMG activity of the pre-suspension
level (Fig. 3). Afterwards, the
mEMG activity gradually increased until the fourteenth day of HU
(P<0.05). In comparison with the pre-suspension values, the mEMG
activity significantly increased by 23% (0.69±0.09 V
s1) on the twelfth and by 32% (0.74±0.1 V
s1) on the fourteenth day of HU (Figs
2A,
3). However, on the fourteenth
day of HU, during the 60 min period of recording in HU, EMG bursts represented
only 76% of this period vs 24% for hypo-activity periods.
L5 afferent neurogram
Physiologically adaptive changes of the quantitative and qualitative
afferent neurogram during HU are illustrated in Figs
2A,
3. The mean afferent neurogram
(0.09±0.02 V s1) was decreased by 60%
(0.036±0.01 V s1) on the day of HU
(P<0.05) in comparison with the pre-suspension level
(Fig. 3). Moreover, the
L5 afferent activity was shifted from `tonic' to `phasic-like'
during HU (Fig. 2A). Between
the sixth and ninth day of HU, afferent bursts increased in amplitude and
duration to reach tonic activity of the pre-suspension level
(Fig. 3). Afterwards, they
increased by 22% (0.11±0.03 V s1) on the twelfth day
of HU (P<0.05) and by 44% (0.13±0.03 V
s1) on the fourteenth day
(Fig. 3).
Recovery
Qualitative and quantitative physiologically adaptive changes of the soleus
EMG activity and the L5 afferent neurogram during 14 days of
reloading are illustrated in Figs
2B,
3.
EMG activity
At the end of the fourteenth HU day, immediately after reloading (RD0), the
phasic-like EMG activity disappeared and the tonic EMG activity of the
pre-suspension level was recovered (Fig.
2B). However, the mEMG activity significantly increased by 51%
(0.85±0.15 V s1) on the day of reloading and by 23%
(0.69±0.1 V s1) 3 days later, in comparison with the
pre-suspension level (0.56±0.09 V s1)
(Fig. 3). Moreover, the soleus
EMG activity was increased by 15% (P<0.05) in comparison with the
EMG value of the fourteenth day of HU (0.74±0.1 V
s1). Between the third and sixth day of reloading, the
quantitative EMG activity regained the value of the pre-suspension level (Figs
2B,
3).
L5 afferent neurogram
The L5 afferent activity presented an adaptive change similar to
that of the EMG activity (Fig.
2B). The mean afferent neurogram was increased by 78%
(0.16±0.04 V s1) on the day of reloading
(P<0.05) and by 45% (0.13±0.03 V s1) on
the third day of reloading (P<0.05) in comparison with the
pre-suspension levels (Fig. 3).
Moreover, the L5 afferent activity was increased by 23%
(0.16±0.03 V s1) in compared with the fourteenth day
of HU (P<0.05). Between the third and sixth day of ground support,
the L5 afferent neurogram recovered the pre-suspension level (Figs
2B,
3).
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Discussion |
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According to Alford et al.
(1987), the soleus EMG activity
was immediately reduced after HU. This activity remained lower than that of
the pre-suspension level until the sixth HU day and was recovered between the
sixth and ninth days. In our study, after the ninth HU day, the soleus EMG
activity gradually increased until the fourteenth HU day. Alford et al.
(1987
) observed that the soleus
EMG activity was maintained at near normal levels after 710 HU days. In
the present work, the soleus EMG activity was higher on the first day of
recovery than at the pre-suspension level and on the fourteenth day of HU.
After the third recovery day, we observed that the soleus EMG activity
regained the pre-suspension level. Similar physiologically adaptive changes
were observed in the L5 afferent neurogram during both HU and
recovery.
Therefore, this study demonstrates that HU conditions cannot be considered as a functional deafferentation, as suggested in the literature, but only as a reduction of afferent information at the beginning of the HU period (between D0 and D6).
As already stated in our results, the soleus EMG activity disappeared immediately after hindlimb unloading. Later, the tonic activity was gradually recovered in phasic-like activity form, the amplitude and duration of which increased progressively to reach the basal tonic activity level. The term `phasic-activity' does not characterize phasic high-amplitude events due to hindlimb movements; indeed, in our study, phasic-like bursts occurred whereas no visible movement of the hindlimbs was observed. Our results did not permitted the determination of the mechanisms implied in this phenomenon.
Immediately after HU
The soleus EMG reduction resulting from HU observed in this work, may be
closely related to the passive shortening of the muscle caused by plantar
flexion (Alford et al., 1987;
Ohira et al., 2002b
;
Riley et al., 1990
), which can
inhibit tension development and decreases in afferent input. In fact, during
the 0G phase of a parabolic flight, Kawano et al.
(2002
) observed reductions in
the rat soleus EMG and efferent activities concomitant with a decrease in
afferent information. However, it is very difficult to determine the precise
nature of the afferent input responsible for alterations in the L5
afferent neurogram and EMG activity during the HU period.
The vestibular system is reported to control head and eye movements in
space. Vestibular and cervical reflexes stabilize the head and neck by
exciting the neck muscles in opposition to head and body movements
(Keshner and Cohen, 1989). On
the one hand, the vestibulocollic reflex (vestibular-neck reflex) aligns the
head with respect to the gravitational vertical. On the other hand, the
cervicocollic reflex aligns the head with respect to the position of the body.
These two reflexes work jointly to stabilize the head
(Peterson et al., 1985
). In
the normal terrestrial situation, the labyrinth detects the gravity vector,
and the otolithic messages project on to the
motoneurons via the
lateral vestibular spinal fasciculus. In real microgravity, these afferent
messages are altered or absent (Correia,
1998
). Immediately after a bilateral labyrinthectomy, the soleus
postural activity has been reported to decrease but to return to control level
after a short period. However, after 17 days, a hyperactivity of the soleus
muscle has been observed (Kasri et al.,
2004
). In our study, using Morey's model (hindlimb unloading), the
gravitational load was maintained and thus, labyrinthine inputs remained
persistent. Moreover, the vestibulocollic and cervicocollic reflexes can occur
thanks to the 30° head down of the rat: the head position was left in HU
conditions and was similar to the control head position. Consequently, in
order to maintain the gravitational force and head position during HU,
labyrinthine inputs could not be significantly modified. Finally, the
vestibulospinal information on hindlimb motoneurons was probably not altered.
For this reason, modifications of vestibular inputs during HU have been
discounted.
Although it has not been directly demonstrated in the literature, some
studies have suggested that a limited amount of afferent information,
particularly provided by plantar cutaneous mechanoreceptors and muscle
spindles, is involved in HU conditions. Indeed, as already stated in the
Introduction, in normal conditions, the information coming from cutaneous
receptors is transmitted to the central nervous system and causes medullary
reflexes that contribute to the stabilization of the feet and maintenance of
postural activity (Aniss et al.,
1992; Kavounoudias et al.,
1998
). In HU conditions, the patterns transmitted by these
cutaneous receptors are very probably disrupted because the soles of the feet
are not in contact with the ground. Consequently, the nervous motor message
could be modified. This hypothesis has been confirmed by experiments that used
the stimulation of plantar cutaneous mechanoreceptors, since the stimulation
of these receptors during the HU period prevents 53% muscular atrophy
(De-Doncker et al., 2000
)
indicating that plantar cutaneous information is greatly decreased during HU.
Concerning the implication of proprioceptive information, Riley et al.
(1990
) have observed that in
HU conditions, the soleus was often in a shortened position as after tenotomy
and immobilization in a plantar flexion position. In these latter conditions,
the natural physiological stimulus of muscle spindles, the muscular stretch
(Hunt, 1990
), was removed.
Consequently, during HU, the soleus muscle spindles were probably little, or
not at all, stimulated and the afferent activity of Ia and II fibers
originating from these stretch receptors was reduced. Indeed, the reactivation
of Ia fibers by tendinous vibrations has been reported as an effective
countermeasure preventing muscle atrophy developed during HU, thus indicating
that proprioceptive information was greatly disrupted in this condition
(Falempin and In-Albon,
1999
).
During HU
Although the plantar flexion occurred during the major part of the HU
period, the soleus EMG activity was gradually recovered to the pre-suspension
level after 710 days. These data may imply intramuscular
reorganization. A reorganization in the number and length of sarcomeres could
occur in HU conditions, resulting in the shortening of the soleus fiber
length, similarly to a shortened position immobilization
(Heslinga et al., 1995). Some
muscle passive tension (stretching) could therefore be restored
(Gillette and Fell, 1996
) and
consequently, muscle spindle discharges could reappear. However, this
mechanism could participate in the early recovery of neuromuscular activities,
but does not explain the increases in the soleus EMG activity on the twelfth
and fourteenth days of HU beyond the pre-suspension levels. Intrafusal fibers
are more resistant to myogenic atrophy and to structure modifications than
extrafusal fibers. This is probably due to the presence of the capsule
surrounding intrafusal fibers (Yellin and
Eldred, 1970
; Maier et al.,
1972
). In a study on the morphological and histochemical
properties of intrafusal fibers after HU
(De-Doncker et al., 2002
), we
have demonstrated that there was no significant difference in number,
cross-sectional area and histochemical properties of intrafusal fibers in
comparison with soleus muscle spindles of control rats. Moreover, in the rat
soleus muscle, the number (HU: 13.5±1.3; CONT: 14.3±1.5) and
length (HU: 2.75±0.2 mm; CONT: 2.82±0.3 mm) of muscle spindles
were not changed after a HU period. Therefore, no intrafusal fiber
reorganization seemed to occur during HU.
A decrease in the GABA immunoreactivity of the sensorimotor cortex has been
observed by D'Amelio et al.
(1996) after 14 days in HU.
Consequently, we can also suggest that during HU, an increase in descending
excitatory inputs on soleus motoneurons could be enhanced and contributed to
the soleus EMG increase observed after the HU period. In addition, Hnik et al.
(1981
,
1982
) previously suggested
that EMG activity reappearance after 12 days deafferentation was
apparently due to hypersensitivity of spinal neurons to supraspinal
influences.
Recovery
During HU reloading, recovery effects could be due to increased levels of
afferent input from muscle spindles and plantar cutaneous receptors above
control levels; some studies support this hypothesis. Indeed, after 14-day HU,
we have previously demonstrated in the rat that Ia and II fiber discharges
from the soleus during ramp-and-hold (3 and 4 mm) and sinusoidal stretches
were increased because of changes in passive mechanical properties of the
soleus during HU (De-Doncker et al.,
2003). Consequently, the stretches could be better transmitted to
the muscle spindles after a HU period and could be related to an increase in
the connective tissue, as previously proposed by authors in tenotomized
(Hnik and Lessler, 1973
) and
shortened immobilized muscles (Gioux and
Petit, 1993
; Maier et al.,
1972
; Tardieu et al.,
1982
). The sensitivity of plantar cutaneous receptors,
participating in the maintenance of the postural activity
(Aniss et al., 1992
), could
also be increased after HU. Indeed, a 14-day period of hindpaw sensory
deprivation decreased cutaneous thresholds and enhanced the responsiveness of
rat cortical somatosensory neurons (Dupont
et al., 2003
). These increases in afferent inputs could explain
why the EMG activity was higher on the first day of reloading than on the
fourteenth day of HU.
To summarize, our data directly showed that contrary to suggestions in the literature, this study demonstrates that HU conditions cannot be considered as a model of functional deafferentation, but only as a reduction of afferent information at the beginning of the HU period.
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Acknowledgments |
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