Department of Physiology, Emory University School of Medicine, Atlanta, Georgia 30322
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ABSTRACT |
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Sokoloff, Alan J.. Localization and Contractile Properties of Intrinsic Longitudinal Motor Units of the Rat Tongue. J. Neurophysiol. 84: 827-835, 2000. Tongue dysfunction is a hallmark of many human clinical disorders, yet we lack even a rudimentary understanding of tongue neural control. Here, the location and contractile properties of intrinsic longitudinal motor units (MUs) of the rat tongue body are described to provide a foundation for developing and testing theories of tongue motor control. One hundred and sixty-five MUs were studied by microelectrode penetration and stimulation of individual motor axons coursing in the terminal portion of the lateral (retrusor) branch of the hypoglossal nerve in the rat. Uniaxial MU force was recorded by a transducer attached to the protruded tongue tip, and MU location was estimated by electromyographic (EMG) electrodes implanted into the anterior, middle, and posterior portions of the tongue body. All MUs produced retrusive force. MU twitch force ranged from 2-129 mg (mean = 35 mg) and tetanic force ranged from 9-394 mg (mean = 95 mg). MUs reached maximal twitch force in 8-33 ms (mean = 15 ms) and were resistant to fatigue; following 2 min of stimulation, MUs (n = 11) produced 78-131% of initial force. EMG data were collected for 105 MUs. For 65 of these MUs, the EMG response was confined to a single electrode location: for 26 MUs to the anterior, 21 MUs to the middle, and 18 MUs to the posterior portion of the tongue. Of the remaining MUs, EMG responses were observed in two (38/40) or all three (2/40) tongue regions. These data provide the first contractile measures of identified intrinsic tongue body MUs and the first evidence that intrinsic longitudinal MUs are restricted to a portion of tongue length. Localization of MU territory suggests a role for intrinsic MU in the regional control of the mammalian tongue observed during feeding and speech.
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INTRODUCTION |
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Despite the
importance of the mammalian tongue in normal oro-motor behavior and the
association of tongue dysfunction with many human clinical syndromes
(e.g., cerebral palsy, Down's syndrome, obstructive sleep apnea,
tongue thrusting; Adachi et al. 1993; Dent
1995
; Guilleminault et al. 1995
; Lowe
1981
; Murdoch et al. 1995
; Yarom et al.
1986
), we lack even a basic understanding of the physiological
organization of the fundamental output elements of the tongue motor
system, i.e., the hypoglossal (tongue) motor units (MUs). Study of
hypoglossal MU organization is hampered by the complexity of tongue
muscular architecture. Eight muscles are present in the tongue of many
mammals: four originating outside the tongue body [the "extrinsic"
muscles genioglossus (GG), hyoglossus (HG), styloglossus (SG), and
palatoglossus] and four having both origin and insertion within the
tongue body [the "intrinsic" muscles inferior longitudinalis (IL),
superior longitudinalis (SL), transversus (T) and verticalis (V)].
Extrinsic and intrinsic muscles interdigitate extensively within the
tongue, making functional isolation of tongue body musculature, and
thus of identified MUs, difficult.
Due in large part to the complexity of tongue anatomy, studies of MU
organization have focused either on MUs of extrinsic muscles (e.g.,
Fuller et al. 1998; Yokota et al. 1974
;
see references in Lowe 1981
) or on MUs commonly
classified as "protrusor" (motor axons coursing through the medial
branch of the hypoglossal nerve) or "retrusor" (motor axons
coursing through the lateral branch) (DiNardo and Travers
1994
; Gilliam and Goldberg 1995
; Kaku
1984
; Sumi 1970
; Travers and Jackson
1992
). Few of these studies have included contractile
characterization of MUs, and thus the relationship between MU activity
and unit contractile properties is unknown.
Further, none of these studies have considered the organization of MUs
of identified intrinsic muscles. Yet information on the organization of
MUs of intrinsic muscles is likely important for developing and testing
models of tongue motor control. For example, one current theory of
tongue control, the muscular-hydrostat theory, posits a central role
for intrinsic muscles in both tongue movements and posture (Kier
and Smith 1985). Additionally, by virtue of their anatomical
distribution, intrinsic muscles may be involved in the independent
control of different tongue regions observed during feeding in mammals
(Hiiemae et al. 1995
) and in the complex changes in
tongue shape observed during speech in humans (Stone
1990
).
The neural mechanisms responsible for the control of regional tongue movements are not known, but presumably involve selective activation of MUs of localized territory within the tongue body. As part of an ongoing investigation of the physiology and activity of hypoglossal MUs, here I describe the contractile properties and location of intrinsic longitudinal MUs, i.e., MUs of intrinsic muscles with axons coursing through the terminal branch of lateral hypoglossal nerve. Two questions necessary to define the role of these MUs in regional tongue control are addressed. First, are intrinsic longitudinal MUs localized within the tongue body? And, second, if localized, do MU properties vary in a systematic way with location? Findings indicate that intrinsic longitudinal MUs produce small forces, are nonfatiguing, and are localized within the tongue body. These results are discussed in light of current theories of tongue control.
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METHODS |
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Nine adult male rats (Sprague-Dawley, 300-350 g) were used in terminal experiments. All surgeries were done in accordance with the NIH Guidelines on the Use of Animals for Research and were approved by the Institutional Animal Care and Use Committee at Emory University. Sodium pentobarbital (40 mg/kg) was administered intraperitonally, and surgery proceeded when withdrawal and eye-blink reflexes were completely suppressed. Supplemental doses (0.4 mg/kg, ip) were given as needed to maintain a surgical plane of anesthesia. At the end of the experiment, rats were euthanized by barbiturate overdose (sodium pentobarbital, iv).
Surgical procedure
Cannulae were secured in the right femoral artery to measure blood pressure and in the right femoral vein for infusion of dextrose (5%) in lactated Ringer solution to support mean blood pressure above 80 mmHg. Body temperature was continuously monitored and maintained at 36-38°C by radiant heat. A cannula was inserted into the trachea, and during the experiment, the rate and volume of respiration were adjusted, when necessary, to maintain end-tidal CO2 between 3-5%. Rats were placed supine in a rigid frame and secured with ear bars and maxilla clamp. The suprahyoid region was dissected to expose the branches of the left hypoglossal nerve (see Data collection). Throughout, care was taken to preserve the blood supply to muscles and nerves. The mylohyoid muscles and anterior digastric muscles were removed bilaterally, the left geniohyoid muscle was separated from the hyoid bone, reflected medially, and its nerve was cut. The main trunk of the hypoglossal nerve was carefully exposed at its emergence deep to the digastric tendon and the proximal portions of the medial and lateral hypoglossal nerve branches were exposed, as were the nerve branches to the GG muscle, the HG muscle, and the SG muscle. Following nerve dissection, the hyoid bone, origin of muscle and connective structures of the tongue, was clamped to ensure that subsequent force measurements would not be attenuated by hyoid movement.
A piece of 2-0 silk suture was secured into the tongue tip and attached
to a strain gauge (Kulite) with an estimated minimal sensitivity of
~0.2 mg resolution for measurement of contractile properties (see
Gilliam and Goldberg 1995; Hellstrand
1981
). Previous study has demonstrated that similar contractile
measures are obtained whether the tongue is attached to a transducer or
is free to move (Hellstrand 1981
). In five experiments,
three indwelling bipolar electrodes (50-µm wire diameter, 0.5-mm
exposed tips) were placed in the center of anterior, middle, and
posterior sections of the left tongue body to record MU
electromyographic (EMG) signals. In these experiments, MUs were
assigned to one of six categories based on the location of EMG
response: anterior, middle, posterior, antero-middle, postero-middle,
or whole tongue. The entire exposure (i.e., supra and infrahyoid
dissections, the oral cavity, and the tongue) was submerged in
mineral oil maintained at 36-38°C. Following data collection, the
tongue was removed and dissected to confirm nerve pattern and EMG
electrode placement.
Data collection
ANATOMICAL ISOLATION OF INTRINSIC LONGITUDINAL MUS.
The population of MUs that project to intrinsic longitudinal muscles of
the left side of the tongue body was isolated by transection of the
hypoglossal nerve branches that project to all other muscles. First,
nerve branches to the left GG, HG, and SG were cut, leaving intact the
motor axons that project to intrinsic tongue muscles. Second, the
medial hypoglossal nerve was cut, disrupting the motor axons that
project to transverse and vertical intrinsic muscles (Hellstrand
1981; O'Reilly and Fitzgerald 1990
); this
eliminated the potential study of transversus and verticalis muscles
which, although oriented perpendicular to the long axis of the tongue, may produce retrusive forces on the transducer when the tongue is
protruded (see Gilliam and Goldberg 1995
). Following
these sections, only the axons coursing in the terminal portion of the lateral hypoglossal nerve branch were left intact. In many mammals, these axons are thought to project to both superior and inferior intrinsic longitudinal muscles; in some mammals, however, superior longitudinal muscles are innervated by branches of the medial hypoglossal nerve (Hellstrand 1981
; O'Reilly and
Fitzgerald 1990
; for recent discussion see Mu and
Sanders 1999
). A glycogen depletion experiment was performed to
definitively identify the MU population examined in the present study.
In one rat, left hypoglossal nerve branches were cut as described
above; the left hypoglossal nerve trunk was placed on a bipolar
electrode and stimulated for 2 h [330-ms burst, 100 parts per
second (pps), 1 burst/s], and the tongue was removed and processed for
glycogen (following Edström and Kugelberg 1968
).
In this experiment, depletion of glycogen was observed in all
ipsilateral intrinsic longitudinal muscles, i.e., including
the superior longitudinal muscles (Fig.
1). Thus, axons left in continuity in the
present study are classified as "intrinsic retrusor tongue body
MUs," i.e., lateral nerve branch motor axons that innervate inferior,
lateral, and superior longitudinal muscle fibers.
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ACTIVE TENSION OF INTRINSIC RETRUSOR MU POPULATION. MU contractile properties were measured in eight animals. Prior to isolation of individual MUs, the effect of tongue length on forces generated by the entire population of intrinsic longitudinal MUs was measured to establish an optimal tongue length for MU characterization. In each experiment, the left hypoglossal nerve trunk was placed on a bipolar electrode and stimulated at 2 times twitch threshold. Tongue length was increased in 10 or more 1-mm increment steps, corresponding to a range of passive tensions between 0 and 10 g, and twitch force was determined at each length. The tongue length at which the largest force was produced was considered optimal for single unit studies.
PHYSIOLOGICAL ISOLATION AND STIMULATION OF INDIVIDUAL MUS.
Conventional glass microelectrodes (15-25 m, 2 M K-acetate) were
driven into single axons in the left hypoglossal nerve trunk to measure
contractile properties of individual MUs (following techniques of
Cope and Clark 1991
). Single motor axons were isolated by intra-axonal injection of depolarizing current (0.5-3.0 nA) in
bursts delivered every 4 s (100 pps, 40-µs duration, 330-ms burst) as the electrode was lowered in 2-µm intervals (Transvertex Microdrive, Harvard Apparatus). Penetration of an isolated motor axon
was determined by a change in force profile coincident with stimulation, and when possible (see RESULTS), the
presence of EMG signal coincident with stimulation. In some
penetrations, current strength was graded (to 3 times threshold) to
verify that multiple MUs were not activated during stimulation.
Microelectrode penetration of isolated motor axons has been
successfully employed to study contractile properties of single MUs in
hindlimb muscles (see Cope and Clark 1991
; Tansey
and Botterman 1996
). Advantages of the intra-axonal technique
include isolation of single motor axons with certainty and the ability
to regularly record from many MUs in single experiments (up to 44 in
the present study) allowing for within-animal analysis of MU measures.
Data analysis
Contractile data were analyzed in SigAvg software (CED). MU twitch contraction time was measured from the beginning of the force deflection to peak force and MU fatigue was determined by comparing initial MU force to force produced following 120-s stimulation or, in less stable penetrations, following 60-s stimulation. To allow extensive comparisons to studies of other muscles, nonparametric tests of correlation (Spearman R) were used to identify relationships between MU properties. Whole nerve stimulation indicated that, for the entire population of MUs, force varied substantially with tongue length (see RESULTS). To investigate whether there was an effect of tongue length on the properties of individual MUs, a Mann-Whitney U Test (Statistica Software) was performed for groups of MUs sampled at different tongue lengths. A one-way analysis of variance (ANOVA) with passive tongue tension (an indirect measure of tongue length) as a covariate was also computed to compare contractile measures for MUs located in different tongue regions; comparisons between treatment means were made using the Tukey honest significant difference test (Statistica Software).
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RESULTS |
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Effects of tongue tension on whole tongue retraction force
The relationship between passive tongue tension and tongue twitch
force produced by supramaximal stimulation of the left hypoglossal nerve with only the terminal branch of the lateral hypoglossal nerve
intact is shown in Fig. 2. Active twitch
force increased during initial increases in tongue length (passive
tension 0 to <2 g), but changed little with further increases (passive
tension 2 g). Because of this relationship, passive tongue tension of
2 g was sought for measurement of MU properties. This criterion was
met for most (77%) MUs. MUs studied at passive tongue tensions of <2
g are, however, included in the analysis to allow tests of the effect
of passive tongue tension on contractile measures of individual
MUs. Tongue tip position during these tests ranged from
completely within the oral cavity (0 g passive tension) to 15-mm
anterior to the root of the upper incisors.
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Description of MU contractile properties
MU FORCE AND CONTRACTION TIME.
One hundred and sixty-five MUs were recorded in eight animals
representing from 3 to 44 MUs per animal (Table
1). The tetanic and twitch responses of a
single unit are shown in Fig. 3. It was
not possible to obtain all measures for each MU, nor was it possible to
attain a passive tension of 2 g for tests of all MUs. For 165 MUs,
tetanic force ranged from 9 to 394 mg (95 ± 71 mg, mean ± SD); for 124 MUs, twitch force ranged from 2-129 mg (35 ± 25 mg), and contraction times ranged from 8 to 33 ms (15 ± 4 ms; see
Table 1). Twitch/tetanic ratios ranged from 0.08 to 0.77 (0.36 ± 0.11).
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MU FATIGUE AND FUSION FREQUENCY.
Following 120 s of repetitive stimulation (see
METHODS), 11 MUs produced from 78 to 131% of initial force
[i.e., fatigue index (FI) of 0.78-1.31; Fig.
4A]. An additional six units
produced from 74 to 117% of initial force after 60 s of
stimulation. By these measures, 16/17 tested MUs are nonfatiguing, and
1/17 is fatigue-intermediate, following the classification of
Burke et al. (1973). Tests of fusion frequency were
completed in five units (Fig. 4B). Summation of twitch force
was evident in all units at 50-Hz stimulation and maximum tetanic force
was obtained between 100 and 125 Hz stimulation.
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Relationships between MU contractile properties
Significant correlations between MU contractile properties were
present in the MU sample (Fig. 5; Table
2). MU twitch force was strongly and
positively correlated with tetanic force (R = 0.89, P < 0.0001; Fig. 5A; Table 2). MU
contraction time was weakly and positively correlated with twitch force
(R = 0.23; P < 0.05; Fig.
5B; Table 2) and with tetanic force (R = 0.19; P < 0.05; Table 2). MU fatigue
(n = 17, see Data collection) was
not significantly correlated with any contractile measure. Significant
differences in tetanic and twitch force were not present in comparisons
between MUs assigned to one of two groups based on contraction time
(Mann-Whitney U test for groups demarcated at 14.5, 19.0, and 20.0 ms) in contrast to findings in other rat muscles (e.g.,
lateral gastrocnemius and soleus, Gillespie et al. 1987;
medial gastrocnemius, Kanda and Hashizume 1992
;
Gardiner 1993
; plantaris, Gardiner and Olha
1987
).
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Relationships between passive tongue tension and MU properties
The demonstration that increases in passive tongue tension from 0 to 2 g were associated with increases in the active twitch tension of the total MU population (see Fig. 2) suggested an effect of passive tongue tension on individual MU measures. Indeed, for the entire MU sample, weak but significant correlations were observed between passive tongue tension and MU tetanic force (R = 0.21, P < 0.01; Table 2; Fig. 6A) and between passive tongue tension and twitch force (R = 0.26, P < 0.005; Table 2; Fig. 6B). A stronger correlation was observed between passive tongue tension and MU contraction time (R = 0.62, P < 0.0001; Table 2; Fig. 6C).
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To further explore the relationships between passive tongue tension and
MU contractile measures, the population of MUs studied at passive
tongue tensions of <2 g was compared with the population of MUs
studied at passive tongue tensions of 2 g. Although there was
substantial overlap in the distribution of measures of these two groups
(Fig. 6), significant differences were present for measures of tetanic
force (P < 0.01), twitch force (P < 0.05), and contraction time (P < 0.001) (Mann-Whitney
U test). Evaluation of the relationship between passive
tongue force and MU contractile properties among MUs within each of
these two groups, however, revealed only a single significant
correlation, i.e., between contraction time and passive tongue tension
for MUs in the
2 g passive tension group (R = 0.45, P < 0.0001).
Analysis of individual experiments
One strength of the intra-axonal technique is the ability to
collect large samples in single experiments allowing within-animal analysis. In all seven experiments for which nine or more MUs were
studied, tetanic and twitch force measures were highly significantly correlated (Spearman R values 0.78-0.97; P < 0.005).
In contrast, MU contraction time measures were significantly correlated
with tetanic force measures in only 2/7 experiments, contraction time increasing with tetanic force in one (R = 0.59, P < 0.01) and decreasing in another (R = 0.42, P < 0.05). MU contraction time measures were
significantly correlated with twitch force measures in only 1/8
experiments (R = 0.58, P < 0.01). The
effect of passive tongue tension on contractile measures was also
minimal, with significance attained in only 2 of 21 possible
correlations across the seven experiments, with twitch force in
experiment 8 (R = 0.68, P < 0.05) and
twitch contraction time in experiment 5 (R = 0.41, P < 0.05.) Thus, many relationships observed for the
entire MU sample are not observed within individual animals.
MU location
EMG signatures were recorded for 105 MUs. For many of these MUs, the EMG response was confined to a single electrode location: for 26 MUs to the anterior tongue, 21 MUs to the middle tongue, and 18 MUs to the posterior tongue. An example of a MU with EMG signature confined to the middle tongue is shown in Fig. 3. Of the remaining MUs, EMG responses were observed in anterior-middle (14/40), middle-posterior (24/40), or all three (2/40) tongue regions. A one-way ANOVA, with passive tongue tension as a covariate (because of its effect on MU properties, see Relationships between passive tongue tension and MU properties), was computed to compare the tetanic force, twitch force, and contraction times of MUs with EMG responses in anterior, middle, and posterior regions. For the combined sample, the only significant effect of location was found for tetanic force (P < 0.05). Tukey posthoc analysis indicated significant difference (P < 0.05) in the tetanic force of posterior (mean = 0.121 g) versus anterior (mean = 0.061 g) MUs. Significant differences were not found for contraction time or for twitch force measures. Additional analysis including MUs localized to anterior-middle and middle-posterior tongue regions revealed a similar pattern: in all significant comparisons, MU force was larger in the most posterior of the groups compared.
Samples were sufficiently large to allow tests of location effects on MU properties in three individual experiments. Significant differences were only observed for twitch and tetanic forces in one experiment (P < 0.05); for each measure, larger values were observed for the most posterior of the tongue regions compared (Tukey posthoc analysis). There was no effect of location on contraction time.
Estimation of MU number
Studies in the cat hindlimb have shown that MU forces do not sum
linearly and that single MU force measures may be influenced by common
compliance and by the internal friction produced by adjacent passive
muscle fibers (see Clamann and Schelhorn 1988; Powers and Binder 1991
). Mechanical interactions among
MUs have not been studied in the tongue, but may be particularly
complex due both to the organization of tongue muscle and connective
tissue structures and to the localization of individual MU territories. Nevertheless, an estimate of the number of MUs that comprise the intrinsic longitudinal muscle was made in the present study. In seven
experiments, the following measures were obtained: 1)
average MU twitch force, 2) average passive tongue tension
at which MU measures were made, and 3) maximal twitch force
produced by stimulation of hypoglossal nerve (following nerve
transections described in METHODS) with the tongue length
near average passive tension (i.e., within 0.050-0.550 g average
passive tension). Maximal twitch force was divided by average MU twitch
force (see Fig. 2). By these estimates, the number of MUs in the seven
experiments ranged from the 131 to 511 (average = 345 ± 119).
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DISCUSSION |
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This study provides the first detailed description of the contractile properties of identified intrinsic tongue MUs. The major findings of this study are that intrinsic longitudinal MUs of the rat tongue body 1) produce small twitch and tetanic forces compared with other rat MUs, 2) have twitch contraction times similar to other rat MUs, 3) are nonfatiguing, and 4) are localized to a portion of anterior-to-posterior tongue length.
Contractile properties: relation to other studies
In previous studies of rat hypoglossal nucleus organization,
Goldberg and colleagues used extracellular stimulation to activate motoneurons innervating tongue muscle generally (Gilliam and
Goldberg 1995) and innervating the styloglossus muscle
specifically (Sutlive et al. 1999
). Similar to the
present study, the activation of motoneurons whose axons course in the
lateral branch of the hypoglossal nerve [i.e., supplying HG, SG, IL,
and SL (see METHODS)] produces contractions that reach
maximal twitch force in 13.5 ms, have a high resistance to fatigue, and
reach tetanic fusion at an average of 92.5 Hz (Gilliam and
Goldberg 1995
; see also Sutlive et al. 1999
).
The average twitch force of styloglossus MUs (36 mg) is also similar to
measures reported here for intrinsic longitudinal MUs.
Differences between the contractile properties of intrinsic
longitudinal MUs and the properties of other rat hypoglossal MUs, however, are also apparent. MUs of the styloglossus express a narrower
range of twitch force measures (17.4-80.0 mg; Sutlive et al.
1999) than do MUs of the longitudinal intrinsic tongue muscles
(2-129 mg). Intrinsic longitudinal MUs express a narrower range of
fatigue measure [all FI > 0.70] than do styloglossus MUs (30%
with FI < 0.70). Additionally, the average force values produced
by extracellular stimulation of unidentified motoneurons in the lateral
nerve (86 mg average MU twitch force and 755 mg average MU tetanic
force, Gilliam and Goldberg 1995
) are much higher than
average values for either styloglossus (Sutlive et al.
1999
) or intrinsic longitudinal MUs (present study). The >2-8 fold difference in these measures compared with the present study may
be due to the inclusion of HG in the study of Gilliam and Goldberg, a
possibility that would suggest that HG MUs produce on average more
force than other retrusor MUs. Differences in force measures may also
be related to the passive tongue tension at which MUs were studied (5 g
in Gilliam and Goldberg 1995
, versus an average of
3.3 g in the present study), although the effect of passive tongue
tension on MU force is weak (see RESULTS). It is also
possible that extracellular stimulation of the hypoglossal nucleus
activated multiple MUs (Gilliam and Goldberg 1995
).
In measures of contraction times, intrinsic longitudinal tongue MUs are
similar to MUs of other rat muscles. Twitch contraction times of rat
tibialis anterior MUs range from 11 to 18 ms (Bakels and Kernell
1993a), with an average of 15.5 ms (Totosy de Zepetnek et al. 1992
), and twitch contraction times of medial
gastrocnemius MUs range from 12.9 to 36.2 ms (Kanda and
Hashizume 1992
; see also Gardiner and Olha
1987
). Tongue MUs differ from hind limb MUs, however, in
measures of force and fatigability. Tibialis anterior MUs produce
5-441 mN tetanic force (Totosy de Zepetnek et al. 1992
;
see also Bakels and Kernell 1993a
) and 1.5-34.5 mN twitch force (Bakels and Kernell 1993a
), and
gastrocnemius MUs have similar values for these contractile measures
(Bakels and Kernell 1993b
; Kanda and Hashizume
1989
). Thus despite similar ranges in contraction time, single
intrinsic longitudinal tongue body MUs produce some 100-1000 times
less force than rat hind limb MUs. Intrinsic longitudinal tongue MUs
have low measures of fatigability when compared with other rat muscles
(FI of 0.05-1.35 measured in tibialis anterior and medial
gastrocnemius MUs; Kanda and Hashizume 1992
;
Totosy de Zepetnek et al. 1992
). Twitch/tetanus ratios
of tongue MUs are similar to ratios of rat lumbrical and medial
gastrocnemius MUs (Gates et al. 1991
; Kanda and
Hashizume 1989
), but greater than twitch/tetanus ratios of rat
tibialis anterior, plantaris, and lateral gastrocnemius MUs
(Bakels and Kernell 1993a
; Gardiner and Olha
1987
; Seburn and Gardiner 1995
).
The forces produced by rat intrinsic longitudinal tongue MUs are
similar to those of oculomotor MUs in the cat and monkey. In the cat
superior oblique muscle, for example, MU twitch forces range from 3 to
237 mg (mean = 27.5) and tetanic forces from 11 to 1327 mg
(mean = 141) (Waldeck et al. 1995). MUs of similar force are found in the primate lateral rectus (means of 10.7 mg twitch
force and 186.2 mg tetanus force; Goldberg et al. 1998
). Unlike rat tongue MUs, however, oculomotor MUs contract very rapidly (<15 ms, Goldberg et al. 1998
; Waldeck et al.
1995
), have a high fusion frequency (e.g., 150-260 Hz,
Goldberg et al. 1998
), and express a wide range of
fatigabilities (FI of 0.01-1.15; Shall and Goldberg
1995
).
There are few studies of the muscle fiber histochemistry of the rat
tongue. Myofibrillar ATPase staining revealed that virtually all muscle
fibers of the rat styloglossus are type IIa (Sutlive et al.
1999). Sato et al. (1989)
reported that 86% of
longitudinal muscle fibers in the rat tongue are "red" or
"intermediate" (i.e., strongly or moderately oxidative). These
findings, in concert with the large percentage of fatigue-resistant MUs
in the styloglossus and intrinsic longitudinal muscles (Sutlive
et al. 1999
), suggest that the contractile/histochemical
relationships of tongue MUs are similar to those of other muscle
systems (see Burke 1981
; Sutlive et al.
1999
). In the present study, however, fatigable units were not
encountered as would be expected of "white" fibers (14% of
longitudinal muscle fibers in Sato et al. 1989
); this may reflect the relatively small number of MUs for which fatigue measures were recorded in the present study, and/or differences in
population of the MUs investigated.
Contractile properties: correlations
Among intrinsic longitudinal tongue MUs, twitch force is strongly
and positively correlated with tetanic force (R = 0.89). A strong positive correlation between force measures is also
present in all seven individual animal analyses (R > 0.77). In contrast, correlations between contraction time and force
measures for the total sample are weak (R < 0.24) and
are significant in only 2 of 7 animals. In this respect, intrinsic
longitudinal tongue MUs are similar to MUs of muscles which have either
very weak and negative or nonsignificant relationships between MU
contraction time and force measures, e.g., the rat tibialis anterior
(Bakels and Kernell 1993a), cat soleus, tibialis
anterior, and extensor digitorum longus (Goslow et al.
1977
; Mosher et al. 1972
), rabbit masseter
(Kwa et al. 1995
), and human masseter and nasal dilator (Goldberg and Derfler 1977
; Mateika et al.
1998
).
MUs are commonly categorized into fast or slow "types" based,
respectively, on the presence or absence of a decline in force during
unfused tetanus (i.e., the "sag" property, see Burke et al.
1973). "Fast" and "slow" MUs often differ in other
contractile properties, with fast units usually producing more force
and contracting more rapidly than slow units. In the present study, sag
was not tested, and MUs were not classified according to type. However, when MUs were segregated into groups based on contraction times that
distinguish fast from slow units in other rat muscles (e.g., 14.5 ms in
the tibialis anterior, 19 ms in the plantaris; Bakels and
Kernell 1993a
; Gardiner and Olha 1987
), no
significant differences between the force measures of the groups were observed.
The independence of force and contraction time measures in intrinsic
longitudinal tongue MUs raises the possibility that MUs may be selected
into activity for either property, i.e., speed or force, in different
behaviors. This contrasts with the organization of many muscles in
which MU force and speed measures are interrelated such that
recruitment of MUs of increasing force results in the obligate
recruitment of MUs of increasingly fast contraction speeds (Burke 1981; Cope and Clark 1991
; for
discussion see Bigland-Ritchie et al. 1998
).
Contractile properties: effect of passive tongue tension
During oro-motor behaviors, the mammal tongue may extend 50-100%
of its resting length (Kier and Smith 1985). Here, weak
correlations were found between passive tongue tension and two measures
of MU force (R < 0.27); a stronger correlation was
found between passive tongue tension and contraction time
(R = 0.62). Differences in MU force and speed of
contraction were also evident when the sample of MUs measured at <2 g
passive tension was compared with the sample of MUs measured at
2 g.
This effect of tongue tension on MU properties was observed over a
range of tongue tensions that corresponded to tongue positions in
normal rat oromotor behaviors (i.e., tongue tip within the oral cavity
to 13 mm anterior to the incisors, see Whishaw and Tompkins
1988
), suggesting that the contractile effects of individual
MUs may change during tongue movement. Direct studies of the
length-tension properties of individual MUs are necessary to fully
explore these relationships.
MU localization and functional morphology of the tongue
Independent kinematic control of different tongue regions has been
documented during mammal feeding (Hiiemae et al. 1995) and human speech (Stone 1990
). The neural bases of
regional tongue control have not been described, but likely involve the
differential activation of MUs located in different tongue body
regions. Due to their circumscribed location within regions of the rat
tongue body, intrinsic longitudinal tongue MUs are candidates for
coordinating regional control of tongue movements. The large number of
intrinsic longitudinal MUs, estimated at 345 in the present study,
suggests that regional coordination by these MUs may be both specific
and complex. Indications that transverse and vertical MUs are also localized in the rat and macaque tongue (based on anatomical tracing studies, i.e., Aldes 1995
; Sokoloff and Deacon
1992
) suggest that regional organization may be a feature of
intrinsic tongue MUs generally.
In the present study, posterior MUs produced more tetanic force
on average than anterior MUs, suggesting a possible functional distinction between retrusor MUs located in these different tongue regions. A nonuniform distribution of fiber types among intrinsic tongue muscle in the macaque, such that the percent of slow twitch muscle fibers is greatest in posterior versus anterior tongue regions,
also suggests possible functional differences in anterior versus
posterior MUs in this species (De Paul and Abbs
1996). Regional fiber-type distributions have not been
described for individual tongue muscles of the rat and thus is it not
known if the spatial differences in contractile properties of rat
retrusor MUs observed here are accompanied by differences in MU
fiber-type composition.
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ACKNOWLEDGMENTS |
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The author thanks Dr. T. C. Cope for graciously providing space, equipment, and technical assistance and for giving so freely of his time; this project would not have been possible without his encouragement and support. The author thanks Drs. T. C. Cope and B. D. Clark for comments on the manuscript, Drs. A. W. English and D. W. Wigston for providing histology and microscopy resources, and G. Cotsonis for statistical advice.
This research was supported by National Institute on Deafness and Other Communication Disorders Grant DC-03302 to A. J. Sokoloff.
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FOOTNOTES |
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Address for reprint requests: Dept. of Physiology, 1648 Pierce Dr., Emory University, Atlanta, GA 30322 (E-mail: Sokoloff{at}physio.emory.edu).
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.
Received 15 October 1999; accepted in final form 11 May 2000.
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REFERENCES |
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