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Fiona Bailey
J Neurophysiol 101:276-282, 2009. First published Nov 5, 2008; doi:10.1152/jn.91065.2008
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J Neurophysiol 101: 276 –282, 2009.
First published November 5, 2008; doi:10.1152/jn.91065.2008.
Pittman LJ, Bailey EF. Genioglossus and intrinsic electromyo- constitute a hydrostatic “skeleton” (Kier and Smith 1985;
graphic activities in impeded and unimpeded protrusion tasks. J Skierczynski et al. 1996; Smith and Kier 1989) and provide the
Neurophysiol 101: 276 –282, 2009. First published November 5, reaction forces needed for tongue movement. In this respect,
2008; doi:10.1152/jn.91065.2008. Eight muscles invest the human
tongue: four extrinsic muscles have external origins and insert into the tongues, trunks, and tentacles offer a novel framework within
tongue body and four intrinsic muscles originate and terminate within which to consider the nervous system control of movement
the tongue. Previously, we noted minimal activation of the genioglos- because cooperative contraction of muscles underpins move-
sus tongue muscle during impeded protrusion tasks (i.e., having ment and provides the structural platform necessary for deliv-
subjects push the tongue against a force transducer), suggesting that ery of external force.
Address for reprint requests and other correspondence: E. F. Bailey, De- The costs of publication of this article were defrayed in part by the payment
partment of Physiology, College of Medicine, The University of Arizona, of page charges. The article must therefore be hereby marked “advertisement”
Tucson, AZ 85721-0093 (E-mail: ebailey@u.arizona.edu). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
276 0022-3077/09 $8.00 Copyright © 2009 The American Physiological Society www.jn.org
EMG ACTIVITY IN IMPEDED AND UNIMPEDED PROTRUSION TASKS 277
METHODS cannot state with certainty which of the muscles we recorded from.
Thus in the remainder of this study we refer to this EMG recording as
We performed experiments in 10 healthy human volunteers (6 women
the “intrinsic muscle” EMG, although most of the activity likely
and 4 men; ages 20 –54 yr). All experimental procedures were approved
originates from the verticalis and transversus muscles.
by the Human Subjects Committee at The University of Arizona. Sub-
Surface electrodes (4-mm-diameter Ag/AgCl) attached to the skin
jects gave their informed consent before participation in the study.
overlying each mastoid process served as indifferent electrodes for
tungsten and fine-wire EMG recordings. A ground strap was placed
EMG recordings around the upper arm. EMG signals were amplified (⫻1,000, Model
EMG activities were recorded from the genioglossus (GG) muscle 15; Grass Instruments, West Warwick, RI) and band-pass filtered
and from the intrinsic tongue muscles. The GG muscle arises from the (0.3–3 kHz). Intrinsic and extrinsic whole muscle EMG activities
medial aspect of the mandibular symphysis and fans out dorsoven- were sampled at 10 kHz and GG SMUAPs were sampled at 20 kHz
trally to insert into the central mass of the tongue (Takemoto 2001). and recorded on the Spike2 data acquisition and analysis system
The protocol for electrode insertion has been reported previously (CED, Cambridge, UK). The amplified and filtered whole muscle
(Bailey et al. 2007a,b). Briefly, we determined the distance from the EMG signals were subsequently rectified and moving-time averaged
skin surface to the inferior border of the GG muscle via ultrasonog- with a time constant of 200 ms.
raphy (Pro Sound 3500; Aloka, Tokyo, Japan) (Eastwood et al. 2003).
For whole muscle GG EMG activities, a tungsten needle electrode (1- Experimental protocol
to 5-m tip diameter, 250-m shaft diameter; FHC, Bowdoinham,
ME) with insulation removed from the terminal tip (⬃2 mm) was Subjects were seated upright in a dental chair with their head
inserted transcutaneously into the floor of the mouth, with the entry supported. Respiratory movements of the chest were monitored by a
point about 1.5 cm from the midline and about 2– 4 cm posterior to the respiratory effort transducer (Pro-Tech, Mukilteo, WA) positioned
(Grass) and displayed using the Spike2 data acquisition and analysis position). When a significant F value was obtained, differences were
program (CED). tested using post hoc contrasts with significance levels adjusted
Tongue tip position (mm) was referenced to neutral or rest position according to the Bonferroni procedure. A one-way ANOVA was used
(i.e., relaxed jaw, mouth slightly open, and tongue tip visible just to test the effect of task (i.e., force vs. position) on the average initial
behind the lower incisors). Positive position values indicate protrusion and peak firing frequencies (Hz) of GG single motor units for each
from the rest position, whereas negative values indicate retraction trial. When a main effect was found, post hoc comparisons were
from this position. Subjects started from their rest position and first performed with significance levels adjusted according to the Bonfer-
protruded and then retracted the tongue to the rest position. Subjects roni procedure. A significance level of P ⬍ 0.05 was used for all
were provided with visual feedback via an ongoing display of tongue comparisons.
position on a slowed timescale but were not instructed to attain a
particular point/location in space. RESULTS
IMPEDED PROTRUSIONS. In this task, an isometric force transducer
(World Precision Instruments, Sarasota, FL) was attached to the lever Within-subject performance on successive unimpeded and
arm described earlier (Fig. 1B). Because forward movement of the impeded protrusion tasks revealed excellent reproducibility
tongue was impeded in this configuration (see Fig. 1B) the task (Fig. 2, A and B). Although the absolute tongue excursion
approximated an isometric contraction. Subjects were required to varied between subjects, the within-subject SE in performance
attain force targets of 10 and 30 g using visual feedback of the target on successive trials was minimal for both unimpeded (⫾2.7
force and their task was to match the target force. mm) and impeded protrusion (⫾3.2 g) trials.
Subjects completed three trials comprising each of the tasks in Representative raw recordings of GG and intrinsic muscle
sequence as follows: unimpeded protrusions; impeded protrusions; EMG activities, tongue position (mm), and force (gm) in
Data analysis
All data were acquired and analyzed using Spike2 and custom-
designed software (CED). Quantitative comparisons of EMG activi-
ties were made as follows. Average whole muscle GG and intrinsic
muscle activities were expressed as a percentage of the maximal
response (% max), as defined earlier. Single motor-unit action poten-
tials were discriminated using a template-matching algorithm based
on waveform shape and amplitude as discussed previously (Bailey
et al. 2007b). For analysis of average discharge rate and variability,
only those motor units whose activities could be followed throughout
each series of unimpeded protrusion and impeded protrusion tasks
were included. The initial firing rate at recruitment was calculated
from the first 10 interspike intervals (ISIs) in both the unimpeded and
impeded protrusions. Peak firing rate was determined as the highest
rate for 10 consecutive ISIs during the task. For each recorded motor
unit mean values for initial and peak firing rates were calculated from
the average of three trials recorded in each condition. The estimate of
the population variance in discharge frequency (needed to calculate
sample size) is based on the only available estimate of the SD in
discharge frequency measured for GG motor units in human subjects
during volitional tasks (3.3 Hz) (Bailey et al. 2007). For this SD and
to detect differences of 4 Hz, with a power of 0.8 at a significance of
0.01 requires about 25 samples.
Task-related differences in whole muscle average EMG activities FIG. 2. A: distance (mm) relative to rest position attained by each subject
were assessed initially with a single within-subjects repeated-mea- (1–10) on successive unimpeded protrusion trials. B: forces attained by each
sures ANOVA testing main effects (and interactions) for muscle (% subject (1–10) on successive impeded protrusion trials for 10-g (black trian-
max GG vs. % max intrinsic) as a function of task (i.e., force vs. gles) and 30-g (gray triangles) force target trials.
task. Relative to GG EMG, the intrinsic muscle EMG activities decreased protrusive force but rather remained stable through-
were significantly smaller in magnitude in the unimpeded out (Fig. 5, right). Thus for all impeded protrusion trials the
protrusion task and significantly larger in the impeded protru- average firing rate was 16.4 ⫾ 8.2 Hz, slightly higher than that
sion tasks (i.e., 30 g, Fig. 4). measured at the onset of the unimpeded protrusions (10.8 ⫾ 2).
Representative raw recordings showing the instantaneous The absence of any correspondence between firing rate and
firing rate of a discriminated single GG motor unit, tongue force during impeded protrusion tasks supports the hypothesis
position, and tongue protrusion force are presented in Fig. 5. that GG motor-unit activities are modulated in accordance with
Consistent with previously published findings (Bailey et al. tongue position, but not isometric force production. These
2007b), we observed systematic changes in GG muscle motor- findings have important implications for our understanding of
unit firing rate as a function of unimpeded tongue protrusion how the nervous system controls tongue muscles during simple
tasks (see Fig. 5, left). In this example, the motor unit was protrusion tasks, as explained in the following text.
recruited about 5 mm from the rest position and discharged at
an initial rate of 10.8 ⫾ 2 (SD) Hz, increasing to a peak rate of DISCUSSION
22.5 ⫾ 2 Hz. For all unimpeded protrusion trials, the firing rate
at recruitment was 11.5 ⫾ 4 Hz and increased to 25.3 ⫾ 4 Hz Summary
at peak displacement. By contrast, firing rate did not exhibit Hydrostats have been extensively studied at a kinematic
any systematic change either as a function of increased or level yet we know remarkably little about patterns of muscle
interaction of intrinsic and extrinsic tongue muscles in all versus) generate most of the tongue protrusion forces, but only
tongue movements (Smith and Kier 1989). when stabilized by contraction of the GG muscle, as discussed
Second, we have shown previously that GG MU activities in the following text.
are tightly modulated in accordance with tongue position
(Bailey et al. 2007b) but not force. Importantly, because the Working model for human tongue protrusion and force
sustained firing rates evident in the force task approximate
those previously recorded in static holding maneuvers (Bailey On the basis of current observations we have devised a
et al. 2007b) we suggest that the GG muscle fulfills a support- working model to clarify the roles fulfilled by the GG and the
ive but not a primary role in the generation of protrusive force intrinsic muscles in each task (see Fig. 6). Consistent with the
(see following text). In contrast, the GG plays a prominent role traditional view of tongue protrusion, GG contraction advances
in unimpeded displacement tasks. Intrinsic protrudor muscles, the tongue base, whereas activation of the intrinsic protrudor
on the other hand, appear to play a major role in both tasks. The muscles in the tongue tip reduces the diameter of the anterior
data suggest that the multivectorial intrinsic muscles that com- body of the tongue. Because the tongue is a constant volume
prise the core of the anterior tongue (i.e., verticalis and trans- structure, the reduction in tongue diameter secondary to intrin-
FIG. 6. A working model of tongue muscle activation in unimpeded and impeded protrusions. Left panels: schematic lateral view of the tongue showing the
extrinsic tongue muscles (genioglossus [GG], hyoglossus [HG], and styloglossus [SG]) that have external bony origins on the mandible (m), hyoid bone, and
styloid process, respectively. The intrinsic muscles transversus (t) and verticalis (v) interdigitate extensively and have both origins and insertions in the central
tongue body. Right panels: force and position traces, with corresponding integrated GG and intrinsic muscle activities. A, left: tongue configuration at rest (dashed
outline) and in unimpeded protrusions. In this task there is activation of both the GG and intrinsic muscles (see EMG activities at right), with corresponding
changes in position but not force. GG activation causes anterior movement of the tongue base (denoted by arrow) and activation of the intrinsic muscles verticalis
and transversus compresses the tongue body, contributing to protrusion beyond the mandible, as described in the text. B, left: schematic of the tongue
configuration at rest (dashed outline) and during an impeded protrusion against an external structure (black bar, representing the force transducer). As in A,
impeded protrusions also involve activation of the GG and intrinsic muscles. Contraction of the intrinsic muscle fibers compresses the tongue body, resulting
in expansion in the long axis, which registers as protrusive force. However, force will not be registered unless GG activation fulfills a platform function that
stabilizes the tongue base (denoted by double-headed arrow), thereby resisting rearward movement that would otherwise occur in this soft-bodied structure. In
this task the magnitude of the intrinsic muscle activities exceeds that of the GG (see right panel). The magnitude and direction of the forces contributed by the
2 extrinsic retractor muscles, hyoglossus (HG) and styloglossus (SG) (arrows), are also incorporated into this working model. Although the activities of these
muscles and resultant forces were not recorded in our experiments, based on respiratory-related tongue muscle activities in human subjects (Mateika et al. 1999;
Oliven et al. 2007), we postulate that the retractor muscles also are coactive with the GG and intrinsic muscles in these tasks. Activation of the HG may be of
particular importance in protrusive force tasks as a secondary stabilizer of the tongue base (Oliven et al. 2007).
sic muscle-mediated contraction results in elongation of the Blumen MB, Perez de la Sota A, Quera-Salva MA, Frachet B, Chabolle F,
tongue. What is crucial, however, is that although the GG Lofaso F. Genioglossal electromyogram during maintained contraction in
normal humans. Eur J Appl Physiol 88: 170 –177, 2002.
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tongue protrusion requires activation of the intrinsic protrudor human genioglossus in patients with obstructive sleep apnea. Respir Physiol
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our observation that during unimpeded protrusions, GG and Eastwood PR, Allison GT, Shepherd KL, Szollosi I, Hillman DR. Hetero-
intrinsic muscle activities are of comparable magnitude (Fig. 6, geneous activity of the human genioglossus muscle assessed by multiple
right). bipolar fine-wire electrodes. J Appl Physiol 94: 1849 –1858, 2003.
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Our data also show that impeded protrusions involve acti-
lingual hydrostatic deformation. J Exp Biol 210: 4069 – 4082, 2007.
vation of GG and intrinsic muscle activities. As stated earlier, Hiiemae KM, Palmer JB, Medicis SW, Hegener J, Jackson BS, Lieberman
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peded, results in the development of protrusive force. In this Kayalioglu M, Shcherbatyy V, Seifi A, Liu ZJ. Roles of intrinsic and
scenario, GG activation fulfills a vital platform function that extrinsic tongue muscles in feeding: electromyographic study in pigs. Arch
counteracts (or resists) rearward movement as intrinsic muscle Oral Biol 52: 786 –796, 2007.
Kier WM, Smith KK. Tongues, tentacles and trunks: the biomechanics and
contraction attempts to elongate the tongue. Note that in this movement of muscular hydrostats. Zool J Linnean Soc 83: 207–324, 1985.
case neural drive to the intrinsic muscles is greater than that for Liu ZJ, Kayalioglu M, Shcherbatyy V, Seifi A. Tongue deformation, jaw
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GG and a primary role for intrinsic protrudor muscles. 52: 309 –312, 2007.