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This Article Abstract Full Text (PDF) Free All Versions of this Article: 98/4/1366    most recent 00955.2004v1 Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (4) Citing Articles via Google Scholar Google Scholar Articles by Hjortskov, N. Articles by Fallentin, N. Search for Related Content PubMed PubMed Citation Articles by Hjortskov, N. Articles by Fallentin, N.

Sympathetic outflow enhances the stretch reflex response in the relaxed soleus muscle in humans

Department of Physiology, National Institute of Occupational Health, Copenhagen, Denmark

Submitted 1 September 2004 ; accepted in final form 5 November 2004

	ABSTRACT

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Animal experiments suggest that an increase in sympathetic outflow can depress muscle spindle sensitivity and thus modulate the stretch reflex response. The results are, however, controversial, and human studies have failed to demonstrate a direct influence of the sympathetic nervous system on the sensitivity of muscle spindles. We studied the effect of increased sympathetic outflow on the short-latency stretch reflex in the soleus muscle evoked by tapping the Achilles tendon. Nine subjects performed three maneuvers causing a sustained activation of sympathetic outflow to the leg: 3 min of static handgrip exercise at 30% of maximal voluntary contraction, followed by 3 min of posthandgrip ischemia, and finally during a 3-min mental arithmetic task. Electromyography was measured from the soleus muscle with bipolar surface electrodes during the Achilles tendon tapping, and beat-to-beat changes in heart rate and mean arterial blood pressure were monitored continuously. Mean arterial pressure was significantly elevated during all three maneuvers, whereas heart rate was significantly elevated during static handgrip exercise and mental arithmetic but not during posthandgrip ischemia. The peak-to-peak amplitude of the short-latency stretch reflex was significantly increased during mental arithmetic (P < 0.05), static handgrip exercise (P < 0.001), and posthandgrip ischemia (P < 0.005). When expressed in percent change from rest, the mean peak-to-peak amplitude increased by 111 (SD 100)% during mental arithmetic, by 160 (SD 103)% during static handgrip exercise, and by 90 (SD 67)% during posthandgrip ischemia. The study clearly indicates a facilitation of the short-latency stretch reflex during increased sympathetic outflow. We note that the enhanced stretch reflex responses observed in relaxed muscles in the absence of skeletomotor activity support the idea that the sympathetic nervous system can exert a direct influence on the human muscle spindles.

motor control; short-latency reflex

However, the results from animal studies may not be transferable into humans, and the sympathetic regulation of the muscle spindle demonstrated in jaw and neck muscles may not be present in other muscles. Macefield et al. (17) failed to observe any changes in muscle spindle firing during a strong and sustained increase in muscle sympathetic nerve activity (MSNA) in the relaxed human leg. In contrast Rossi-Durand and coworkers (26, 28) found that mental arithmetic, known to increase MSNA in leg muscles, facilitated the stretch reflex in the soleus muscle. Furthermore, a recent study suggested that proprioceptive acuity involving the muscle spindles was unchanged or, in one condition, improved during sympathetic activation (20).

The possibility of a direct sympathetic modulation of human muscle spindles and the potential consequences from this on motor reflex functions, i.e., reflex enhancement or depression, remains a subject for debate, and it was the aim of the present study to examine the short-latency stretch reflex in the soleus muscle during elevated sympathetic outflow. This was tested by eliciting tendon tap reflexes in the soleus muscle during three different maneuvers known to increase MSNA in nonactive leg muscles, i.e., during static handgrip exercise followed by posthandgrip ischemia (31, 33) and during mental arithmetic (1).

	METHODS

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Subjects.   Nine healthy subjects (4 men and 5 women) participated in the study. The subjects were 37.2 yr (SD 6.3) with average heights and weights of 173 cm (SD 5.3) and 71.4 kg (SD 13.1), respectively. The local ethics committee of Copenhagen approved the study. All participants gave their informed consent before their inclusion in the study.

Procedure.   The protocol is illustrated in Fig. 1. When arriving to the laboratory the subjects were interviewed and the protocol was explained. Because bladder distension increases MSNA (7), the subjects voided before the experiment. Electromyograph (EMG) electrodes were placed at the right soleus muscle. Maximal voluntary contraction (MVC) was determined from the peak force of three maximal isometric efforts using a handgrip dynamometer (Bofors). From this peak force, 30% MVC was calculated. The stretch reflexes were elicited by tapping the Achilles tendon during six tapping trials, i.e., during 3 min of rest (rest 1), during 3 min of static handgrip exercise at 30% MVC followed immediately by 3 min of posthandgrip ischemia, followed by another 3 min rest (rest 2), during 3 min of mental arithmetic, and finally during 3 min rest (rest 3). The order of the static handgrip exercise/posthandgrip ischemia and mental arithmetic interventions was randomized. Tapping was started 1 min into rests 1-3, the static handgrip exercise, posthandgrip ischemia, and mental arithmetic interventions and lasted until 20 s before the cessation of the interventions. The participants reported subjective stress experiences just after rest 1 and after mental arithmetic.

View larger version (17K): [in this window] [in a new window]   Fig. 1. Experimental protocol. Subjects were randomized to participate in either procedure 1 or 2. Tapping was performed in 6 tasks each of 3-min duration: Rest 1, 2, and 3 (R1, R2, and R3, respectively), mental arithmetic (MA), static handgrip exercise (SHG), and posthandgrip ischemia (PHI). Three resting periods without tapping each of 3-min duration and 2 periods with stress ratings each of 1-min duration were included. BP, blood pressure; HR, heart rate.

Stretch reflexes.   Subjects were seated in a chair of the Biodex System III isokinetic dynamometer (Biodex Medical, Shirley, NY) with the right leg placed on a pedal in an ankle joint position of 90° so that a standardized relaxed position could be maintained without any muscle activity occurring. The angle of the knee joint was 100–120°. The stretch reflexes were elicited by tapping the Achilles tendon during 90 s (50 taps). An automatic reflex hammer produced taps by indentations of a constant duration of 5 ms and depth of 5 mm. Both parameters were continuously measured during the tapping. The electromechanical tapping system consisted of a prodder and a position sensor fixed to the armature of a solenoid. A cap 1 cm in diameter was attached to the skin of the subject; the cap and the end of the prodder made up an electrical contact for detecting the tap onset. The position sensor (linear potentiometer) was used for measuring the position of the prodder, i.e., the depth of the tap. The stroke length of the prodder was 10 mm, enabling a tapping depth in the range of 0–10 mm. The velocity of the prodder could be varied corresponding to a tapping duration from 3.5 to 20 ms for a tapping depth of 5 mm. Electric signals from the position sensor and cap prodder contact were recorded by a computer with a sample frequency of 3 kHz.

Electromyography.   As a measure of the activation of the soleus muscle and as an indirect measure of produced muscle force, EMG was obtained from bipolar surface electrodes. Pregelled Ag-AgCl surface electrodes (720-01-k, Medicotest, Ølstykke, Denmark) with a diameter of 0.7 cm were used. EMG was measured from the soleus muscle with the electrodes placed on the posterior medial side of the Achilles tendon. The proximal electrode was located 3 cm below the insertion of the gastrocnemius muscle on the Achilles tendon. The interelectrode distance was 2 cm. The raw EMG signals were sampled with a frequency of 5,000 Hz. The data were high-pass filtered with a cutoff frequency of 10 Hz. Before additional processing of the data occurred, visual checks for noise and artifacts were performed. The onset of the short-latency stretch reflex was determined by averaging 50 reflex responses. The latency was defined as the point in time when the EMG signal exceeded a threshold level of 3 SDs of the background EMG. Tapping the Achilles tendon elicited generally an EMG response consisting of one peak named M1 (32). Mean peak-to-peak amplitudes of M1 were calculated.

Blood pressure and heart rate.   Noninvasive continuous beat-to-beat changes in heart rate (HR, beats/min) and systolic (SBP, mmHg), diastolic (DBP, mmHg), and mean arterial (MAP, mmHg) blood pressures were measured with an inflatable cuff placed over the proximal portion of the middle finger connected to a Finometer device (Finapres Medical Systems BV-TNO TPD Biomedical Instrumentation) and recorded by a computer. The HR and blood pressure data were analyzed by use of BeatScope software package version 1.1 (TNO TPD Biomedical Instrumentation). The blood pressure was automatically corrected for hydrostatic pressure to compensate for vertical movements of the hand with respect to heart level and the concomitant pressure changes in the finger blood pressure.

Subjective experience of stress.   The participants reported subjective experiences of stress just after rest 1 and after mental arithmetic at the following four 11-point scales (0 = not at all, 10 = extremely): 1) stressed, 2) tensed, 3) exhausted, and 4) concentrated (15, 16).

Statistics.   For each participant, mean values and SDs were calculated for SBP, DBP, and MAP, for the self-rating scales, and for the different stretch reflex characteristics in the different treatments, i.e., rests 1–3, static handgrip exercise, posthandgrip ischemia, and mental arithmetic. Two-way ANOVA with repeated measurements with cardiovascular data, subjective experience of stress, and stretch reflex characteristics as dependent variables, treatments as fixed factors, and subjects as random factors was used to compare the different treatments. Tukey's post hoc test tested differences between treatments. The level of significance was set at P < 0.05. The cardiovascular data, the self-rating data, and stretch reflex characteristics are shown as mean (SD).

	RESULTS

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The cardiovascular data are presented in Table 1. SBP, DBP, and MAP were significantly elevated during static handgrip exercise (P < 0.001), posthandgrip ischemia (P < 0.001), and mental arithmetic (P < 0.05) compared with rests 1-3. HR was significantly elevated during static handgrip exercise and mental arithmetic compared with rests 1-3 and posthandgrip ischemia (P < 0.05). Furthermore, SBP, DBP, MAP, and HR during rests 1-3 did not differ, indicating a stable baseline. Finally, no differences were observed between static handgrip exercise, posthandgrip ischemia, and mental arithmetic for SBP, DBP, and MAP. The time course for HR and MAP along with superimposed stretch reflexes during rest 1, mental arithmetic, static handgrip exercise, and posthandgrip ischemia for one subject are illustrated in Fig. 2. The changes expressed as percent change from rest 1 in MAP and HR are illustrated in Fig. 3. The participants reported significantly more stress [6.9 (SD 2.4) vs. 0.6 (SD 0.9)] and tenseness [5.4 (SD 2.1) vs. 0.9 (SD 1.1)] during mental arithmetic compared with rest 1 (P < 0.001). Furthermore, no changes were found for exhaustion [1.6 (SD 2.3) vs. 0.2 (SD 0.4)] and concentration [6.2 (SD 2.9) vs. 5.3 (SD 2.5)] between mental arithmetic and rest 1.

View larger version (40K): [in this window] [in a new window]   Fig. 2. A: time course of mean arterial BP (MAP; top curve) and HR (bottom curve) for 1 subject. Horizontal bar indicates the protocol and the time for the tapping sequences. B: mean (50 taps) stretch reflex responses of electromyograph (EMG) from the soleus muscle during R1, R2, R3, MA, SHG, and PHI for 1 subject.

View larger version (18K): [in this window] [in a new window]   Fig. 3. Percent change from R1 for MAP (A), HR (B), and size of the soleus stretch reflex peak-to-peak amplitude (C) during R2, R3, MA, SHG, and PHI. Values are means (SD) (n = 9). *P < 0.001 vs. R1–3. P < 0.05 vs. R1–3. P < 0.05 vs. SHG, MA.

	DISCUSSION

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Static handgrip, posthandgrip ischemia, and mental stress all increased the amplitude of the short-latency stretch reflex in the soleus muscle. Interestingly, the internal relationship between the magnitudes of the responses elicited by the three interventions may reflect differences in their ability to increase muscle sympathetic outflow.

Static handgrip exercise at 30% MVC elicits a marked increase in MSNA in the nonexercising legs. Mark et al. (18) demonstrated a 193% increase in MSNA recorded from the peroneal nerve during static handgrip exercise at 30% MVC, Scherrer et al. (30) demonstrated a 431% increase, whereas Vissing et al. (33) demonstrated a 273% increase in the second minute of static handgrip exercise.

During posthandgrip ischemia, the MSNA remains elevated above baseline level and in some studies (18, 33) it is maintained at a level comparable to the exercise recordings. In most studies, however, there is a decline in MSNA in the occlusion period (21, 25, 30), and Kamiya et al. (14) found a reduction of 40% when handgrip exercise was compared with posthandgrip ischemia. In mental stress experiments, increases of 43 to 367% in MSNA, with a relatively large variability between subjects, have been reported. When mental stress is compared directly with handgrip exercise in the same experimental series, the MSNA is consistently larger during static handgrip than during mental stress [Peak changes in MSNA during handgrip and mental arithmetic, 188 and 51%, respectively (34)]. Seemingly, the relative ranking of enhanced stretch reflex responsiveness in the present study fits nicely with the previously reported magnitude of peak changes in MSNA during handgrip, posthandgrip ischemia, and mental stress. Additionally, consistent with the large variability in MSNA during mental stress compared with handgrip exercise in the literature, the variability in the enhancement of the stretch reflex in our study is greater in the mental task (coefficient of variation = 0.90) than in the static handgrip exercise (coefficient of variation = 0.64) and posthandgrip ischemia (coefficient of variation = 0.74).

The consistent enhancement of stretch reflex responsiveness we found contrasts with animal data reporting a decrease in static and dynamic muscle spindle sensitivity during stimulation of the cervical or lumbar sympathetic chain (10, 24, 27). However, the results from human studies are ambiguous and there may be methodological or species differences. In a study by Macefield et al. (17), microneurographic recordings from muscle spindles showed no changes in discharge frequency of either primary or secondary muscle spindle afferents during a strong and sustained physiological activation of muscle sympathetic outflow. However, the study investigated only static sensitivity of the muscle spindles and not the dynamic sensitivity of the muscle spindles exposed to controlled stretch. Matre and Knardahl (20), who studied the effect of increased MSNA on proprioceptive acuity, found that proprioception was unchanged in one condition and improved in another, and they could not exclude the possibility of a sympathetically mediated enhancement of spindle sensitivity in humans. Furthermore, studies investigating mental stress seemingly support the idea of an enhanced reflex response due to sympathetic modulation.

A mental computation task (28) and unpleasant picture viewing (3) both clearly facilitated the stretch reflex in the soleus muscle. An increased firing rate from primary muscle spindle afferents and increased stretch sensitivity during mental computation have also been demonstrated (26). In a study of a mental computation task, Rossi-Durand and colleagues (28) observed that the increases in stretch reflex amplitude occurred without H-reflex changes, indicating changes in muscle spindle sensitivity rather than changes in -motoneuron excitability or presynaptic inhibition on Ia afferents. They ascribed the increased stretch sensitivity during mental computation to a fusimotor sensitization of muscle spindles and suggested that, in relaxed subjects performing mental computation, the presetting of the fusimotor activation in priming spindle sensitivity could prepare the muscle spindles to better play their role in proprioception and motor control.

Activation of fusimotor neurons during mental stress seems feasible because mental tasks activate the same cortical areas that are involved in movement and motor tasks (9). Nevertheless, although animals can activate their fusimotor neurons independently of the skeletomotor system (-motor), this has not been found in humans despite intensive search (8, 9, 13). The observation of an increased stretch reflex in relaxed muscles with no skeletomotor activity during mental computation tasks and in all three tests conditions in the present study thus supports the idea of a direct modulation of muscle spindle sensitivity via the sympathetic nervous system.

It could be argued that although the soleus muscle remains inactive during all three maneuvers used to increase MSNA, the handgrip and mental stress situation involve a central command component that at least in theory could influence the fusimotor system. The enhancement of the stretch reflex response during posthandgrip ischemia, however, persists in a situation in which the central command component is eliminated, as evidenced in the return of HR to baseline levels (29). In this case, modulation of spindle sensitivity seems to rely on the influence of a peripheral sympathoexcitatory reflex elicited via metabolites trapped in the occluded muscle and resulting in an increased muscle sympathetic outflow. However, because we tested only the contribution from the muscle spindle, we cannot exclude the possibility of a reflex reinforcement via presynaptic disinhibition acting at the Ia motoneuron synapse.

The enhanced stretch reflex sensitivity during posthandgrip ischemia could originate from a residual effect from static handgrip exercise. However, because Enoka et al. (6) demonstrated a quick T reflex recovery (within seconds) after static exercise, and we started Achilles tendon tapping 60 s after static handgrip exercise, this indicates that the enhanced sensitivity was related to posthandgrip ischemia.

Gregory et al. (12) studied the mechanisms of the potentiation of the stretch reflex during the Jendrassik maneuver, corresponding to the static handgrip exercise in the present study. They demonstrated that the fusimotor system is not involved in the reinforcement and neither is direct excitatory or presynaptic disinhibitory effects on motoneurons. As an alternative, they proposed that oligosynaptic neurons might contribute to the tendon stretch reflex, which may not be strictly monosynaptic. Taking the findings of the study by Gregory et al. and the findings from our study into account, the stretch reflex may be enhanced via sympathetic modulation during static handgrip exercise.

When considering the functional implication of an increased stretch reflex gain during states of high MSNA, such as during mental stress, the potency of the reflex system could tune the system to a more powerful and appropriate reaction. However, the increased stretch reflex sensitivity during increased MSNA may have potentially adverse effects. Interestingly, increased spine loading was observed during a stressful standardized lifting task compared with nonstressful conditions (5, 19). The authors suggest that mental stress might cause an overreaction of the musculoskeletal system, manifesting itself through less controlled motions and increased muscle coactivation. We suggest that the demonstration of an increased stretch reflex and the likelihood of an optimization of the motor reflex system in the present study may indicate a "fight-and-flight-reaction" at the expense of fine motor control, which was impaired during stressful situations (22, 23).

In conclusion, although no definite interpretations can be made as to whether the muscle spindle is regulated by the sympathetic nervous system, the present study clearly indicates a facilitation of the stretch reflex and supports the idea of a modulation of muscle spindle sensitivity with increased sympathetic drive in humans.

	FOOTNOTES

 

Address for reprint requests and other correspondence: N. Hjortskov, National Institute of Occupational Health, Dept. of Physiology, Lersø Parkallé 105, DK-2100 Copenhagen, Denmark (E-mail: nhj{at}ami.dk)

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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This Article Abstract Full Text (PDF) Free All Versions of this Article: 98/4/1366    most recent 00955.2004v1 Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (4) Citing Articles via Google Scholar Google Scholar Articles by Hjortskov, N. Articles by Fallentin, N. Search for Related Content PubMed PubMed Citation Articles by Hjortskov, N. Articles by Fallentin, N.