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Delayed muscle fiber transformation after foreign-reinnervation of excessive muscle tissue.

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THE ANATOMICAL RECORD 223:347-355 (1989)
Delayed Muscle Fiber Transformation After ForeignReinnervation of Excessive Muscle Tissue
Institute of Anatomy, University of Zurich-Irchel, CH-8057 Zurich, Switzerland
Following partial denervation motor units can increase (by selfreinnervation) as much as four to five times their normal size. To investigate the
still unknown quantitative reinnervation capacity of a motor nerve in the case of
foreign-reinnervation, in adult male rats the denervated sternomastoid muscle was
either self-reinnervated by its original nerve or foreign-reinnervation by the omohyoid nerve, which had to reinnervate the three times the amount of muscle fibers
and six times the amount of muscle mass. After survival times of 7, 8, 9, or 10
months, nerves and muscles were investigated histochemically and immunohistochemically. The omohyoid nerve could fully reinnervate the sternomastoid muscle,
but at 7 and 8 months this muscle still revealed nearly the same proportions of IIA
and IIB fibers as were seen in the self-reinnervated sternomastoid at all stages.
However, in the following 2 months a shift of the fiber pattern toward that of the
normal omohyoid was observed, as evidenced by a strong increase in type IIB fibers
(from 24% to 62%),at the expense of type IIA fibers. These findings are in contrast
to those after foreign (cross) reinnervation of leg muscles where the fiber transformation (according t o the foreign motor input) occurs in parallel with the reinnervation process during the first 2-3 months. The delayed fiber transformation observed
could be the consequence of the highly enlarged peripheral field of the omohyoid
motoneuron pool or could merely reflect a general difference between limb and neck
muscles. Whatever the case may be, in the present experiments the afferent input,
which is not fully restored until 9 months, could play a crucial role in contrast to
limb muscles, where the successful motor reinnervation takes place in the absence
of sensory activity.
The morphological, physiological, and metabolic characteristics of muscles are largely determined by the innervating motoneurons (Buller et al., 1960; Close, 1965;
Guth, 1968; Buchthal and Schmalbruch, 1980; Jolesz
and Sreter, 1981; Pette and Vrbova, 1985). Within most
muscles the proportions of the different fiber types are
rather constant over long periods, the content of transitional fibers being very low. However, the fiber spectrum of a given muscle may be altered by a variety of
stimuli, such as training (Salmons and Henriksson, 1981;
Howald, 1982; Schantz, 1986; Baumann et al., 1987),
hormones (mainly thyroid hormones) (Ianuzzo et al.,
1977; Fitts et al., 1980; Nicol and Bruce, 1981; Nwoye
and Mommaerts, 1981; Nwoye et al., 1982; Johnson et
al., 1983; Florini, 1987; Muntener et al., 1987),artificial
chronic stimulation, or foreign-reinnervation (Guth,
1968; Jolesz and Sreter, 1981; Pette and Vrbova, 1985).
A special kind of neuromuscular plasticity is seen in
the aging muscle (Campbell et al., 1973; Kugelberg,
1976; Caccia et al., 1979; Jenny et al., 1980; Larsson,
1982; Edstrom and Larsson, 1987). Beside an altered
fiber type composition (mainly in slow muscles), a gradual loss of motoneurons is observed (Larsson, 1982; Edstrom and Larsson, 1987), leading to a partial
denervation of the muscle. A considerable amount of
these muscle fibers are reinnervated by collateral
0 1989 ALAN R. LISS, INC.
sprouting from neighboring axons (Harriman et al.,
1970; Kugelberg et al., 1970; Grinnell and Herrera, 1981;
Wernig and Herrera, 1986; Edstrom and Larsson, 1987),
resulting in an enlargement of the remaining motor
units. This denervation-reinnervation process leads to a
consequent reorganization of fiber types in which type
grouping (Karpati and Engel, 1968) replaces the usual
checkerboard pattern of fiber types.
These observations lead to the question of the amount
of muscle fibers that can additionally be innervated by
a single axon. Neurophysiological experiments with partially denervated muscles have shown that motor units
can increase by as much as four to five times their
normal size (Thompson and Jansen, 1977; Brown and
Ironton, 1978; Brown et al., 1981; Grinnell and Herrera,
1981; Hatcher et al., 1985). However, the studies mentioned above only examined the motoneurons that were
self-reinnervating their original muscle. Nothing is
known about the quantitative and qualitative reinnervation capacity in the case of foreign-reinnervation.
Received May 4,1988, accepted August 8,1988.
Address reprint requests t o Markus Miintener, Anatomisches Institut der Universitat Zurich-Irchel, Winterthurerstrasse 190, CH-8057
Zurich, Switzerland.
In the present investigation the omohyoid nerve was
brought to reinnervate the denervated sternomastoid
muscle. The sternomastoid muscle has six times the
amount of muscle mass and three times the amount of
muscle fibers, including type I fibers, which are lacking
in the omohyoid muscle (Gottschall et al., 198Ob; Muntener et al., 1980). Histo- and immunohistochemical investigation of nerve and muscle revealed a successful
foreign-reinnervation. However, in this quantitatively
asymmetric type of cross-reinnervation, the foreign motor input led to a delayed fiber transformation starting
7 months after reinnervation, in contrast to the classical
cross-reinnervation experiments in limb muscles (with
comparable fiber ratios) in which the fiber transformation roughly parallels the reinnervation process.
Young adult male rats (2.5 months old; 250-300 g;
strain Zur:SIV) supplied by the Institute of Laboratory
Animal Science, University of Ziirich, were used. The
animals were anesthetized with 0.25 m l k g body weight
Innovar-Vet (Pitman-Moore) IM combined with 2.5 mg
Valium (Roche) and 7.5 mg Nembutal (Abbott) IP.
Surgical Procedures
As in the human, the sternomastoid muscle in rat
arises from the manubrium of the sternum and is inserted into the mastoid. The sternomastoid nerve (entering laterally into the muscle) originates from two
separate roots: a motor root from the accessory nerve
and a sensory root from the cervical plexus (Gottschall
et al., 1980b). The two omohyoid muscles (inferior and
superior), which are connected by a n intermediate tendon, extend from the anterior border of the scapula to
the hyoid bone, passing behind the sternomastoid. The
omohyoid superior muscle lies close to the lateral border
of the sternohyoid. It is supplied by a branch of the
superior radix of the ansa cervicalis, which enters the
muscle medially a t the point where it crosses the sternomastoid (Muntener et al., 1980).
In 13 animals the right sternomastoid muscle was
denervated by resecting the sternomastoid nerve between the point of entry into the muscle and the fusion
of its motor and sensory roots. For additional prevention
of self-reinnervation, the accessory nerve was transected
and the proximal stump sutured into the posterior belly
of the digastric muscle. The omohyoid superior nerve
was exposed and cut near its entrance into the muscle.
After excision of a short segment (for the first determination of the number of alpha-motor axons), the nerve
was sutured medially into the sternomastoid muscle,
opposite to the point of entry of the original nerve. To
avoid a growth of omohyoid nerve fibers toward the
denervated omohyoid superior muscle, this muscle was
In 11animals the accessory and sternomastoid nerves
were transected and loosely adapted (without suture).
Fourteen age-matched animals served as controls.
Histochemical Procedures
After survival times of 7,8, 9, and 10 months, respectively, the animals were deeply anesthetized with Nembutal, and the functional reinnervation was evidenced
(see below and under Results).
The experimental sternomastoid and contralateral
sternomastoid and omohyoid superior muscles were either frozen in toto in melting isopentane (- 160°C) or
divided transversely into three parts. The cranial third
was frozen, the middle third was fixed with 4% formaldehyde in 0.2 M phosphate buffer @H 7.4), and the
caudal third was fixed with Bouin’s fluid and embedded
in paraffin. Control muscles were processed in the same
Cryocut cross sections (12 pm) were reacted for myofibrillar ATPase according to Guth and Samaha (19701,
with certain modifications as described elsewhere (Miintener, 1979,1982). For the demonstration of alkali-stable
ATPase, preincubations at pH 10.4 and 10.5 were combined with incubation at pH 9.5 or 9.6. For the demonstration of acid-stable ATPase, preincubation at pH 4.3
or 4.25 was followed by incubation at pH 9.5. In half of
the muscles the cryocut sections were processed for the
combined demonstration of myofibrillar ATPase (after
alkali and acid preincubation) and acetylcholinesterase
(AChE, E.C., according to Ashmore et al. (1981)
and Toop (1976).
Every eighth cryosection (12 pm) of the muscles frozen
in toto was treated according to the alpha-naphthylacetate method for nonspecific esterases with fast red as a
coupling agent (Pearse, 1972).
Fibers were classified into the following types: IA
(equivalent to the classical “slow-twitch oxidative,” i.e.,
type I fiber); IB and IIC (both transitional fibers) (Brooke
and Kaiser, 1970; Karpati et al., 1975; Jansson et al.,
1978); and IIA (“fast-twitch oxidative glycolytic”) and
IIB (“fast-twitch glycolytic”). Fiber typing and counting
of types IA, IB, and IIC was performed as described
elsewhere (Muntener, 1982). For the determination of
the number of IIA and IIB fibers (as well as the total
number of fibers), the slides were directly enlarged on
photographic paper and the fibers counted. In the normal sternomastoid muscle a deep “red” portion (consisting of types I and I1 fibers and containing all the muscle
spindles) and a superficial “white” portion (lacking type
I fibers) are clearly distinguishable. Such a grouping is
no longer the case in the self- and foreign-reinnervated
muscles. Thus mean percentages of different fiber types
were also calculated for normal muscles.
Omohyoid superior and sternomastoid nerves were either fixed in 4% paraformaldehyde in 0.1 M sodium
cacodylate buffer (pH 7.6) and processed according to the
method of Karnovsky and Roots (1964), or fixed in 2.5%
glutaraldehyde in 0.1 M sodium cacodylate buffer (pH
7.61, postfixed with 0 ~ 0 4 and
embedded in epon (for 1
pm semithin sections).
Single Fiber Preparation
The formaldehyde-fixed middle portions of the muscles
containing the majority of the end plates (EPs) and additional entire control muscles were divided into thin
bundles, incubated in the medium of Koelle and Friedenwald (19491, and further processed for single fiber
preparations as described elsewhere (Miintener and
Zenker, 1986). On orthographically projected EPs, the
AChE-stained areas were measured using a MOP-AM02
image analyzing system.
Morphometric Procedures
Determination of the mean diameters of the different
muscle fiber types, mean diameter of axons, and number
of alpha-motor axons was performed as described elsewhere (Miintener et al., 1980; Gottschall et al., 1980a,b).
Briefly, the cross-sectional areas of a representative
number of each muscle fiber type were measured with
the MOP-AM02 image analyzing system and the fiber
diameters calculated by assuming a cylindric form of
the muscle fibers. Analogously, the diameters of all myelinated motor and sensory axons of the nerves investigated were determined in semithin sections. For
differentiation between motor and sensory nerve fibers,
histochemical demonstration of axonal AChE was used
(Karnovsky and Roots, 1964) and the diameters of the
AChE-positive(motor)axons evaluated. The populations
of alpha- and gamma-motor axons were arbitrarily separated by dividing the smallest class (5.0-6.0 pm) between the two peaks of the diameter histogram.
Number and localization of EPs were determined
semiquantitatively. The sections (every eighth, stained
for nonspecific esterases) were projected on to a screen
on which 20 vertical test lines were superimposed. The
muscle was aligned so that the lines passed parallel to
its deep to superficial axis. The EPs within each strip
were counted and each amount symbolized on a horizontal line with a dot of corresponding size (diameter of the
dot = 1mm per EP). By assembling these dot diagrams
along the longitudinal axis of the muscle, a two-dimensional representation of the extension and density of the
area containing EPs (in the following called “end plate
zone” [EZ]) was obtained. Superimposed on this representation of the EZ was a reconstruction of the intramuscular branching pattern of the nerve (Fig. 1). This
reconstruction also served for the evaluation of a successful foreign-reinnervation.
Three months after reinnervation, the animals (selfand foreign-reinnervated) showed no asymmetry in head
posture or movement in running and swimming tests.
Self-reinnervation was successful in all animals; type
I fibers were regularly present in these muscles. The
foreign-reinnervation of the sternomastoid was successful in ten animals, as evidenced by physiologic and morphologic criteria, i.e., there was a twitch response when
cutting the omohyoid nerve, and an absence of such a
response when cutting the sternomastoid nerve stump;
the reinnervated muscle completely lacked type I fibers;
the intramuscular nerves were branches of the omohyoid superior nerve. Since the short omohyoid nerve
Fig. 1. Diagrammatic representation of the end plate zone (shadowed) of a normal sternomastoid muscle. The density of the end plates
(EPs) is indicated hy dots of graded size (one to ten EPs per unit area)
or squares (more than ten EPs; see text for details). For graphical
reasons the end plate zone is elongated by a factor of 4. The dark lines
represent the intramuscular main branches of the sternomastoid nerve.
Fig. 3. Relative fiber type proportions in self-reinnervated (S-STM)
(A) and foreign-reinnervated (F-STM)(B) sternomastoid muscle. Numbers indicate months after surgery; each bar represents the mean
values of two to three animals (for clarity the indication of the SD has
been omitted). For comparison the fiber type ratios of normal sterno-
1- (
mastoid (N-STM)and normal omohyoid (N-OMO)are shown on the left
and on the right side in A and B, respectively. Note the strong increase
of the proportion of IIB fibers in the F-STM between 8 and 9 months,
leading to a fiber pattern similar to that of N-OMO.
ran through scar tissue adhesions (to adjacent muscles), 2B,C). The former deep (red) portion was only identifiathe sternomastoid muscle could not be stimulated ble according to the presence of the persistent muscle
spindles. One foreign-reinnervated muscle exhibited a
narrow area with very small denervated fibers ( - 5% of
total fiber number).
Seven months postoperatively both the self- and forThe regained muscle mass (in percentage of agematched control muscles) was comparable in all stages. eign-reinnervated sternomastoid muscles revealed a low
The following percentages (mean t- SD) were calculated: percentage of type IIB fibers (25% and 24%, respectively). While in the self-reinnervated muscles the ratio
15.5% after foreign-reinnervation and 93.6
12.4%after self-reinnervation. In all experimental mus- of the fiber types remained the same during the whole
cles the total fiber number as well as the diameters of period investigated, in the foreign-reinnervated muscles
the different fiber types (myosin-based classification) the proportion of IIB fibers strongly increased, from 24%
varied within the normal range. Transitional fibers (type to 60%, at the expense of IIA fibers, until month 9 (Fig.
IB and IIC) were only sporadically found. Fiber splitting 3). Thereafter the fiber type distribution remained eswas not observed. Groups of fiber types were dispersed sentially constant in the foreign-reinnervated muscles
over the entire cross-sectional area of the muscles (Fig. also (Fig. 3).
Fig. 2. Transverse sections of normal (A), self-reinnervated (B; 9 fibers (present only in normal and self-reinnervated sternomastoid)
months postoperatively), and foreign-reinnervated (C; 10 months post- appear white, as they are completely lacking in activity. Type IIA
operatively) sternomastoid muscle and of normal omohyoid muscle 0) fibers are black to dark gray, and IIB are intermediate-stained in
stained for myofibrillar ATPase (preincubation at pH 10.5, incubation different degrees of intensity (see left and right side in A). Note “type
at pH 9.5 or 9.6). In the sternomastoid muscles (A-C), the deep muscle grouping” in the experimental muscles (B,C). x40.
portion is on the left and the superficial one on the right. Type IA
Fig. 4. Cross section of the same omohyoid superior nerve before (A)
and 10 months after (B,C)reinnervation of the sternomastoid muscle.
The reinnervating nerve consists of one large (B) and two small (C)
branches embedded within scar tissue. Before implantation of the
nerve (A), 21 alpha-axons and after 10 months of survival (B,C), 23
alpha-axons were determined (see text for details). Epon-embedded
semithin sections, phase contrast. x 1,150.
The contralateral muscles did not differ from normal
control muscles.
mean sizes of the EPs in normal omohyoid and sternomastoid and in experimental sternomastoid muscles did
not differ significantly during the period investigated.
With the semiquantitative method used, 41.7 -t 6.8%
(SD) of the EPs present in the muscles (one EP per
muscle fiber) were statistically surveyed for the graphic
representation of the EZ. In normal and in both self- and
foreign-reinnervated sternomastoid, the pyriform EZ
was constantly situated in the center, extending over
24-40 32% of the muscle length. In the foreign-reinnervated sternomastoid, the branches of the omohyoid superior nerve invaded the EZ medially according to the
implantation site.
The reinnervating omohyoid nerve was regularly
found to branch before its entry into the muscle, leading
mostly to a very short nerve stem (Fig. 4).However, in
four animals the nerve was long enough to allow a clear
determination of the number of alpha-axons (as determined by a series of consecutive sections lying 0.2 mm
from one another); on an average, 61 & 5% of the myelinated axons were alpha-axons. In these cases the
numbers of alpha-axons counted before and after reinnervation were comparable (& 10%).In the other animals the second determination yielded higher (4585%)
values because of the proximal branching of some axons.
The number of alpha-axons in the self-reinnervating
sternomastoid nerve varied within the normal range. In
this nerve between 34% and 39% of the myelinated
axons were found to be alpha-motoric.Muscle fiber type
ratio, fiber diameter, total fiber number, number of alpha-axons, and motor unit size of experimental and control animals after ten months’ survival time are
summarized in Table 1.
It is well known from partial denervation experiments
that motor axons can sustain a much larger peripheral
field as long as motoneurons and muscle are well
matched (Thompson and Jansen, 1977; Brown and Ironton, 1978; Brown et al., 1981; Grinnell and Herrera,
1981; Hatcher et al., 1985).The aim of the present study
was to evaluate if motoneurons display the same capacity when reinnervating a much larger foreign muscle of
different fiber composition and function. Fiber number
and diameter were restored quantitatively throughout,
End Rate Zone (€2’)
following self- and foreign-reinnervation, reflecting an
Analysis of the single fiber preparations of entire mus- undisturbed trophic situation of the reinnervated
cles showed all fibers to have a single end plate. The muscles.
TABLE 1. Overall proportions and diameters of the different fiber types (myofibrillar ATPase),
number of muscle fibers and alpha-axons, average size of motor units in normal (N-STM),
self-reinnervated (S-STM), and foreign-reinnervated (F-STM) sternomastoid and normal omohyoid (N-OMO)
muscle after 10 months of survival (mean f SD)
Fiber type proportions (%)
Fiber diameter
Number of muscle
Number of
Average size of
4.2 f 1.0
49.3 f 6.2
46.5 f 7.1
71.5 k 4.9
22.9 f 0.2
38.2 f 2.4
61.8 f 2.4
26.1 f 7.8
43.1 f 7.1
66.8 f 16.2
86.5 f 10.0
44.5 & 8.2
70.7 f 12.1
87.1 f 12.8
83.4 f 9.1
61.8 f 8.1
65.9 & 6.3
89 f 8
93 f 11
4,940 f 600
25 f 10
1,650 f 310
22 & 6
‘Number of animals.
’Fiber type not present.
Establishment of
final fiber pattern
IReinnervation I
Establishment of
Establishment of
final fiber pattern
IReinnervation I
Fig. 5. Time course of the establishment of the fiber pattern after
foreign-reinnervation. If the fiber ratio of the original to the foreign
muscle is comparable (“symmetric” reinnervation), the fiber transformation leading to the final fiber pattern occurs parallel to the reinnervation. In the case of a considerable excess of musculature to be
reinnervated (“asymmetric” reinnervation), a fiber transformation in
two steps is observed. The first reinnervation phase with an intermediate fiber pattern, precedes the establishment of the final fiber pattern, according to the foreign motor input.
The cases in which the number of alpha-axons was the
same before and after foreign-reinnervation demonstrated the capability of the omohyoid nerve to reinnervate a considerable excess of fiber number (threefold)
and muscle mass (sixfold), also proving that it is not the
nerve that determines the number of muscle fibers to be
reinnervated. There is strong evidence that in the other
cases, with higher axon numbers after reinnervation,
the sternomastoid muscle was also reinnervated exclusively by the omohyoid nerve (and not by branches of
axons to other infrahyoid muscles). Branching of regenerating myelinated axons leading to the same increased
number of axons (distally to the regeneration site) as in
the present study (average 60%) has also been found in
other nerves (Carter and Lisney, 1987).
However, two remarkable observations were made: a
strong predominance of oxidative fibers (types IA and
IIA) in the self-reinnervated muscles on the one hand
and a highly delayed fiber transformation in the foreignreinnervated muscles on the other hand. Compared with
controls, in the self-reinnervated sternomastoid muscles
at all stages increased percentages of types IA and IIA
fibers were found at the expense of IIB fibers. This
finding is in marked contrast to hindlimb muscles (cat
and rat) and infrahyoid muscles (rat) where after selfreinnervation mainly a normal fiber distribution is restored (Chan et al., 1982; Dum et al., 1985a,b; authors’
unpublished observation). Probably in the sternomastoid muscle IIA alpha-axons are more aggressive and
vigorous in reinnervating than IIB alpha-axons. The
same phenomenon has been observed in partially denervated hindlimb muscles (Hatcher et al., 1985).
As expected, the foreign-reinnervated sternomastoid
muscles exhibited qualitatively the fiber type distribution of the omohyoid muscle, i.e., only type I1 (A and B)
fibers. However, the quantitative fiber type ratios were
most striking. At 7 and 8 months postoperatively the
proportions of IIA and IIB fibers were mostly the same
as in the self-reinnervated sternomastoid muscles. But
in the following 2 months the proportion of IIB fibers
strongly increased, from 24% to 62%, changing the fiber
pattern of the foreign-reinnervated muscle toward that
of the normal omohyoid muscle (Fig. 3). This shift in
fiber composition was also evidenced histochemically by
the reaction for cytochrome c oxidase and immunohistochemically using antibodies against the Ca2+-binding
protein parvalbumin (data not shown).
To our knowledge this kind of delayed muscle transformation in response to cross- or foreign-reinnervation has
not yet been observed. On the one hand, this could be
the consequence of the highly enlarged peripheral field
of the omohyoid motoneuron pool, meaning that a n excess of muscle mass is trophically reinnervated in a first
consolidating phase before it is transformed according
to the new motor input (Fig. 5). On the other hand, the
delayed transformation could also reflect a general difference between limb and neck muscles, which are primarily controlled from supraspinal centers (Rapoport,
In leg muscles with comparable fiber ratios the establishment of the final fiber pattern occurs parallel to the
reinnervation, and the motoneuron activation patterns
remain largely unaltered when their axons reinnervate
foreign muscles (O’Donovan et al., 1985).
The motor reinnervation of the extrafusal fibers is
complete after 2-3 months (depending on the age of the
animal), while the sensory reinnervation of the muscle
spindles takes around 9 months (Collins et al., 1986).
Thus the omohyoid motoneuron pool reinnervating the
sternomastoid muscle receives the full afferent input
long after the re-establishment of the motor innervation.
Additionally, the sternomastoid muscle contains 10 to
15 times more muscle spindles than the omohyoid muscle (Gottschall et al., 1980b; Muntener et al., 1980). It
can be hypothesized that the afferent feedback modifies
and/or increases the activity pattern of the motoneurons, which would not be able to induce a corresponding
muscle fiber pattern until afferent reinnervation is
largely completed. If so, this could explain why a second
fiber transformation occurred at such a late period (between 8 and 9 months) in the present experiments. The
transformation was most probably brought forth by a n
increased synaptic remodeling, leading to larger IIB and
smaller IIA motor units (Wernig and Herrera, 1986).
Thus, in contrast to limb muscles, in which restoration
of the motoneuron properties (after self- and foreignreinnervation) does not require full restoration of sensory activity (Kuno et al., 1974; Gallego et al., 1980;
Goldring et al., 1980), in our case for whatever the rea-
son (increased muscle mass or singularity of neck muscles), the afferent input could play a crucial role.
We thank Ms. I. Drescher, R. Forster, C. Meyer, and
H. Weber for excellent technical assistance. The monoclonal antibodies against parvalbumin were a gift of Dr.
M.R. Celio, Kiel, F.R.G. We are indebted to Drs. W.
Neuhuber and W. Zenker for helpful suggestions. We
are grateful to the Stiftung fur Wissenschaftliche Forschung a n der Universitat Zurich for financial support.
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