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J Appl Physiol 99: 1442-1445, 2005. First published June 23, 2005; doi:10.1152/japplphysiol.00180.2005
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Disuse atrophy increases the muscle mechanoreflex in rats

Naoyuki Hayashi,1 Satoshi Koba,2 and Takayoshi Yoshida2,3

1Institute of Health Science, Kyushu University, Fukuoka; and 2Graduate School of Engineering Science and 3School of Health and Sport Sciences, Osaka University, Osaka, Japan

Submitted 14 February 2005 ; accepted in final form 18 June 2005


   ABSTRACT
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MATERIALS AND METHODS
 RESULTS
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We investigated the effect of disuse atrophy on the magnitude of the muscle mechanoreflex. The left leg of eight rats (6–7 wk, male) was put in a plaster cast for 1 wk. The rats were decerebrated at the midcollicular level. We recorded the pressor and cardioaccelerator responses to 30-s stretch of the calcaneal tendon, which selectively stimulated the muscle mechanosensitive receptors in the left atrophied and right control triceps surae muscles. Atrophied muscles showed significantly lower mass control muscles (1.0 ± 0.1 vs. 1.4 ± 0.1 g; P < 0.05). At the same stretch tension (229 ± 20 g), the pressor response to stretch was significantly greater in the atrophied muscles than in the control muscles (13 ± 3 vs. 4 ± 2 mmHg, P < 0.05). The cardioaccelerator response was not significantly different (8 ± 4 vs. 4 ± 2 beats/min). Comparing responses at the same relative tension (57 ± 6 vs. 51 ± 8% of maximal tension), the pressor response was still significantly greater in the atrophied triceps surae than in the control (14 ± 4 vs. 4 ± 2 mmHg; P < 0.05). These results suggest that disuse atrophy increases the magnitude of muscle mechanoreflex.

muscle mass; exercise pressor response; cardiovascular deconditioning

ONE OF THE NEURAL MECHANISMS increasing blood pressure during exercise is the exercise pressor reflex, which originates from mechano- and metabosensitive receptors in active muscles and can thus be considered as comprising the mechanoreflex and metaboreflex, respectively (8, 18). These reflexes are observed in various animals, including humans and rats (6, 8, 26). The primary pathway of the exercise pressor reflex arc includes group III and IV afferent fibers (15). Triceps surae muscles contain thin fibers, mechanoreceptors, and metaboreceptors (9, 16).

The effect of the exercise pressor reflex on cardiovascular deconditioning is not fully understood. Cardiovascular deconditioning is induced by head-down bed rest and spaceflight (1), and it is characterized in part by a less pressor response to exercise (10, 25) and by orthostatic intolerance (1). Kamiya et al. (10) recently compared pressor response before and after head-down bed rest, and they observed attenuated increases in arterial pressure during both static exercise and postexercise circulatory occlusion, the latter being used to stimulate the metabosensitive receptors in exercising muscles. In contrast, muscle sympathetic nerve activity responses to postexercise circulatory occlusion are reportedly higher after spaceflight compared with before (4). Capillary volume, mitochondrial function, and oxidative capacity in muscles were reported to decrease after disuse (11, 20, 28). In addition, cardiac atrophy and consequent reductions of stroke volume, which have been noted after bed rest and spaceflight (22, 24), could reduce blood flow to the active muscle and increase metabolic products. Variations in pressor response could thus be attributable to changes in the metabolic status of active muscle in the previous studies (4, 10).

No evidence exists for any relationship between disuse atrophy and the magnitude of the muscle mechanoreflex. Exposure to spaceflight and bed rest causes disuse atrophy in skeletal muscles (3, 21), while magnitude of the mechanoreflex is related to muscle mass (30). We can rule out any effects of atrophy-induced metabolic changes on the metaboreflex. Magnitude of the mechanoreflex might thus be expected to become blunted when muscle mass is decreased by disuse. The present study compared the magnitude of muscle mechanoreflex between atrophied and control leg muscles in rats. In this cardiovascular model, control cardiovascular function should be identical when responses in the two limbs are compared with each other.


   MATERIALS AND METHODS
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 MATERIALS AND METHODS
RESULTS
 DISCUSSION
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General.   All experimental procedures were approved by the Animal Care and Use Committee of the School of Health and Sport Sciences at Osaka University and were conducted in accordance with the American Physiological Society's Guiding Principles for Research Involving Animals and Human Beings. Eight male Sprague-Dawley rats (6–7 wk, 240–280 g) were anesthetized using a mixture of halothane (4%) and oxygen. The left ankle of the hind leg was inserted into a 3.5-cm-long tube, with the joint fixed at 130–150° to immobilize the limb. The tube was attached to the leg using glue containing {alpha}-cyanoacrylate. Care was taken not to occlude the peripheral circulation.

At 1 wk after limb immobilization, rats were again anesthetized using a mixture of halothane (4%) and oxygen. The trachea, the jugular vein, and right common carotid artery were cannulated. The carotid catheter was attached to a Statham P23XL transducer (Ohmeda, Madison, WI) to measure arterial pressure. Syringe needles were set in the back of each animal for electrocardiography. Signals were amplified (model AB-621G, Nihon Kohden, Tokyo, Japan). Body temperature was maintained using a heat pad.

The triceps surae muscles of both hind legs were isolated. Origins of the muscles were left intact. The calcaneal bone was severed and attached to a string. Nerves supplying the left triceps surae muscles were exposed. Skin flaps were attached to bars to form a pool, which was filled with mineral oil. All visible nerves, except for those innervating the triceps surae muscles (tibial nerve), were severed.

Each rat was placed in a stereotaxic apparatus (model ST-7, Narishige, Tokyo, Japan). Decerebration was performed as previously described (6). Dexamethasone (0.2 mg iv) was administered. The left carotid artery was occluded immediately before the decerebration. Cortical tissue over the colliculi was aspirated. The brain was sectioned vertically with a blade at the midcollicular level. All tissue rostral to the section and the neural tissues covering the cerebellum were aspirated. The cranial vault was filled with agar. Immediately after decerebration, anesthesia was stopped. To replace the blood loss, saline was given intravenously (<1 ml) to maintain basal arterial pressure. A recovery period of 2 h was allowed to eliminate the effects of halothane and to stabilize the preparation.

Protocols.   To selectively stimulate mechanically sensitive receptors, triceps surae muscles were passively stretched for 30 s using a weight hung form the string attached to the tendon. The muscles were preloaded at 20-g tension in a control period before commencement of the trial. At the beginning of the stretch, the weight was brought down by the experimenter's hand. To match the tension developed by both legs, more than three different magnitudes of tension were applied. If spontaneous behaviors were observed during the trial, the data for that period were discarded.

To determine the maximal tension generated in triceps surae muscles, we stimulated the tibial nerves at the level that supramaximally recruited motor axons (60 Hz; 0.5 ms; 10 times motor threshold). The tension developed was measured using a force transducer (model TB-611T, Nihon Kohden) attached to the string from the tendon. To confirm that responses to tendon stretch were reflex in origin, the nerve supplying the muscles was severed and the same protocol of passive stretching was then repeated. At the end of the experiment, triceps surae muscles from both legs were excised and weighed.

Data analysis.   All values are expressed as means ± SE. Changes in variables from prestimulation baseline value were compared between right control and left atrophied muscles using paired t-tests. Muscle mass and peak developed tension were compared between muscles using paired t-tests. The significance level was set at P < 0.05.


   RESULTS
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 MATERIALS AND METHODS
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Muscle mass was significantly less for atrophied triceps surae muscles (1.0 ± 0.1 g) than for control muscles (1.4 ± 0.1 g). Maximal tension generated by supramaximal stimulation was significantly smaller in atrophied muscles (329 ± 51 g) than in control muscles (511 ± 41 g).

At baseline, mean arterial pressure (MAP) was 75 ± 5 mmHg in atrophied muscle and 76 ± 5 mmHg in control muscle, and heart rate (HR) was 386 ± 10 beats/min in atrophied muscles and 384 ± 10 beats/min in control muscles. No significant differences in MAP or HR at baseline were identified between atrophied and control muscles.

An example of MAP response to stretch is shown in Fig. 1. Stretch significantly increased MAP. Compared with responses at the same stretch tension (229 ± 20 g), MAP response was significantly greater in atrophied muscles than in control muscles (13 ± 3 vs. 4 ± 2 mmHg; Fig. 2), whereas no significant difference was observed in HR (8 ± 4 vs. 4 ± 2 beats/min). Compared at similar relative tensions corrected by maximal tension developed in the triceps surae (57 ± 6 vs. 51 ± 8% of maximal tension), MAP response was still significantly greater in atrophied muscles than in control muscles (14 ± 4 vs. 4 ± 2 mmHg; P < 0.05). No significant difference in HR response were observed between muscles (atrophied, 7 ± 4 vs. control, 4 ± 2 beats/min).



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  		Fig. 1. Examples of mean arterial pressure responses to 200-g stretch tension (open bar) applied to the control ({circ}) and the atrophied ({bullet}) triceps surae muscles in a rat. Greater magnitude of mean arterial pressure response was observed in atrophied muscles.

 


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  		Fig. 2. Mean mass of triceps surae muscles (A), maximal developed tension to supramaximal stimulation (B), and peak pressor response to similar absolute tension (C). Muscle mass and maximal tension were significantly lesser in the atrophied muscles (filled bars) than in the control (open bars). Peak pressor response was greater in the atrophied muscles than in the control. *Significant difference vs. control, P < 0.05.

 

   DISCUSSION
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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The new finding in the present study is that disuse atrophy increases the magnitude of muscle mechanoreflex. Similar results were obtained in both absolute and relative tensions. We had hypothesized that disuse atrophy would blunt the magnitude of muscle mechanoreflex due to the decrease in muscle mass. This was because magnitude of the exercise pressor reflex, which is one of the neural mechanisms acting to increase blood pressure during exercise, is related to the muscle mass (7, 30). The present result clearly negates this hypothesis.

Exposure to spaceflight and bed rest causes disuse atrophy (3, 21). Smaller muscles elicit a lesser magnitude mechanoreflex than larger muscles (30). Less pressor response to exercise and orthostatic intolerance are observed after spaceflight and bed rest (1, 10, 25). As a result, we have supposed that reductions in mechanoreflex after disuse atrophy contribute to cardiovascular deconditioning. This idea was not supported by the present finding.

The present animal model offers technical advantages in that mechanosensitive receptors can be selectively stimulated under identical cardiovascular conditions. The present study thus offers the first demonstration of the effects of disuse atrophy on the mechanoreflex.

The magnitude of the metaboreflex elicited by postexercise muscle ischemia after inactivity has remained controversial (4, 10). Differing results could be associated with variations in cardiovascular and metabolic conditions before and after intervention. Enhanced glycolytic activity in red gastrocnemius muscle has been reported after hindlimb unweighting (14). Capillary volume, mitochondrial function, and oxidative capacity in muscles reportedly decrease after disuse (11, 20, 28). Cardiac atrophy and consequent reductions of stroke volume have been reported after bed rest and spaceflight (22, 24). Thus, given the advantages of the present model, we tried to collect data of metaboreflex under the same cardiovascular conditions. However, data on the metaboreflex could not be successfully collected, because spontaneous movements were frequently observed in the rats, particularly in atrophied muscle, as previously reported (6).

The role of the exercise pressor reflex in patients with diseases characterized by decreased activity such as chronic heart failure (CHF) and myocardial infarction (MI) remains an area of considerable debate (2). Because of limited activity, patients with these diseases should display smaller muscle mass. Interestingly, CHF patients have been shown to exhibit greater exercise pressor reflex than control subjects (23). Moreover, the mechanoreflex appear to be increased in CHF patients (17, 19) and in rats with MI (13). The present finding suggests that a partial explanation for the greater pressor reflex in these disease processes may be related to disuse atrophy.

The present study did not investigate the mechanism underlying changes in the magnitude of the mechanoreflex. We can only speculate regarding candidate mechanisms responsible for the greater magnitude of mechanoreflex in atrophied muscle. The most likely mechanism appears to be a change in muscle fiber type. Muscles containing a greater population of fast type fibers reportedly evoke a greater exercise pressor reflex. Wilson and Mitchell (29) reviewed previous studies and concluded that the response is mediated predominantly by fast-twitch fibers. A shift from slow-twitch toward fast-twitch fibers has been reported in soleus muscle after tail suspension (20). Increases in magnitude of the muscle mechanoreflex may thus be related to alterations in fiber type during disuse atrophy.

The present results were unlikely to be influenced by metabolites, because reflex responses were evoked using muscle mechanoreflex. Passive stretch of muscle activates mechanoreceptors, but it does not increase metabolism in triceps surae muscles (27). However, slight but significant increase in ATP contents in plantaris and gastrocnemius muscles have been shown following hindlimb unweighting (14). Recent reports have suggested that ATP in skeletal muscle, a purinergic P2 receptor agonist, enhances the magnitude of the mechanoreflex (5, 12). Although we have no data on the effect of baseline ATP concentration on the magnitude of mechanoreflex, ATP concentrations may have been increased in atrophied muscle in the present study and thus might have played a role in elevating the magnitude of reflex. Further studies are needed to characterize the effect of baseline ATP concentrations on the magnitude of mechanoreflex.

Magnitude of the mechanoreflex in control muscles in the present results was substantially less than described in previous studies, which have reported increases in MAP of 15–20 mmHg in decerebrate rats (6, 26). The magnitude in the present study was also less than that of exercise pressor reflex observed in humans (10, see Ref. 8). We have no explanation for the lesser magnitude of mechanoreflex in decerebrate rats, because limited number of studies have been done in decerebrate rats.

In summary, we compared the muscle mechanoreflex in atrophied and control triceps surae muscles in rats. The magnitude of muscle mechanoreflex was greater in atrophied muscles than in control muscles. This result suggests that the disuse atrophy increases the magnitude of mechanoreflex evoked from skeletal muscle.


   GRANTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This study was supported by Grant-in-Aid for Scientific Research 15700418 from the Ministry of Education, Science, Sport, Culture, and Technology of Japan (to N. Hayashi).


   ACKNOWLEDGMENTS
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 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
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REFERENCES
 
The authors express gratitude to Prof. Marc P. Kaufman (University of California at Davis) for critical reading of the manuscript.


   FOOTNOTES
 

Address for reprint requests and other correspondence: N. Hayashi, Institute of Health Science, Kyushu Univ., 6-1 Kasuga-kouen, Kasuga, Fukuoka 816-8580, Japan (e-mail:naohayashi{at}ihs.kyushu-u.ac.jp)

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.


   REFERENCES
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