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Soleus T-reflex amplitude modulation when standing humans adopt a 1
challenging stance 2
3
Gordon R. Chalmers 4
Department of Physical Education, Health and Recreation, 5
Kinesiology and Physical Education Program 6
Western Washington University, Bellingham WA, USA 7
8
Corresponding author: 9
Dr. G. Chalmers 10
Department of Physical Education, Health and Recreation 11
Kinesiology and Physical Education Program 12
Western Washington University, MS-9067 13
516 High St. 14
Bellingham WA 15
98225-9067 16
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Phone (360) 650-3113 18
FAX (360) 650-7447 19
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Key words: human, T-reflex, stretch reflex, soleus, tandem stance, balancing 22
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Abstract 1
The amplitude of the short latency EMG response to soleus muscle stretch 2
produced by a mechanical tendon tap (T-reflex) was determined when subjects 3
stood in a stable stance position and a challenging stance with a reduced base of 4
support in the sagittal plane (tandem stance). Most subjects (14 of 19) decreased 5
mean T-reflex amplitude when in the tandem stance position, compared to the 6
stable stance (mean (s)), -13.7% (31%). All nine subjects who performed the 7
tandem stance without lightly touching support boxes, decreased their T-reflex 8
amplitude in the tandem stance position, -31% (20%), p = 0.002, Cohen’s d = 1.5. 9
Ten subjects needed to lightly touch the support boxes with the back of two or 10
three fingers while in the tandem stance. Five of these decreased reflex amplitude 11
while the others increased reflex amplitude, 2.0% (32%). For all subjects, and for 12
the subgroups of those that could, or could not perform the tandem stance without 13
touching support boxes, there was no significant change in soleus or TA bEMG 14
levels. These data demonstrate that the soleus T-reflex is modulated (typically 15
decreased) when a difficult tandem stance is performed. Possible mechanisms of 16
modulation of the T-reflex across the sanding tasks were discussed. 17
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Introduction 1
It has been frequently observed that the soleus Hoffmann (H-) reflex is 2
decreased in amplitude when a person changes from a stable standing position, to 3
a standing position that involves a greater degree of balance challenge with the 4
same level of muscle activation (G. R. Chalmers & Knutzen, 2002; Earles, Koceja, 5
& Shively, 2000; Hoffman & Koceja, 1995; Huang, Cherng, Yang, Chen, & Hwang, 6
2009; Solopova, Kazennikov, Deniskina, Levik, & Ivanenko, 2003; Tokuno, Taube, 7
& Cresswell, 2009; M. H. Trimble & Koceja, 2001). The decrease in soleus H-8
reflex amplitude during a challenging standing task is believed to be due to spinal 9
inhibition of the Ia afferent signal to stabilize the posture by preventing the Ia 10
signal (potentially enhanced during the difficult task, see below) from being strong 11
enough to excessively activate spinal motor neurons, while still allowing the 12
enhanced afferent information to be available to higher control centers (Hayashi, 13
Tako, Tokuda, & Yanagisawa, 1992; Hidler & Rymer, 1999; Katz, Meunier, & 14
Pierrot-Deseilligny, 1988; Llewellyn, Yang, & Prochazka, 1990; V. G. Macefield, 15
Gandevia, Bigland-Ritchie, Gorman, & Burke, 1993; McIlroy et al., 2003; Nafati, 16
Rossi-Durand, & Schmied, 2004; Taube et al., 2007). Greater cortical involvement 17
during precision, difficult or novel movements has been indicated by a number of 18
studies (McIlroy et al., 2003; Schmied, Pagni, Sturm, & Vedel, 2000; Schubert et 19
al., 2008; Sibley, Carpenter, Perry, & Frank, 2007; Solopova et al., 2003; Tokuno 20
et al., 2009). 21
In contrast to the many studies examining soleus H-reflex modulation across 22
different standing tasks, information on how, or if, the soleus stretch reflex is 23
5
modulated when a person performs a challenging standing task is sparse. When 1
subjects stood quietly without support, the Achilles tendon stretch reflex was 2
decreased in size, compared to with hand support (Elner, Gurfinkel, Lipshits, 3
Mamasakhlisov, & Popov, 1976). Background electromyographic (bEMG) activity 4
was not measured by Elner and Gurfinkel (Elner et al., 1976) but may be assumed 5
to be similar based on the similar ankle plantar flexor demands in both tasks. For 6
the muscles of the anterior compartment of the leg, removing hand support while 7
standing resulted in an increased muscle spindle response, although muscle 8
stretch reflex response was not measured (Burke & Eklund, 1977). These studies 9
differ from the H-reflex studies above, in that the degree of balance challenge was 10
minimal; standing without hand support was the most challenging task for the 11
subjects. In contrast, H-reflex studies commonly challenge the balance of standing 12
subjects with a reduced base of support in the sagittal plane or by using an 13
unstable surface. 14
Information obtained by H-reflex studies cannot be assumed to reveal 15
operation and function of the stretch reflex. For example, the soleus H-reflex was 16
depressed during the stance phase of walking compared to sitting or standing, 17
while the stretch reflex was not (Andersen & Sinkjaer, 1999; Sinkjaer, Andersen, & 18
Larsen, 1996), and the H-reflex was depressed more than the T-reflex when the 19
ankle was dorsiflexed (Guissard, Duchateau, & Hainaut, 1988). Similarly, during 20
an attention demanding wrist extensor muscle motor task and when switching from 21
a supine to standing position the H-reflex was inhibited while the stretch or T-reflex 22
was facilitated (Nafati et al., 2004; Shimba, Kawashima, Ohta, Yamamoto, & 23
6
Nakazawa, 2009). Divergent reflex modulation was also observed in the first 1
dorsal interosseous muscle when exerting a force against a unstable inertial load, 2
compared to a stable fixed load; there was no change in the stretch reflex, while 3
the H-reflex was increased (Maluf, Barry, Riley, & Enoka, 2007). 4
In summary, while much is known about the modulation of the soleus H-reflex 5
across standing balance tasks of increasing challenge, far less is known about the 6
operation of the more physiologic stretch reflex pathway during such tasks. There 7
is the potential for modulation of the spindle sensitivity, even at equivalent muscle 8
activation levels, and possible differences in the spinal modification of stretch 9
versus electrically invoked afferent signals, that would not be revealed in H-reflex 10
studies. The goal of this study was to determine if the amplitude of the sort latency 11
EMG response to soleus muscle stretch produced by a mechanical tendon tap (T-12
reflex) is modulated when a person performs a challenging standing balance task 13
with a reduced base of support in the sagittal plane. 14
Methods 15
Subjects 16
Nineteen subjects (11 male, 8 female; age mean ± standard deviation: 24 ± 6 17
years, age range: 18 - 45 years) with no known neurological, muscular, or gait 18
pathologies participated in this study. Older adults, well-trained athletes, and 19
people with dance or gymnastic experience were not recruited as these 20
characteristics modify soleus reflex function (Aagaard, Simonsen, Andersen, 21
Magnusson, & Dyhre-Poulsen, 2002; G.R. Chalmers & Knutzen, 2000; Koceja & 22
Kamen, 1988; Nielsen, Crone, & Hultborn, 1993; Taube et al., 2007). All subjects 23
7
complied with the requirement that they only consume light food, and no 1
stimulants or tobacco for two hours prior to testing (Eke-Okoro, 1982) . Further, all 2
subjects reported any medications they were taking and it was verified that none 3
took any medications that affected the muscular or nervous systems. The 4
experiments were approved by the Ethics Committee on Human Experiments at 5
Western Washington University, and all subjects gave their written informed 6
consent prior to inclusion in the study. 7
Experimental Procedure and Data Acquisition 8
All measurements were made on the right leg, with surface electrodes placed 9
and not removed until completion of data collection, in a room isolated from visual 10
and auditory distractions. Skin at the electrode sites was thoroughly cleaned with a 11
light abrasive, and EMG recording electrodes (Ag-AgCl, 10 mm in diameter, 3-cm 12
interelectrode distance) were placed on the soleus, along the midline of the dorsal 13
aspect of the leg with the proximal electrode 1 cm distal to medial head of the 14
gastrocnemius, and on the tibialis anterior (TA) muscle, one third of the distance 15
from the patella to the lateral malleolus (Zipp, 1982) . A 26-cm2 metal plate ground 16
electrode was attached to the right wrist. Muscle EMG signals were amplified by 17
bipolar differential amplifiers with a common mode rejection ratio of 90 dB, and a 18
frequency bandpass of 10-1000 Hz (Grass P5, West Warwick, RI). The EMG 19
signals were digitized at 2100 Hz with a 12-bit data acquisition card (Micro 1401, 20
Cambridge Electronic Designs, Cambridge, UK) and were analyzed using Spike2 21
software (Cambridge Electronic Designs). The soleus EMG signal was displayed 22
in a raw format to allow for peak-to-peak measurements of the evoked T-reflex 23
8
EMG response following tendon tap (Toft, Sinkjaer, & Espersen, 1989). The EMG 1
signals were concurrently displayed in a rectified and then smoothed format (all 2
smoothed EMG signals were calculated as each point averaged over the previous 3
40 millisecond period) to provide feedback to the subject and to allow for 4
measurement of the bEMG level prior to a stimulus. 5
During all measurements, subjects kept eyes open and looked at a blank 6
computer screen, or at a screen providing EMG feedback (described below) and 7
avoided any muscle contractions, other than those needed to maintain the 8
standing position (Taube, Leukel, & Gollhofer, 2008). It was ensured that the angle 9
of the right ankle was not varied during the experiment due to the dependence of 10
stretch reflexes on ankle angle (Patikas, Kotzamanidis, Robertson, & Koceja, 11
2004; Weiss, Kearney, & Hunter, 1986). 12
A random sequence of the two stance positions tested was then assigned to 13
the subject: stable stance (standing with feet spaced at a natural preferred 14
distance apart, with the heel of the left foot in line with the toes of the right foot and 15
both hands placed on the top of solid support boxes on each side of the subject), 16
and tandem stance (standing with the left foot placed directly in front of, and with 17
heel touching the toes of, the right foot, and arms held loosely at the sides). For 18
ten subjects the tandem stance position was so difficult that it could not be 19
performed without a high level of soleus and TA cocontraction and movements of 20
the upper body. These subjects were allowed to place the back of two or three 21
fingers of both hands gently against the vertical sides of the support boxes lateral 22
to them to obtain touch sensation without mechanical support. Even with these 23
9
additional points of contact, subjects reported and the researcher observed that 1
the tandem stance task was still significantly more difficult than the stable stance. 2
EMG activity was recorded from the soleus while the subject stood in the stable 3
and then the tandem stance positions for 20 seconds each, and the minimum and 4
maximum levels of the rectified and smoothed EMG record over 20 random points 5
in the EMG record were measured. The minimum and maximum EMG levels were 6
used subsequently to form a target range of soleus bEMG levels for data collection 7
during the two standing tasks, to ensure that bEMG levels were similar when 8
measures were made during the two tasks. 9
A mechanical tendon tapper was adjusted so that it would strike the Achilles 10
tendon. The force of the strike was adjusted by changing the length of the arc a 11
hammer swung through. The hammer was a steel bar pivoting on a very low 12
friction axis with multiple set points of release. A micro switch in the head allowed 13
a timing pulse to be recorded when the hammer contacted the leg. Pilot studies 14
determined that the hammer contacted the skin for a duration of 15 ms. The 15
reliability of the force delivered was determined by having the hammer hit a force 16
transducer in the same manner with which it hit a subject’s leg. The hitting force 17
was tested for 20 repeated strikes at each of the two hammer heights (i.e. force) 18
settings used for this experiment. For the two force levels, the mean ± s and 19
coefficient of variation were 256 N ± 23 N, 9% and 338 N ± 12 N, 3%. The striking 20
force for each subject was selected to be the one that produced an obvious stretch 21
reflex response without discomfort. 22
10
In both of the stance positions, the following procedure was followed for each 1
subject. The subject was provided with feedback on the current right soleus and 2
TA rectified and smoothed EMG level by means of a computer monitor positioned 3
directly in front of the subject’s face. The target range of bEMG levels was divided 4
into 10 steps, and the sequence of those steps was randomly assigned as target 5
contraction levels. A target contraction level was presented as a horizontal line on 6
the computer monitor. If the target level was greater than the contraction level the 7
subject was already producing to maintain stance, then the subject performed a 8
right leg ankle plantar flexion contraction so that the feedback bEMG level 9
matched the target level. The plantar flexion forces were always small enough that 10
the ankle angle did not change. If the TA was observed to have more than minimal 11
electrical activity, the subject was asked to reduce the activity before proceeding. 12
When the soleus bEMG level approximately matched the target and had been held 13
steady for at least 1 second, an Achilles tendon tap was delivered. If a muscle 14
contraction above that needed to naturally maintain the stance was required, the 15
subject then relaxed for at least 20 seconds to ensure that no post-voluntary 16
activation depression of the reflex occurred in the subsequent test (Grey et al., 17
2008; Pierrot-Deseilligny & Mazevet, 2000). This process was repeated until a 18
minimum of 20 measures of the T-reflex had been recorded for the stance 19
position, with these measures varying in soleus bEMG level. The total amount of 20
time spent practicing the tandem stance position prior to the actual measurements 21
did not exceed five minutes. 22
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Data Analysis 1
For each mechanical stimulation, the peak-to-peak amplitude of the T-reflex 2
EMG response (Figure 1) and the mean rectified and smoothed soleus and TA 3
bEMG levels over 0.1 seconds prior to the stimuli were determined. In all subjects 4
the tandem stance position was more difficult to maintain than the stable stance 5
position, resulting in greater co-contraction of the ankle plantar and dorsiflexors in 6
many subjects. In addition to providing feedback on TA bEMG activity so that 7
subjects could avoid co-contraction, the delivery of stimuli was avoided if more 8
than a slight co-contraction was being observed. Nevertheless, in some of the 9
tandem stance measures, the TA bEMG level was higher than that typically 10
observed during the stable stance. To ensure that the contraction of the TA was 11
similar across the data used to compare the two stances, to take care that 12
reciprocal inhibition was not changing (Maluf et al., 2007; Richard B. Stein, 13
Estabrooks, McGie, Roth, & Jones, 2007), the following procedure was used to 14
eliminate samples taken when the TA bEMG activity was elevated. In all subjects 15
the TA bEMG activity was low and consistent in the stable stance position. For 16
each subject’s tandem stance data, stimuli were omitted from analysis if the TA 17
bEMG activity was greater than two standard deviations above the mean TA 18
bEMG activity for the same subject’s stable stance position (Solopova et al., 19
2003). If this did not result in a difference of less than 10% in mean TA bEMG 20
activity for the two stance positions, then trials with the greatest TA bEMG activity 21
were successively omitted, until a difference of 10% or less was obtained (Tokuno 22
et al., 2009). 23
12
For each subject the peak-to-peak amplitude of the T-reflex EMG responses 1
and the corresponding soleus bEMG levels were plotted for each of the stance 2
positions (Figure 2). Soleus T-reflex amplitude was compared across the two 3
stances within each subject at a similar level of motoneuron excitability, the latter 4
reflected by the soleus bEMG level (Bove, Trompetto, Abbruzzese, & Schieppati, 5
2006; Kearney, Lortie, & Stein, 1999; Maluf et al., 2007; Matre, Sinkjaer, Knardahl, 6
Andersen, & Arendt-Nielsen, 1999; Simonsen, Dyhre-Poulsen, & Voigt, 1995; 7
Sinkjaer et al., 1996). The soleus bEMG activity range that was common to both of 8
the stance positions tested in a subject was used to limit which measures of reflex 9
amplitude were used for comparison across the two stances (between vertical 10
bars in Figure 2), data points outside this common range were excluded from 11
calculations. The soleus T-reflex amplitude observations within the range of 12
common soleus bEMG activity were averaged, for each of the stance positions. 13
To determine if the mean T-reflex amplitude, soleus bEMG activity and TA 14
bEMG activity within an individual were different when comparing the stable and 15
tandem stance positions, the measure in the tandem stance position was 16
expressed as a percentage change from the measure observed in the stable 17
stance position in the same individual. The percentage change in each measure 18
occurring with the change to the tandem stance for each subject was then 19
averaged across subjects to produce a mean within subject change in T-reflex 20
amplitude, soleus bEMG activity and TA bEMG activity when comparing the stable 21
and tandem stance positions. This data analysis approach prevented intersubject 22
differences in absolute or normalized T-reflex amplitude from obscuring 23
13
intrasubject changes in amplitude with a change in stance position, as may occur if 1
averages were determined across subjects for each stance position before body 2
position averages were compared. 3
4
Statistical Analyses 5
Two-tailed single-sample t-tests were used to determine if the percent change 6
between the stable and tandem stance position was significantly different from 7
zero, for the T-reflex amplitude, soleus bEMG activity and TA bEMG activity. 8
Statistical analysis was carried out for all subjects, and for both the subgroups of 9
subjects who could, and could not, perform the tandem stance without touching 10
the support boxes. The alpha level for each of these nine tests was adjusted with 11
the Bonferroni adjustment (i.e., 0.05/9 = 0.0056) (Vincent, 1999), and analysis was 12
carried out using SPSS (version 17, SPSS Inc., Chicago, Il). Results are reported 13
as mean (standard deviation). To determine the practical significance of the 14
results, Cohen’s d was calculated for comparisons that were statistically significant 15
(Faul, Erdfelder, Lang, & Buchner, 2007; Hatcher, 2003). 16
Results 17
Fourteen of 19 subjects decreased mean T-reflex amplitude when in the 18
tandem stance position, compared to the stable stance, with a mean decrease of 19
13.7% (31%) (table 1, figure 3). Nine of the nineteen subjects were able to perform 20
the tandem stance without touching the support boxes. All of these subjects 21
decreased their T-reflex amplitude when in the tandem stance position, compared 22
to the stable stance (table 1, figure 3). Their -31% (20%) mean decrease in reflex 23
14
amplitude was statistically significantly different from zero change (p = 0.002), and 1
the change was classified as large based on the Cohen’s d value of 1.5 (Vincent, 2
1999). For the 10 subjects who needed to lightly touch the support boxes with the 3
back of two or three fingers while performing the tandem stance, a greater 4
variability in their T-reflex amplitude change was observed. Half of these subjects 5
decreased reflex amplitude while the others increased reflex amplitude, resulting 6
in a mean change of 2.0% (32%). For all subjects, and for the subgroups of those 7
that could, or could not perform the tandem stance without touching support 8
boxes, there was no significant change in soleus or TA bEMG levels (table 1, 9
figure 3). 10
Discussion 11
This study has shown that when subjects reduced the width of their standing 12
base of support, to make the standing task more difficult, most (14 of 19) reduced 13
the amplitude of their T-reflex, compared to the amplitude when in a stable wide 14
stance position. The reduction in T-reflex amplitude was statistically significant and 15
large (Cohen’s d interpretation) for subjects that could perform the tandem stance 16
without finger touch support. This reduction in T-reflex amplitude is consistent with 17
the idea that during a challenging motor task, Ia afferent mediated reflex size may 18
be reduced to prevent the spindle Ia signal from being strong enough to 19
excessively activate spinal motor neurons (Hayashi et al., 1992; Hidler & Rymer, 20
1999; Llewellyn et al., 1990; V. G. Macefield et al., 1993; McIlroy et al., 2003; 21
Taube et al., 2007). Some portion of the reduced soleus T-reflex observed during 22
the tandem stance may be due to an increased anxiety associated with the task, 23
15
as opposed to the motor challenge, per se. When anxiety was increased while 1
maintaining a simple standing posture, by having subjects stand at the edge of an 2
elevated platform, H-reflex amplitude was reduced compared to a low platform 3
condition, and the reduction was not strongly related to a reduced soleus bEMG 4
activity concurrently observed (Sibley et al., 2007). 5
Within subjects, the amplitude of the T-reflex did not show a consistent pattern 6
of increasing as the bEMG level of the stretched muscle increased (Figure 2), as 7
has been observed in some other studies (Pruszynski, Kurtzer, Lillicrap, & Scott, 8
2009; R. B. Stein, Hunter, Lafontaine, & Jones, 1995; Toft, Sinkjaer, & 9
Andreassen, 1989). This may be explained by the observations of Blackburn and 10
coworkers, which showed that soleus stretch reflex amplitude was not related to 11
soleus bEMG level, when the bEMG varied over a small 13 ± 7% range of the 12
maximum voluntary contraction (MVC) level (Blackburn, Mynark, Padua, & 13
Guskiewicz, 2006). The range of soleus bEMG examined in the present study was 14
much smaller than 13% of the subject’s MVC level, only slight contractions above 15
that needed to maintain stance were produced by the subjects. 16
The correction of lateral instability during single legged stance can involve hip 17
corrective strategies (Gribble & Hertel, 2004), when the ankle corrections are 18
unable to maintain control (Tropp & Odenrick, 1988). In the present study the 19
subjects were instructed to maintain postural control by their ankle musculature. 20
Instability that involved hip movement was considered excessive and the subjects 21
were required to limit movement to their ankles, and stabilized themselves by light 22
finger touch, if needed. For the control of inversion and eversion movements of the 23
16
ankle, the triceps surae plays a functional role in humans (Klein, Mattys, & Rooze, 1
1996). 2
Subjects who needed to lightly touch adjacent support boxes to be able to 3
steadily maintain the tandem stance position, exhibited either a moderate 4
decrease or an increase in T-reflex amplitude compared to stable stance. All of the 5
subjects that increased their T-reflex amplitude compared to stable stance were 6
ones that required the light touch of the boxes. Previous studies indicate that 7
haptic stabilization by finger touch diminishes the reduction in H-reflex amplitude 8
seen when standing, or standing on one foot, and that the effect is greatest when 9
lateral touch, such as used in the current study, is employed (Hayashi et al., 1992; 10
Huang et al., 2009). Accordingly, for the subjects that required a light finger touch 11
during the tandem stance, it is may be that their T-reflex would have been smaller 12
in the tandem stance position, if they could have maintained a stable tandem 13
stance without finger touch. This haptic stabilization may have contributed to the 14
increase in T-reflex amplitude seen in five subjects in the tandem stance position, 15
despite the subjects reporting, and the researcher observing, that the tandem 16
stance position was still very difficult. Alternately, for some difficult skills, or 17
perhaps for some people performing those difficult skills, an increase in stretch 18
reflex amplitude may be more appropriate for the task. Nafati and coworkers 19
demonstrated that during an attention demanding wrist extensor muscle motor 20
task the T-reflex was facilitated (Nafati et al., 2004). Similarly, hand muscle studies 21
have found that during a position control task, the stretch reflex response is 22
17
increased compared to a force control task at the same force level (Akazawa, 1
Milner, & Stein, 1983; Kanosue, Akazawa, & Fujii, 1983). 2
3
Mechanism of reflex amplitude modulation 4
The amplitude of the soleus stretch reflex may be modulated in the spinal cord. 5
This was demonstrated by Burke and coworkers who showed that changes in 6
Achilles tendon jerk reflex amplitude could be modified by conditions such as 7
distraction, discomfort, attention changes, rate of tendon percussion or distant 8
muscle contraction, while these conditions did not modify the afferent response to 9
muscle stretch (Burke, McKeon, & Skuse, 1981). 10
For the soleus H-reflex, produced by electrical stimulation of afferent axons in 11
the posterior tibial nerve, the reflex modulation that occurs between standing tasks 12
of different difficulties is likely due to changes in presynaptic inhibition of the Ia 13
afferent signal between the tasks (Angulo-Kinzler, Mynark, & Koceja, 1998; 14
Capaday & Stein, 1987; Edamura, Yang, & Stein, 1991; Faist, Dietz, & Pierrot-15
Deseilligny, 1996; Hayashi et al., 1992; Katz et al., 1988; M.H. Trimble, 1998). 16
This assumes the tasks examined have comparable alpha motoneuron excitability 17
(R. Stein & Kearney, 1995) (reflected by background EMG), reciprocal inhibition 18
(Crone & Nielsen, 1989) (reflected by antagonist EMG), and that the frequency of 19
afferent activity does not produce homosynaptic post activation depression in the 20
Ia afferents (Hultborn et al., 1996). In the current study, the interval between 21
stimuli avoided homosynaptic depression (Grey et al., 2008; Pierrot-Deseilligny & 22
Mazevet, 2000). Additionally, changes in the T-reflex amplitude in the tandem 23
18
stance, compared to the stable stance, cannot be attributed to changes in soleus 1
or TA muscle activity. As a group, there was no significant change in the soleus or 2
TA bEMG levels when performing the tandem stance compared to the stable 3
stance (table 1). Additionally, the correlation between the mean change in T-reflex 4
amplitude and mean change in soleus bEMG level for subjects was negligible (r= 5
0.04). While a very weak correlation between individuals’ mean change in T-reflex 6
amplitude and mean change in TA bEMG level was found (r= 0.33), it’s positive 7
value is the opposite one would expect if an increase in TA activation in the 8
tandem stance position were a factor, via reciprocal inhibition, to produce the 9
decreased T-reflex amplitude observed in most individuals (Crone & Nielsen, 10
1989). Cutaneous, and non-spindle prioprioceptive influences on the spinal 11
networks are not expected to change between the two stance positions examined, 12
and so are unlikely to explain the reduced T-reflex amplitude observed. Similarly, 13
soleus stretch amplitude and velocity, stimuli to muscle spindles (Dimitriou & Edin, 14
2008; R. Stein & Kearney, 1995), are assumed to be the same for the two stance 15
positions, based on the unchanged right ankle position and soleus muscle 16
activation levels for the two positions, and the demonstrated consistency of the 17
striking force. There is, however, the possibility that activity of other muscles 18
controlling medial and lateral ankle movement could have changed during the 19
tandem stance task, and this could have affected the soleus motoneurons. 20
Additionally, reflex modulation through poly synaptic connections between Ia 21
afferents and alpha motor neurons could occur, although this would be observed 22
19
at slightly later times than the monosynaptic response (Jankowska, 1992; Ludvig, 1
Cathers, & Kearney, 2007). 2
The amplitude of stretch reflex, may also be modulated by changes in the 3
mechanical sensitivity of the muscle spindles (Naoyuki Kakuda & Nagaoka, 1998). 4
In cats, static and dynamic gamma drive to spindles and Ia sensitivity was 5
elevated during novel exploratory and difficult beam walking tasks (Hulliger, 1993; 6
Prochazka, Hulliger, Trend, & Durmuller, 1988). In humans, the Ia signal is 7
similarly enhanced during challenging tasks, although whether this can occur by 8
fusimotor activation without concurrent extrafusal activation is debated. During 9
precision finger movements, fusimotor activity and the firing rates of spindle 10
afferents was increased, although in most cases skeletomotor activity was 11
elevated as well, indicating that fusimotor activity was not controlled independently 12
of skeletomotor activity (N. Kakuda, Vallbo, & Wessberg, 1996; N. Kakuda, 13
Wessberg, & Vallbo, 1997). Similarly, during a standing balance task that required 14
increased muscle activation, pretibial muscle fusimotor drive was increased to 15
affect spindle discharge (Aniss, Diener, Hore, Burke, & Gandevia, 1990). In 16
contrast, during an attention and accuracy demanding motor task, the tendon 17
reflex of wrist extensor muscles was enhanced, with no change in muscle activity, 18
suggesting enhanced fusimotor spindle sensitization (Nafati et al., 2004). Similarly, 19
selective enhancement of fusimotor drive to increase spindle sensitivity was 20
suggested by Hospod and coworkers (Hospod, Aimonetti, Roll, & Ribot-Ciscar, 21
2007) to explain enhanced limb movement pattern recognition during an 22
attentional test. Likewise, during unsupported stance, low threshold cutaneous and 23
20
muscle afferents from mechanoreceptors in the human foot appear able to reflexly 1
activate fusimotor neurons innervating pretibial flexor muscles (Aniss et al., 1990). 2
The potential for a possible increased muscle sympathetic drive during the tandem 3
stance to alter spindle sensitivity is unclear, based on contrasting experimental 4
results (Hjortskov, Skotte, Hye-Knudsen, & Fallentin, 2005; Kamibayashi et al., 5
2008; V. G. Macefield, Sverrisdottir, & Wallin, 2003) 6
In sum, the current results can not establish the mechanism of the modulation 7
in T-reflex amplitude when subjects shifted to the tandem stance position. The 8
soleus H-reflex data showing an increase in presynaptic inhibition of the Ia afferent 9
signal acting on soleus motor neurons when standing without support (Katz et al., 10
1988) suggest that an increase in presynaptic inhibition may have played a role in 11
the decreased T-reflex amplitude observed in most subjects in the tandem stance 12
position. The T-reflex, however, is less depressed by presynaptic inhibition than 13
the H-reflex is (Enriquez-Denton et al., 2002; Morita, Petersen, Christensen, 14
Sinkjaer, & Nielsen, 1998). Previous studies discussed above suggest that the Ia 15
afferent signal may be greater in the difficult tandem stance, again suggestive that 16
the presynaptic inhibition acting on the Ia afferent signal would need to increase to 17
produce a net decrease T-reflex amplitude in the tandem stance position. No 18
change, or a decrease, in the Ia afferent signal in the tandem stance position, 19
however, cannot be ruled out. 20
21
Comparison to H-reflex studies 22
21
It is interesting to compare the T-reflex modulation when changing between a 1
stable and tandem stance position, found in the present study, with the H-reflex 2
modulation observed in similarly aged subjects for the same two motor skills 3
previously (G. R. Chalmers & Knutzen, 2002). In both studies, most subjects 4
decreased reflex amplitude when in the unstable tandem stance position, while a 5
few subjects increased reflex amplitude (Figure 3), and the range of changes were 6
similar, although smaller in the H-reflex study that included fewer subjects. If it 7
were known that the subjects that greatly decreased T-reflex amplitude also 8
greatly decreased H-reflex amplitude, and visa-versa, then it would be suggestive 9
of an important role of presynaptic inhibition in modulating T-reflex amplitude 10
across the stance positions, based on the evidence that H-reflex modulation 11
between standing tasks of different difficulties is likely due to changes in 12
presynaptic inhibition of the Ia afferent signal between the tasks (Katz et al., 1988) 13
. 14
Acknowlegments 15
The author thanks Geoff Landis for his expert technical assistance, and XXX 16
for providing comments on the manuscript. 17
Conflict of Interest 18
There are no conflicts of interest associated with this work. There are no study 19
sponsors. 20
21
22
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39
27
Table 1: Changes in mean T-reflex amplitude, soleus bEMG activity and TA bEMG 1
activity when subjects performed a tandem stance, compared to stable stance. 2
Results are reported as mean (standard deviation). * Significantly different from 3
zero change (p = 0.002). 4
5 T-reflex
amplitude
Soleus
bEMG
activity
TA
bEMG
activity
All Subjects (n=19) -13.7 %
(31%)
-2.7%
(9%)
0.3%
(6%)
Subjects who could perform the tandem stance without
lightly touching support boxes (n=9)
-31.2%
(20%)*
-3.7%
(9%)
-2.4%
(6%)
Subjects who needed to lightly touch support boxes while
performing the tandem stance (n=10)
2.0%
(32%)
-2.0%
(10%)
2.8%
(5%)
6
28
Figure 1: T-reflex EMG responses for a single subject in the stable stance (solid 1
line) and tandem stance (dashed line) positions. These two data samples are 2
representative examples from the subject illustrated in figure 2B who 3
demonstrated a 16% decrease in mean T-reflex amplitude when tandem stance 4
measures were compared to stable stance measures. Tendon tap occurred at time 5
zero (vertical dotted line). 6
7
Figure 2: T-reflex amplitude versus soleus bEMG plots for subjects who 8
demonstrated an increase (A, +49%), or decrease (B, -16%; C, -63%) in mean T-9
reflex amplitude when tandem stance measures (triangles) were compared to 10
stable stance measures (boxes). Only measures within the range of soleus bEMG 11
that was common to both stance positions, between vertical bars, were used to 12
calculate mean reflex amplitude for the position. Horizontal bars identify the mean 13
T-reflex amplitude of the stable stance (solid line) and tandem stance (dashed 14
line) data between the vertical bars. 15
16
29
Figure 3: Changes in mean T-reflex amplitude, soleus bEMG activity and TA 1
bEMG activity when subjects performed a tandem stance, compared to stable 2
stance. Nine of the nineteen subjects were able to perform the tandem stance with 3
hands near their sides (circles), while ten subjects needed to lightly touch the 4
vertical sides of adjacent support boxes with the back of two or three fingers while 5
performing the tandem stance (crosses). For comparison purposes, data from a 6
previous study (G. R. Chalmers & Knutzen, 2002) is included showing change in 7
H-reflex amplitude when performing a tandem stance compared to a stable stance 8
(diamonds). 9
10
