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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 56:B254-B258 (2001)
© 2001 The Gerontological Society of America

Motor Unit Properties of Nerve-Intact Extensor Digitorum Longus Muscle Grafts In Young and Old Rats

Paul S. Cedernaa,b, Hirotaka Asatoa,b, Xiaoming Gua, Jack van der Meulenb, William M. Kuzon, Jr.a,b, Bruce M. Carlsona,c and John A. Faulknera,d,e

a Institute of Gerontology and Departments of, University of Michigan Health Systems, Ann Arbor
b Surgery, University of Michigan Health Systems, Ann Arbor
c Cell and Developmental Biology, University of Michigan Health Systems, Ann Arbor
d Biomedical Engineering, University of Michigan Health Systems, Ann Arbor
e Physiology, University of Michigan Health Systems, Ann Arbor

Decision Editor: Edward Masoro, PhD


   Abstract
Top
 Abstract
Materials and Methods
 Results
 Discussion
 References
 
Impaired reinnervation has been implicated as the cause of the threefold disparity in the recovery of maximum force (P0) of standard muscle grafts in old compared with young rats. The specific, null hypothesis of this study is that compared with age-matched control extensor digitorum longus (EDL) muscles, nerve-intact EDL muscle grafts in young and old rats show no evidence of an age-related impairment in reinnervation. Nerve-intact grafts were performed in 3-month-old and 23-month-old rats and were evaluated 60 days postoperatively. Compared with age-matched control EDL muscles, nerve-intact grafts in young and old rats showed no difference in muscle mass or motor unit numbers. The mean motor unit P0 for nerve-intact graft muscles in both age groups was significantly lower than that of age-matched control muscles. These data support our hypothesis that if axons are allowed to regenerate in an endoneurial environment, there is no evidence of an age-related impairment in muscle reinnervation.

OLD age is associated with decreased muscle mass and force-generating capabilities (1). A factor partially responsible for the reduction in muscle mass and the impairment of force production in old as compared with young animals is an age-related decrease in the regenerative capacity of skeletal muscle (2)(3)(4). A major question arising from this observation is whether the reduced success of muscle regeneration in old rats is due to a reduction in the intrinsic regenerative capacity of the muscle itself, or if the differences can be accounted for by extrinsic factors such as impaired reinnervation. For these hypotheses to be tested, free whole muscle transplantation models have been used.

The standard free grafting procedure of a muscle involves proximal and distal tenotomy and repair, denervation, and devascularization (5)(6)(7). A nerve-implant free graft involves the same procedures, except that the nerve is implanted into the muscle at the completion of the procedure (8)(9). In standard and nerve-implant grafts, the muscle fibers undergo ischemic necrosis. Muscle fiber regeneration in these models requires revascularization and reinnervation (6)(9)(10). The advantages of nerve-implant grafting over standard grafting procedures were a slight improvement in the recovery of force production and a significant decrease in the variability of force development. Presumably, the improvement was due to a more consistent pattern of reinnervation (6). For whole extensor digitorum longus (EDL) muscles grafted in 3-month-old rats, the standard grafts and nerve-implant grafts revascularized completely (10). Despite complete revascularization, muscle force production was impaired, as demonstrated by a 55% reduction in maximum isometric tetanic force (P0) in standard grafts (7)(11)(12) and a 45% reduction in nerve-implant grafts (8). In nerve-implant grafts of EDL muscles performed in 26-month-old rats, muscle force production was impaired further, as demonstrated by an 81% reduction in P0, a nearly threefold difference from their young counterparts (8).

When grafted into young hosts, EDL muscles from young (4-month old) or old (24-month old) donor rats recover equally well; when muscles from young or old donor rats were grafted into old hosts, the recovery was equally poor (9). Furthermore, in both young and old rats, fully denervated EDL grafts recover equally poorly, and fully innervated, bupivacaine-treated EDL muscles regenerate equally well (13). Taken together, these observations indicate that the regenerative capacity of EDL muscles from old rats is equivalent to that of EDL muscles from young rats. Consequently, the twofold to threefold difference in the P0 developed by nerve-implant EDL grafts in young compared with old rats is not due to an age-related difference in the intrinsic process of muscle fiber regeneration.

In young rats, nerve-intact EDL muscle grafts develop a P0 of 80–90% of control EDL muscles, a recovery that is substantially better than the recovery of P0 following standard and nerve-implant grafts (14)(15). The difference between nerve-implant and nerve-intact EDL grafts is that in the former, the motor nerve is divided and surgically implanted into the muscle, whereas in the latter, the motor nerve is never physically separated from the muscle. In nerve-intact grafts, the intramuscular portions of the motor axons undergo ischemic necrosis with Wallerian degeneration of the distal segment of the motor nerve fiber, but the endoneurial conduits necessary to guide axonal regeneration are preserved (15). Therefore, muscle fibers in nerve-intact grafts must regenerate and become reinnervated, but the milieu for axonal elongation and neuromuscular synaptogenesis is likely more favorable than that for standard or nerve-implant grafts, in which the axons must regenerate outside the endoneurial sheaths (7)(14).

Three mechanisms could contribute to impaired reinnervation of standard and nerve-implant grafts: impaired axonal elongation, compromised collateral sprouting in an extraendoneurial environment, and impaired synaptogenesis. The relative contributions of each of these mechanisms to axonal regeneration and muscle reinnervation could be greater in old compared with young rats, would then account for the decrease in the force production of standard and nerve-implant grafts in old rats. Our working hypothesis is that the disparity in the recovery of the force-generating capacity of standard and nerve-implant grafts in old compared with young rats results from an impaired ability of grafts in old animals to become reinnervated when axonal regeneration occurs outside the endoneurial sheath. To eliminate the influence of extraendoneurial axonal elongation on the reinnervation of EDL grafts, we utilized a nerve-intact EDL muscle graft model. The specific, null hypothesis is that compared with their age-matched control EDL muscles, nerve-intact EDL grafts in 5-month-old and 25-month-old rats show no differences in whole muscle mass, specific P0, motor unit number, or motor unit P0.


   Materials and Methods
Top
 Abstract
 Materials and Methods
Results
 Discussion
 References
 
Animal Model
Male 3-month-old and 23-month-old, Wi/HicksCar rats that had been inbred for over 100 generations were obtained from a specific pathogen-free colony at the University of Michigan Medical Center. The survival curve of specific pathogen-free male Wi/HicksCar rats is shown in Fig. 1. Nerve-intact grafts of the right EDL muscle in these rats served as the animal model for this study, and unoperated EDL muscles in separate groups of age-matched rats served as controls. All animal housing, care, and operations were in accordance the National Institutes of Health's Guide for the Care and Use of Laboratory Animals, and the experimental protocol was approved by the University Committee on the Use and Care of Animals. Rats were housed individually, provided food and water ad libitum, and exposed to a 12-hour light–dark cycle. For all nerve-intact grafting procedures, rats were maintained in a deep plane of ether anesthesia; for all measurements of muscle contractile properties, a deep plane of sodium pentobarbital general anesthesia was induced (30–40 mg/kg administered intraperitoneally) and then supplemented as required to maintain this level. Aseptic conditions were maintained during all procedures.



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  		Figure 1. Survival curve (squares) of 50 male Wi/HicksCar rats that were allowed to live a normal life span under specific pathogen-free (SPF) conditions. The line connected by circles represents the mean body mass of all surviving animals at the age indicated.

 
Nerve-intact EDL muscle grafts were performed by using a longitudinal incision on the anterolateral hindleg. The EDL muscle belly was freed from surrounding tissue, tendons of origin and insertion were sharply divided, and the vascular pedicle was severed, rendering the muscle ischemic. The integrity of the peroneal nerve (motor nerve to the EDL muscle) was preserved. The tendons of origin and insertion were then repaired by using interrupted 7-0 polyglycolic acid sutures, which restored the muscle to its original resting length. The hindleg incision was closed in layers with 5-0 chromic suture. Previous investigations have demonstrated that the nerve-intact grafting procedure produces ischemic necrosis of the majority of the fibers in the muscle, with preservation of the basal lamina surrounding both muscle fibers and intramuscular axons (5)(15). Rats were administered oral terramycin for the first 7 postoperative days.

Experimental Design
Prior to the grafting procedure, young and old rats were allocated randomly into either a nerve-intact graft (NI) group or an unoperated, control (CTRL) group. After the grafting procedure, all rats were allowed to recover for 60 days before a second operative procedure was performed to measure whole muscle and single motor unit contractile properties. The 60-day recovery period has been demonstrated to be sufficient to allow stabilization of the contractile properties of EDL standard grafts (16). The four groups created a straightforward 2 x 2 experimental design: (1) 5-month-old control group (CTRL-5mos), (2) 5-month-old nerve-intact graft group (NI-5mos), (3) 25-month-old control group (CTRL-25mos), and (4) 25-month-old nerve-intact graft group (NI-25mos).

Measurement of Whole Muscle Contractile Properties
An in situ assessment of the contractility of EDL muscles and motor units was made while the rats were under general anesthesia, in a manner similar to that of previous studies (7)(14)(17). In a custom-built apparatus, the knee and pelvis were firmly pinned and the foot was supported. Body temperature was monitored and maintained at 37°C with a heating pad; muscle surface temperature was monitored and maintained at 35°C. For each rat, the distal EDL tendons were identified through a small incision on the dorsum of the foot, divided, and secured to a Kulite BG-1000 force transducer (Kulite Semiconductor, Leoniea, NJ). A lateral thigh incision was made to expose the sciatic nerve and its branches. As a way to avoid motion artifact during contractile property measurements, the sciatic nerve branches to all hindlimb muscles except the EDL were severed. The peroneus, gastrocnemius, soleus, plantaris, and tibialis anterior muscles were divided and reflected. Throughout the evaluation, the EDL muscle and peroneal nerve were regularly bathed in warm mineral oil (36°C).

Force measurements.-- The EDL muscles were activated indirectly with supramaximal nerve stimuli (square pulses, 0.2-ms pulse duration, 2–6 V) generated by a Grass S88 stimulator (Grass Instrument Co., Quincy, MA) and delivered to the peroneal nerve, 2 cm proximal to the EDL muscle, using a shielded bipolar silver wire electrode (Harvard Apparatus, South Natick, MA). Force output was recorded with an analog-to-digital converter interfaced with a microcomputer with appropriate software. Twitch contractions were used to determine the optimum muscle length for force production, L0. With the muscle set at this length, a single 300-ms stimulation at 80 Hz was delivered, and L0 was again checked by using twitch contractions. All subsequent isometric force measurements were made at L0, which was measured directly with digital calipers. A force-frequency curve was constructed by measuring force during 300-ms trains of stimuli at increasing frequencies (25–250 Hz) until force plateaued at P0. As a way to obtain an estimate of the force-generating capabilities of control and nerve-intact grafts in young and old rats independent of the muscle physiologic cross-sectional area (CSA), the P0 (in kilonewtons) was divided by the total fiber CSA [muscle mass (kilograms)/fiber length (meters) x 1.06 (muscle density in kilograms per cubic meter)] to provide a value of specific P0 (kilonewtons per square meter) (18).

Measurement of Motor Unit Contractile Properties
Contractile properties of single motor units were measured in situ at 35°C with the EDL muscle length secured at L0 (7)(14). The spinal cord was exposed from the midthoracic level to the sacrum by performing a laminectomy. A dorsal skin pouch was created and filled with warmed mineral oil (36°C) to prevent desiccation. The ventral spinal roots from L2 to L6 were isolated and divided. Small filaments of the distal ventral roots were dissected free and stimulated to elicit EDL contraction. The filaments were systematically reduced until the electrical stimulus elicited only one motor unit response. The criteria used to determine if single, as opposed to multiple, motor units were being stimulated were as follows: (1) an all-or-none twitch response to finely graded stimuli; and (2) a smooth, sigmoid-shaped frequency-force curve. Previous work in our laboratory has shown these two criteria to be reliable when used in the selection of single motor units (19). For each motor unit, the maximum tetanic force was measured by using a protocol identical to that for the whole muscle. As many single motor units as possible were identified and studied for each muscle. The total number of motor units in each EDL was estimated by dividing the whole muscle P0 by the mean motor unit P0 for that muscle (7)(19). If fewer than six motor units were measured for a single muscle (<10% of the total number of motor units for control EDL muscles), then the motor unit number was not calculated for that EDL muscle.

Data Analysis
The mean and standard deviations of each variable measured were computed for each group. The significance of the main effects of age (5 months vs 25 months) and of the experimental intervention (nerve-intact EDL grafts vs unoperated control EDL muscles) were determined by using a two-way analysis of variance (ANOVA). The interaction between these main effects was included in the model. For a given variable, individual group means were compared post hoc by using t tests of least-square means only if the F ratio from the corresponding ANOVA achieved significance. Appropriate Bonferroni corrections were applied to all post hoc comparisons. Statistical computations were performed by using a microcomputer and the Statistical Analysis System (SAS, Inc., Cary, NC). For this study, {alpha} was set a priori at 0.05.


   Results
Top
 Abstract
 Materials and Methods
 Results
Discussion
 References
 
Of the 39 rats allocated to the four groups in the experimental design, perioperative mortality resulted in the death of eight rats prior to the completion of the data collection. The distribution of the remaining 31 rats in the four groups is presented in Table 1 , along with the values for the body mass, EDL muscle mass, whole muscle P0, and specific P0. The distribution of motor units in the four groups is presented in Table 2 , along with values for the average motor unit P0 and calculated motor unit numbers per EDL muscle. A total of 304 motor units were measured, with a range of 65–89 motor units per group. The number of motor units studied in individual muscles ranged from four to 23 (average 10.8 ± 7), comprising an approximate range of 7–38% of the calculated total number of motor units in the EDL muscles. In three muscles, less than 10% of the total number of motor units was sampled. These data were not utilized to calculate the mean motor unit P0 for those individual muscles and consequently were not used to estimate the number of motor units per EDL muscle. The muscle masses, whole muscle P0, and the number of motor units sampled per muscle and graft are in good agreement with previous data obtained in our laboratory (7)(8)(9) and in the laboratory of other investigators (20).


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  		Table 1. Sample Size, Body and Muscle Masses, P0, and sP0 for Each Experimental Group

 

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  		Table 2. Motor Unit Sample Size, Mean P0 of Motor Units, and Motor Units per EDL Muscles for Control and Nerve-Intact Grafts

 
The body masses did not differ among the four groups. The EDL muscle masses between the NI-5mos and the CRTL-5mos groups and between the NI-25mos and CRTL-25mos groups were not different. In contrast to the lack of any difference in the body masses among the age groups, the EDL muscle masses of the old control rats were 78% that of the young rats (Table 1 ). The EDL muscle P0 for rats in the NI-5mos group did not differ from that of the CTRL-5mos group (p = .08). Despite the lack of a difference, the 12% reduction in force development between NI-5mos and CTRL-5mos rats, in the absence of a loss in total fiber CSA, is evident in the 16% decrease in specific P0 in the NI-5mos group ( p < .02). Similar to that of young rats, nerve-intact grafting of the EDL muscle in old rats resulted in deficits in both absolute P0 and specific P0 (Table 1 ). Interestingly, EDL whole muscle P0 was reduced 24% in the old compared with the young control rats, but the specific P0 remained unchanged. The 22% atrophy of the EDL muscles in the old compared with the young control rats accounted for this reduction in whole muscle P0.

Compared with the control groups in young and old age categories, the mean motor unit P0 for EDL muscles was reduced 18% and 24%, respectively, for the age-matched nerve-intact grafting groups (Table 2 ). No differences were observed for the estimated number of motor units in EDL muscles from the NI-25mos group (40 ± 3) compared with the CTRL-25mos group (42 ± 2), or between the NI-5mos group (65 ± 4) and the CTRL-5mos group (61 ± 3). However, a dramatic reduction in the total number of motor units per EDL muscle was identified in the old compared with the young rats.


   Discussion
Top
 Abstract
 Materials and Methods
 Results
 Discussion
References
 
These data support our hypothesis that compared with age-matched control EDL muscles, nerve-intact EDL muscle grafts in young and old rats show no evidence of an age-related impairment in reinnervation. At any age, the major difference between nerve-intact grafts and standard or nerve-implant grafts is the presence of the endoneurial sheath, which provides the conduits through which the axons regenerate to the denervated muscle fibers (7)(14)(15)(21). In nerve-intact EDL grafts in young and old rats, the number of motor units per muscle was maintained compared to age-matched control muscles, suggesting that axons regenerating within an endoneurial environment have similar abilities to elongate and establish functional synaptic connections (14).

In standard, nerve-implant, and nerve-intact EDL grafts, regardless of the age of the animal, a deficit in P0 is observed, compared with age-matched control animals. The force deficit in nerve-intact grafts of young rats is due to incomplete muscle fiber regeneration and reinnervation following ischemic necrosis of the muscle (15)(16)(22). Force deficits of similar magnitude have been identified in nerve-intact grafts in young and old rats in the present study, suggesting a common mechanism for this force deficit in both age groups. A full complement of muscle fibers regenerate in nerve-intact EDL muscle grafts (23) along with complete recovery of motor unit numbers, which suggests nearly complete reinnervation of the grafts. Despite the nearly complete recovery, an 18–24% decrease in motor unit P0 in the nerve-intact EDL grafts was noted in both age groups. A number of factors could contribute to this decrease in motor unit P0, including a decrease in motor unit innervation ratio, a decrease in motor unit CSA, or a decrease in force production by single muscle fibers. Overloading the nerve-intact grafts with an appropriate high-load, low-repetition conditioning program may increase the P0 of nerve-intact muscle grafts, but it would not completely eliminate the discrepancy between control and nerve-intact graft P0 (24)(25).

When standard and nerve-implant grafting procedures are performed, the deleterious effect of requiring the motor axons to regenerate outside the endoneurial sheath is inevitable. For young rats, this results in a 50% reduction in number of motor units compared with control muscles (14)(16). Motor unit studies have not been performed on standard EDL grafts in old rats, but data from previous investigations predict that motor unit numbers would be reduced to values even less than the 50% deficit in motor units reported for standard grafts in young rats (14)(26)(27). Our conceptualization of the three general mechanisms operating to impair the isometric contractile function in EDL muscle grafts include the following: (1) factors directly affecting the absolute force production of single innervated muscle fibers in all types of grafts; (2) an intrinsic, age-related impairment of axonal regeneration in standard and nerve-implant grafts in old rats; and (3) impaired axonal regeneration in an extraendoneurial environment in standard and nerve-implant grafts regardless of the age of the rats. Of these, impaired axonal regeneration outside the endoneurial sheath appears to be the most deleterious, and this could be related to the increased amount of interstitial connective tissue, especially in old rats. The hierarchical arrangement of axonal regeneration in young and old animals in an endoneurial compared with an extraendoneurial environment is supported by experimental data for EDL grafts in young and old rats: nerve-intact grafts in young and old rats > standard grafts in young rats > standard grafts in old rats.

In summary, motor reinnervation is a complex process involving axonal elongation, terminal branching, synaptogenesis, competitive synapse elimination, and synapse maturation. Although the present experiment was not designed to distinguish age-related differences in these mechanisms, these data support our hypothesis that if axons are allowed to regenerate in an endoneurial environment, there is no evidence of an age-related impairment in muscle reinnervation. Future experiments have been designed to identify the aspects of nerve regeneration that are deficient in the muscle-grafting models to account for the reduced muscle reinnervation in old animals.


   Acknowledgments
 
This research was supported by a National Institutes of Health Program Project, PO1 AG 10821. We thank Cheryl Hassett for her skilled assistance during the operations.

Address correspondence to Paul S. Cederna, MD, University of Michigan Health Systems, Department of Surgery, 2130 Taubman Center, 1500 East Medical Center Drive, Ann Arbor, MI 48109-0340. E-mail:

Received August 15, 2000

Accepted December 26, 2000


   References
Top
 Abstract
 Materials and Methods
 Results
 Discussion
 References
 

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