1Medical Research Council Group in Sensory-Motor Neuroscience and 2Department of Physiology, Queen's University, Kingston, Ontario K7L 3N6, Canada; 3Laboratory of Neurophysiology, School of Medicine, Université Catholique de Louvain, 1200 Brussels, Belgium; 4School of Pharmacy, University of Southern California, Los Angeles 90033; and 5Department of Biomedical Engineering, University of Southern California, Los Angeles, California 90089
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ABSTRACT |
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Corneil, Brian D.,
Etienne Olivier,
Frances J. R. Richmond,
Gerald E. Loeb, and
Douglas P. Munoz.
Neck Muscles in the Rhesus Monkey. II. Electromyographic Patterns
of Activation Underlying Postures and Movements.
J. Neurophysiol. 86: 1729-1749, 2001.
Electromyographic
(EMG) activity was recorded in 12 neck muscles in four alert monkeys
whose heads were unrestrained to describe the spatial and temporal
patterns of neck muscle activation accompanying a large range of head
postures and movements. Some head postures and movements were elicited
by training animals to generate gaze shifts to visual targets. Other
spontaneous head movements were made during orienting, tracking,
feeding, expressive, and head-shaking behaviors. These latter movements
exhibited a wider range of kinematic patterns. Stable postures and
small head movements of only a few degrees were associated with
activation of a small number of muscles in a reproducible synergy.
Additional muscles were recruited for more eccentric postures and
larger movements. For head movements during trained gaze shifts,
movement amplitude, velocity, and acceleration were correlated linearly
and agonist muscles were recruited without antagonist muscles. Complex
sequences of reciprocal bursts in agonist and antagonist muscles were
observed during very brisk movements. Turning movements of similar
amplitudes that began from different initial head positions were
associated with systematic variations in the activities of different
muscles and in the relative timings of these activities. Unique
recruitment synergies were observed during feeding and head-shaking
behaviors. Our results emphasize that the recruitment of a given muscle
was generally ordered and consistent but that strategies for
coordination among various neck muscles were often complex and appeared
to depend on the specifics of musculoskeletal architecture, posture, and movement kinematics that differ substantially among species.
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INTRODUCTION |
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Much work on simian head
movement has focused on orienting behaviors (e.g., Crawford et
al. 1999; Freedman and Sparks 1997
) in an effort
to extend work done on saccadic eye movements in head-restrained
preparations. Studies of the saccadic system usually employ saccades
themselves as an index of the underlying neural events and kinetics
because the mechanics of this system are relatively intuitive. In
contrast, head movements are generated by more than two dozen muscles
operating on a complex multiarticular linkage endowed with substantial
inertia (Richmond and Vidal 1988
; Winters 1988
). The design and interpretation of experiments on such a system requires knowledge of its structural elements, which is provided
in the companion paper on muscle morphometry (Richmond et al.
2001
).
Chronically indwelling electrodes in animals provide the opportunity to
assess reliably electromyographic (EMG) activity in muscles not
accessible in humans. Studies in human neck muscles have generally
relied on surface EMG from large, relatively superficial muscles
(Dee and Zangemeister 1998; Hannaford et al.
1985
; Keshner et al. 1989
;
Mayoux-Benhamou and Revel 1993
; Mayoux-Benhamou
et al. 1997
; Zangemeister et al. 1982
) or
percutaneous EMG from only one or two muscles whose identities can be
hard to determine (Mayoux-Benhamou et al. 1995
). A
broader range of muscles have been studied previously in cats
(Keshner 1994
; Keshner et al. 1992
;
Richmond et al. 1992
; Thomson et al. 1994
,
1996
; Wilson et al. 1983
), but the differing features of feline head-neck structure potentially limit the
applicability of these results to primate studies. Previous studies in
monkeys have recorded neck muscle EMG in a few neck muscles or during a
restricted subset of head movements (Bizzi et al. 1971
;
Le Goff et al. 1992
; Lestienne et al. 1995
,
2000
). However, little systematic study to date has focused on
the relationships between simian head kinematics and neck muscle
activation during a more extensive sampling of neck muscles and head movements.
In this study, the spatial and temporal patterns of EMG activity were examined in a large number of neck muscles in monkeys free to move their heads. Head postures and movements were generated either in a trained protocol requiring gaze shifts to visual targets or were generated spontaneously during orienting, tracking, feeding, expressive, and head-shaking behaviors. The inclusion of the latter head movements increased the range of kinematic patterns beyond those which accompanied trained gaze shifts.
Some results have been reported previously in abstract form
(Corneil et al. 1996, 1999
).
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METHODS |
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Surgical and training procedures
Four male monkeys (Macaca mulatta) weighing 5.4-9.1 kg were used in these experiments according to procedures approved by the Queen's University Animal Care Committee and the guidelines of the Canadian Council on Animal Care. Each monkey underwent two surgeries. In both, anesthesia was induced with ketamine hydrochloride and maintained with isoflurane. Antibiotics were administered pre- and postoperatively, and anti-inflammatories and analgesics were administered postoperatively.
In the first surgery, eye coils were implanted subconjunctivally
(Judge et al. 1980) to monitor gaze (eye-in-space)
position (Fuchs and Robinson 1966
), and a head post was
attached to the skull by way of a dental acrylic pedestal that also
held the leads and connectors. Monkeys were trained on oculomotor tasks
(see following text) prior to the second surgery. In the second
surgery, chronically indwelling EMG electrodes were implanted in neck
muscles using a similar approach to that described in cats
(Richmond et al. 1992
). Muscle layers were separated
from the dorsal midline raphe to gain access to the cleavage planes
between muscles. Up to 12 muscles in each monkey were implanted using
bipolar epimysial patch electrodes or bipolar intramuscular hook
electrodes (Table 1). Full details of the
electrode design have been described previously (Loeb and Gans
1986
). In both, the recording contacts were 3 mm long,
separated by ~3 mm and were oriented perpendicularly to the long axis
of the muscle fiber fascicles. Some muscles implanted with
intramuscular hook electrodes were shielded from the potential cross-talk of adjacent muscles by suturing Silastic sheeting to the
overlying fascia. Muscle layers were approximated with a midline closure. A ground wire consisting of a single, partially bared loop of
Teflon-coated, multistranded stainless steel was stitched to
subcutaneous fascia. The leads from all implanted electrodes were
tunneled subcutaneously to the acrylic skull pedestal and soldered to
multipin connectors. By the second or third postoperative day, all
animals appeared to be making normal head movements.
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Experimental procedures
Prior to EMG recording, the monkey was placed in a primate restraining chair designed to permit unrestrained head movements. Monkeys l and f were placed in a commercially available primate chair (Crist Instruments), modified to allow attachment of a body harness which permitted approximately ±45° of trunk rotation in the horizontal plane. Monkeys z and r were placed in a custom-made primate chair that permitted the monkeys to be tethered to the chair via a customized primate vest (Lomir Biomedical). This arrangement was more effective at preventing trunk rotation (estimated to be ±10°) without restraining the head or neck. We saw no evidence that patterns of EMG activities differed in the two chairs, but a wider range of the head positions was typically achieved when using the custom-made chair.
Spontaneous sessions were recorded in monkeys l, f, and z in which volitional head movements were generated during a variety of orienting, tracking, feeding, or expressive behaviors in a well-lit room. Experimenters in the room encouraged head movements by displaying food, verbalizing, or hand-waving; desired movements were rewarded with food and verbal praise. The animals appeared to behave normally and showed no signs of stress.
Monkeys z and r worked in trained
sessions in a dark, sound-attenuated room, performing an
oculomotor task in which they had been trained previously. Stimuli
consisted of 60 light-emitting diodes (LEDs) arranged at the front and
both sides of the monkey, spanning 90° to the right and left of
center, and 45° above and below center. To receive a liquid reward,
the monkey had to fixate the central LED for 500 ms, look to one of
eight randomly selected peripheral LEDs illuminated as the central LED
was extinguished, fixate the peripheral LED for
500 ms, look back to
the central LED illuminated as the peripheral LED was extinguished, and
fixate the central LED for
500 ms. The locations of the eight
peripheral LEDs were varied between blocks, allowing a considerable
range of head postures and centrifugal (away from midline) and
centripetal (toward midline) movements to be obtained over several days.
Data collection and analysis
A flexible ribbon-cable that did not interfere with head
movements linked the EMG connector(s) to the signal processing
electronics. The signal-processing architecture used for
monkey l was different from that used for the
other monkeys. Briefly, all EMG signals for monkey
l were amplified differentially, bandwidth filtered (100-5,000 Hz) and recorded on an FM tape recorder. Segments of interest were rectified and integrated into 3.3-ms bins and digitized at 3.3 ms (see Thomson et al. 1994 for details).
Sessions for monkey l were videotaped at 60 fields/s using two shuttered cameras placed above and to one side of
the monkey, allowing estimation of the position of the head on the body.
For monkeys f, z, and r,
digitized signals of the EMG activity and the gaze (eye-in-space) and
head (head-in-space) positions derived from the magnetic coil system
were recorded simultaneously. The coil system (CNC Engineering) yokes
the two horizontal fields together, hence the relationships between
induced current and horizontal coil position was linear over a range of
±90° from center. The search coil and a tube for the fluid reward
were secured to the head pedestal and did not interfere with normal
head movements or vision. The EMG ribbon-cable led to preamplifiers and
low-pass filters (MAX274 integrated IC filter,
fc = 8 kHz, roll-off = 24 dB/octave,
Maxim Electronics) that filtered out the coil frequencies. Data were
then fed into an Analog Preprocessor and Timer (Aztec Associates) that
enabled computer-programmable amplification, filtering (100- to
5,000-Hz bandwidth), rectifying and digitizing of the signals into 2-ms
bins. The amplification was adjusted for different channels to yield a
maximal peak-to-peak output voltage of ~5 V. The amplitudes reported
here correspond to raw EMG signals with ~10 times larger peak-to-peak
amplitudes (Bak and Loeb 1979). Bins with amplitudes
5
µV were assumed to represent noise; this value was generally used as
a limit below which the muscle was classed as silent and data points
were excluded from correlation analyses. The EMG signals and the
horizontal and vertical gaze and head position signals were digitized
at 500 Hz with a Pentium computer running a real-time data acquisition
system (REX version 5.4) (Hays et al. 1982
). The
behavioral sessions for monkeys f, z,
and r were videotaped using a single infra-red camera in conjunction with an infra-red light source, synchronized by a software-controlled trial counter placed in the camera's field of view.
Behaviors of interest from spontaneous sessions (monkeys l, f, and z) were selected by inspecting the videotaped sessions. In the trained sessions (monkeys z and r), analyses were performed only on correct trials. Segments or trials in which the monkey adopted a posture unsuitable for these experiments (i.e., head resting on neck plate or torso twisted away from the frontal plane) were not analyzed. Head velocity and acceleration traces were obtained by differentiation and double-differentiation, respectively, of position signals. The onsets and offsets of orienting head movements were determined when the head velocity crossed a 10°/s threshold. The onset and offset of translating or torsional movements were determined by examining the videotaped sequences along with the head position signals. The "zero" position to which both horizontal and vertical planes were referenced occurred when the monkey's head was pointed straight ahead without inclination or declination, such that the search coil mounted on the head, and hence the frontal plane of the head, was oriented parallel to the front panel of the coil frame.
When appropriate, the temporal aspects of the EMG signals in some
muscles were determined by quantifying the time of activation and
silencing. Although no strict quantitative criteria were used, sudden
changes in EMG activity levels were easily delineated. To quantify the
magnitude of the EMG response during stable postures, the EMG signal
was averaged over the duration of the postural segment. To quantify EMG
response magnitude during head movements, the EMG signal was first
smoothed with a 50-ms running average (i.e., ±25 ms from the point
under consideration), selected because it approximates the dynamics of
muscle-force development and reduces the variability arising from the
stochastic nature of the EMG signal (Loeb and Gans
1986). EMG response magnitude was quantified by taking the peak
of this smoothed signal over a period ranging from 75 ms before
movement onset to the time of peak head velocity to capture an estimate
of the EMG contributing to the accelerational torques required to
produce the movement. For very transient EMG signals during rapid head
movements in which this method was inappropriate (e.g., bursts in Fig.
6), the magnitude of the EMG signal was obtained by integrating the
area under the EMG curve, without smoothing.
Overall, we analyzed a total of 1,053 postural segments (110 from monkey l, 67 from monkey f, 670 from monkey z, 206 from monkey r), 2,311 movement segments (359 from monkey f, 1,811 from monkey z, 131 from monkey r), and 70 complex segments composed of multiple movement phases (i.e., head shakes, translations, feeding behaviors, etc.; 57 from monkey f, 13 from monkey z). Movement data from monkey l were not analyzed quantitatively, but movements were inspected to ensure that the EMG patterns were qualitatively similar to results from the other monkeys. For the sake of simplicity given the number of recorded muscles, analyzed data from a given muscle are presented only if that muscle served as an agonist or antagonist to the posture or movement in question.
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RESULTS |
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All monkeys held a variety of postures and generated head movements during either spontaneous (monkeys l, f, and z) or trained (monkeys z and r) sessions. It was impossible to obtain perfectly comparable records from monkey to monkey because different muscles were implanted (Table 1), but consistent patterns of neck muscle activation were observed across multiple segments and monkeys. To illustrate this point, most figures display multiple postures or movements from monkey z and one of either monkey f or r. Small differences were often seen in the activities of muscles from one sequence to the next; where appropriate, we identify idiosyncratic observations to distinguish them from the more general patterns. We present EMG patterns associated with postures and movements in the horizontal plane, postures and movements in the vertical plane, and during forward translations or vigorous head shakes.
EMG activity during postures or movements in the horizontal plane
TURNED POSTURES. All monkeys frequently held their heads in turned postures. The eccentricity of head postures analyzed here ranged up to ±70° from center for monkey z, ±60° for monkey f, ±50° for monkey r, and ±40° for monkey l. EMG activity was negligible in all recorded muscles when the head was held at the central "zero" position and when the head was turned away from the preferred direction of the muscle. Modestly turned postures <20° from center were associated with consistent activity only in the ipsilateral suboccipital muscles obliquus capitis inferior (OCI) and rectus capitis posterior major (RCP maj) (Fig. 1, A and B, 3rd and 4th columns). Larger turned postures ~20-50° from center were associated with stronger activation in the ipsilateral suboccipital muscles, and a lower level of activity in ipsilateral splenius capitis (SP cap; Fig. 1, A and B, 2nd and 5th columns). These same ipsilateral muscles were activated strongly in extreme postures >50° from center, and sternocleidomastoid (SCM) contralateral to the side of turning also became active (Fig. 1, A and B, 1st column). The EMG activity during turned postures was usually <50 µV/bin for the suboccipital muscles and <20 µV/bin for the larger muscles, although these values were exceeded at extreme postures.
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TURNING MOVEMENTS. Muscle recruitment during trained sessions. The same muscles active during turned postures (OCI, RCP maj, SP cap, and SCM) were recruited synchronously ~10-50 ms before head movements during trained gaze shifts (Fig. 3). Suboccipital muscles OCI and RCP maj were active during small turns (Fig. 3, A and C), and the larger muscles SP cap and SCM were additionally active during larger turns (Fig. 3, B and D). Occasionally, this initial activation was a phasic burst followed by lower tonic levels typical of the posture held at the end of the movement (e.g., Fig. 3, A and C); in other segments, no distinct phasic burst was apparent (Fig. 3, B and D). Antagonist muscles whose mechanical turning actions were away from the turn were essentially not recruited (Fig. 3).
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EMG activity during postures or movements in the vertical plane
VERTICAL HEAD POSTURES. All monkeys held their heads in different vertical postures, but the range of postures varied. Monkeys f, l, and r held vertical head postures ranging from 30° in inclination to 20° in declination. Monkey z held a wider range of postures from 55° in inclination to 50° in declination. The analysis of head postures in the vertical plane was more difficult than in the horizontal plane because some muscles active in vertical postures were also active in turned postures (e.g., RCP maj, SP cap, and SCM). Further, our implantation regime was not identical in all monkeys, hence we occasionally report results obtained from only one monkey.
In all four monkeys, very little activity was recorded when the head was in the central position (Fig. 10, 3rd column; the R-OCI activity in Fig. 10A is due to a small rightward turn). Complexus (COM) became increasingly active as head inclination increased, whereas biventer cervicis (BC), which lies immediately medial to COM, did not display strong tonic postural activity related to head inclination (Fig. 10A, 1st and 2nd column). Obliquus capitis superior (OCS, monkey l only) and RCP maj (Fig. 10A, monkeys z and r) were also recruited when the head was inclined modestly. Rhomboideus capitis (RH cap) was recruited with increasing head inclination in monkey f (Fig. 10B, 1st and 2nd column) but not monkey z (data not shown). SP cap (3 monkeys) and AS ant (monkey z only) also became increasingly active at progressively larger angles of inclination (Fig. 10, A and B). OCI was recruited only at extreme angles of inclination (Fig. 10A, 1st column). Maximal activation of all muscles when the head was held in an inclined posture seldom exceeded 50 µV/bin.
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HEAD MOVEMENTS IN THE VERTICAL PLANE. Muscle recruitment during trained sessions. Figure 11 shows four inclining head movements and three declining head movements generated by monkeys z and r. For larger inclining movements (Fig. 11, A and E), moderate synchronous activation in COM and BC preceded the onset of the inclining movement by ~20-40 ms. Peak activation of these muscles during inclining movements never exceeded 50 µV/bin. The activity profile consisted of an initial phasic component in both muscles, followed by a tonic component predominantly in COM typical of the posture held at the end of the movement. COM activity was bilateral in monkey r, but a similar determination could not be made for BC because the R-BC electrodes in this monkey failed. The magnitudes of the phasic components of COM and BC scaled to the size of the movement (Fig. 11, B and F). Further, EMG activity during inclining movements was limited to agonist muscles; antagonist muscles (R-SCM in Fig. 11, A and B) were not recruited.
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Feeding behaviors and head shakes
All monkeys moved their heads during eating or head shaking. The neck muscle activities during these movements attested to the larger range of highly orchestrated recruitment patterns that the monkey is capable of generating. During these movements, EMG patterns became quite specialized, and previously inactive muscles were recruited. We did not focus quantitatively on such movements because the magnetic search coil system provided calibrated measurements only for horizontal and vertical rotations, not for torsional rotations nor translational movements.
The EMG patterns shown in Fig. 16 were generated during a representative forward translation along the occipito-nasal axis, which monkey f used to crane for offered food. The unique feature of this type of movement was the strong and increasing bilateral activation in SCM (Fig. 16), which occurred without significant activity in other muscles that were typically synergistic (OCI and SP cap) or antagonistic (COM) with SCM. TRAP was also active during this movement, although compared with SCM, the activity in TRAP was more discrete and did not increase greatly during the movement. Similarly strong activity was observed in R-SCM in monkey z during craning movements, although this muscle was not implanted bilaterally.
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All monkeys spontaneously generated head-shaking sequences consisting of multiple oscillations in which the head was rapidly turned from one side to another over a period of 0.5-2 s. Head shakes were associated with the highest levels of EMG activity recorded in all muscles, regardless of whether the muscle linked the skull to the spinal column (OCI, SP cap, RCP maj, COM), the skull to the shoulder girdle (TRAP, RH cap), or the shoulder girdle to the spinal column (AS ant, AS post). Figure 17A shows a typical example consisting of seven oscillations over a period of 1 s. All muscles displayed discrete bursting profiles, and had activity levels >60-100 µV/bin. A closer examination of the temporal aspects of the EMG activity revealed that some muscles burst twice per cycle, whereas other muscles burst only once per cycle (Fig. 17, B and C). In those muscles bursting twice per cycle, the magnitude of the two bursts differed. The synergies identified for rapid turns could be discerned during head shakes, but coactivation was stronger during shakes than turns (e.g., note the bilateral activation in the OCI muscles in Fig. 17B). Strong activation in many muscles often occurred 20 ms prior to the start of the turn toward the preferred direction (i.e., R-OCI and R-SP burst before right turns; L-OCI, L-RCP maj burst before left turns: Fig. 17C), while these muscles lengthened.
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DISCUSSION |
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This report is the first detailed examination of
EMG activation in multiple monkey neck muscles during a large range of
head postures and movements. Similar studies in cats revealed that individual neck muscles, and even individual compartments within a
given neck muscle, are controlled by the CNS in specific and reproducible ways (Keshner 1994; Keshner et al.
1992
; Richmond et al. 1992
; Thomson et
al. 1994
, 1996
; Wilson et al. 1983
) but revealed
complex and somewhat counter-intuitive patterns, as discussed in the
following text. The activity from analogous muscles in monkeys is
similarly specific and reproducible but somewhat simpler to relate to
kinematics. This discussion focuses on the similarities and differences
between cats and monkeys in terms of the likely kinetics of the various
postures and movements and the comparative architecture of the muscles
as revealed in the companion paper (Richmond et al.
2001
). This approach must eventually be combined with
quantitative kinetic and biomechanical analyses of normal and perturbed
head movements, as well as single-unit recording studies in the brain
stem, to understand fully the underlying neuromuscular control.
Methodological considerations
To study head movements systematically, we examined head movements generated during trained gaze shifts since these are measured easily and reproduced consistently. However, had we only studied trained head movements, we would not have observed the wealth of variation in EMG activation that accompanied spontaneous head movements. For example, craning movements were associated with coactivation of the two SCM muscles (Fig. 16), which are antagonists during head turns. Head shakes were associated with very high levels of activity in all muscles, apparently phased to contribute to the high accelerations observed during such rapid movements (Fig. 17). General features of these movements were observed by comparing repeated sequences generated over the course of weeks. If future studies are concerned with the neuromuscular strategies underlying such movements, clever ways will have to be devised to elicit many such movements reproducibly.
In this study, we recorded only horizontal and vertical head rotations and not the remaining 4 degrees of freedom (df; torsional rotation and 3 directions of translation). Qualitatively, we observed motion in all 6 df during the natural repertoire of head movements. Translating movements were frequently generated when the monkeys craned for food or tried to visualize objects partially obstructed by barriers. Torsional rotations of varying magnitudes were generated during orienting movements and feeding behaviors but were generally excluded from analysis. Other methodologies, such as three-dimensional coil systems and analysis of reflective and fluoroscopic markers, would be better suited to quantifying such motion and estimating the kinetic implications to better understand the specialization of neck muscle control for these tasks.
Postures and synergies
To hold its head in the central position, the chair-restrained monkey requires little or no muscle activity (Fig. 10), probably because the head is aligned vertically on top of the cervical and thoracic vertebrae so that the weight of the head is borne by compression of underlying vertebrae. Deviations from this "metastable" position required increased levels of muscle activity to balance the head. Interestingly, both statically inclined and declined postures were associated with flexor and extensor muscle activity that was variable but sometimes included some co-contraction of antagonist muscles (Fig. 10).
To hold its head in progressively more turned postures, the monkey was
observed to recruit progressively all of the muscles that tended to
pull the head into such turned postures. Suboccipital muscles such as
OCI and RCP maj were active for even the smallest deviations from
center to which activity in multiarticular head turners such as SP cap
and SCM was added for more turned postures. Similar trends have been
reported previously (Bizzi et al. 1971; Lestienne
et al. 1995
, 2000
) and have been suggested to reflect underlying kinematics: small turns are thought to be executed by
rotations at suboccipital joints whereas larger turns require additional rotations about lower cervical vertebrae (Kapandji 1974
). Furthermore, some muscles (e.g., RCP maj, SP cap, and
SCM) are also involved in postures and pure movements in the vertical axes. This observation is interesting considering that horizontal and
vertical components of head movements appear to be controlled by
separate brain stem structures downstream of the superior colliculus (owls: Masino and Knudsen 1990
; cats: Grantyn and
Berthoz 1987
; Isa and Naito 1994
, 1995
;
Sasaki et al. 1999
; monkeys: Cowie and Robinson
1994
).
The postural activity of some monkey neck muscles was different
from that reported for homologous cat muscles (Akaike et al. 1989; Guitton and Mandl 1978
; Keshner et
al. 1992
; Richmond et al. 1992
; Roucoux
et al. 1980
, 1989
; Thomson et al. 1994
, 1996
). The differences may be related to the posture of the cervicothoracic joints, which some of these muscles cross. Studies in cats are usually
conducted with the trunk oriented horizontally and the cervicothoracic
column in an S-shaped configuration, whereas studies in chaired monkeys
are conducted with the trunk and cervical column oriented more
vertically. In cats, BC is active tonically over most of the range of
inclined and declined midline head positions, including the central
position; in monkeys BC had little activity during tonic postures (Fig.
10). However, BC has been found to become active when monkeys hold
their heads in neutral postures during quadrupedal stance when the
cervicothoracic region is held in a more S-shaped posture like that in
which cats were studied (E. Keshner and B. Peterson, unpublished
observations). Further, large horizontal turns in cats are associated
with paradoxical activity in the contralateral COM muscle; in chaired
monkeys, COM was active only when it could contribute positive work in inclination or during oblique turns. In the monkey, the long cervical muscles that contribute to large horizontal turns may impose mostly compression forces in addition to the axial rotation of the vertical cervical column; in the cat these muscles presumably produce complex torsional forces along the S-shaped cervical column that may require some degree of cocontraction for stabilization. The preferential recruitment of extensors contralateral to oblique turns may serve to
counteract small torsional rotations (Fig. 15).
When rhesus monkeys move in their natural environment, they do so with
weight borne on all four limbs. They have been classified as
terrestrial quadrupeds, although they can resort to facultative bipedalism when it is useful (e.g., carrying food) (Napier and Napier 1967, 1985
). At rest, they typically adopt a squatting body posture that frees their hands for tasks such as feeding and
grooming. The presence of the squatting posture and facultative bipedalism has led some to regard monkeys as bipeds to differentiate monkeys from obligatory quadrupeds like rodents and cats (Graf et al. 1995
; Vidal et al. 1986
). Both the use
and anatomy of the monkey head-neck-scapular system are distinct from
cats and humans. Compared to cats, monkeys do not use the head as the
primary prehensile organ, they have a more modest dorsal neck muscle
mass, and they have a scapula attached mechanically to the trunk via
the clavicle. Compared to humans, the orientation of the primate
scapula is more parasagittal than frontal, and monkeys retain
musculature apparently unique to quadrupeds (e.g., RH cap and somewhat
separate BC and COM) (Richmond et al. 1999a
). These
observations do not preclude monkeys as animal models for human head
movements, but caution extrapolating results across species.
Because rhesus monkeys are neither obligatory quadrupeds nor bipeds,
legitimate concerns may be raised regarding the squatting posture
imposed by our primate chairs. Although we could not measure the
orientation of the cervical column directly, a previous study using
X-ray photography confirmed that similar craniocervical postures were
obtained during squatting in chair-restrained and unrestrained monkeys
(Vidal et al. 1986). We reiterate that the activation
patterns observed in chair-restrained, squatting monkeys will likely
change when monkeys adopt a quadrupedal posture; biomechanical differences between the two postures are likely reflected in distinct uses of at least some of the muscles of the head-neck-scapular complex,
particularly those spanning the cervicothoracic junction.
Movements and kinetics
The head movements generated during trained gaze shifts followed simple scaling rules for amplitude, velocity, and acceleration in both the horizontal and vertical axes. Muscle recruitment during these movements appeared to be associated both qualitatively and quantitatively with the presumed kinetic requirements of the movements. The kinetics reflect a mixture of elastic, viscous and inertial force requirements related to position, velocity, and acceleration, respectively, but the covariance of these variables during trained movements makes it difficult to use such data to test hypotheses about neuromuscular strategies. Spontaneous movements exhibited a wider range of kinematic patterns that make it possible to consider the kinetic strategies. This reinforced the notion that neck muscle activation in chaired monkeys is relatively simple to relate to the mechanics and kinetics of head movement.
VARIATIONS IN MOVEMENT DYNAMICS.
Head movements during trained gaze shifts were associated with phasic
and tonic patterns of recruitment in agonist muscles consistent with
overcoming elastic and viscous forces (Figs. 3 and 11). Very rapid
movements of the same amplitude were associated with large reciprocal
phasic bursts in agonist and antagonist muscles consistent with the
requirements of accelerating and decelerating an inertial mass (Figs.
6, 7, 13, and 14). Triphasic patterns of recruitment have been
described for rapid arm movements (Hallett et al. 1975;
Lestienne 1979
; Marsden et al. 1983
), and
for SCM and SP cap during head movements in humans (Zangemeister
et al. 1982
). The activation of antagonistic muscles in humans
may be a consequence of instructing fast movements. Our results suggest that antagonist muscle activation may be more the exception than the
rule, particularly in trained tasks with no premium on either speed or accuracy.
CENTRIFUGAL VERSUS CENTRIPETAL MOVEMENTS. Comparisons of centrifugal and centripetal turning movements matched for size and speed revealed that the initial position of the head affected muscle recruitment. The first event preceding centripetal turns was the silencing of previously active contralateral muscles (Figs. 8 and 9). In addition to releasing stored elastic energy to assist in initiating the turn, the silencing of contralateral muscles may also avoid the high forces that would be required to stretch active muscles: had the silencing of contralateral muscles coincided with the activation of ipsilateral muscles, remnant forces produced by lengthening the contralateral musculature would have resisted the developing turning forces.
The synergy for centripetal but not centrifugal turns was found to include AS ant, which spans from the lateral half of the scapula to the transverse process of C1. The biomechanical implications of this activity are not clear, but the temporal ordering of recruitment suggests that forces developed by AS ant play a role in the early acceleration of centripetal turns. The involvement of AS ant in centripetal turns is surprising considering this muscle, at least in humans, is viewed commonly as being involved in scapular elevation rather than head turns (Bull et al. 1984Muscle architecture
Some differences in muscle function between cats and monkeys may
relate to differences in the architecture of individual muscles in
addition to the postural differences noted in the preceding text. For
example, RCP maj in the cat is almost a pure head extensor. In monkey,
its skull insertion is distributed more laterally (Richmond et
al. 2001), contributing a turning moment that is reflected in
its recruitment during horizontal postures and turns. The gradual loss
of distinctive muscle functions that seems to be associated with the
tendency to hold the neck and torso in a vertical orientation may be a
driving force for the simplification of the primate neck musculature
with evolution. For example, COM and BC in the cat are anatomically and
functionally distinct (Richmond et al. 1992
). In the
monkey, COM functions somewhat similarly to BC and often merges
anatomically with the anterolateral edge of BC (Richmond et al.
2001
). In humans, both muscles appear to have been subsumed into the single muscle semispinalis capitis (Kamibayashi and
Richmond 1998
).
Cat neck muscles tend to be much more specialized in their
distributions of muscle fiber types than monkey muscles. In the cat,
neck muscles range from 10 to 65% Type 1 (slow-twitch)
(Richmond and Vidal 1988; Richmond et al.
1999b
; Selbie et al. 1993
) while the same
muscles in monkeys range from 23 to 45% (Richmond et al.
2001
). The recruitment of some cat muscles appears to be
specialized for tonic postures versus dynamic movements (Thomson
et al. 1994
, 1996
). In the monkey, the neutral head position
requires little tonic muscle activity; recruitment during other
postures and movements seems related more closely to simple force
requirements inferred from the kinematics of the behavior.
Conclusions
The complementary approaches used in this and the companion paper
(Richmond et al. 2001) further the understanding of the morphometric, biochemical and physiological organization of monkey neck
muscles. Such understanding is important for the development of
realistic biomechanical models of head control in monkeys and for
future neurophysiological studies on head movement control. Further,
this paper emphasizes that monkey neck EMG, at least in the squatting
posture, relates relatively simply to the kinematics and presumed
kinetics of the movement. This result is heartening for understanding
human head-movement control, where most deep neck muscles are
inaccessible. However, the central neuromuscular strategies for human
head movement cannot simply be assumed from the musculoskeletal
architecture. For example, simple "lines of force" logic would not
have predicted the sequential activation of muscles during centripetal
turns. Although tempered with the knowledge of the differences between
humans and monkeys, the study of neck EMG in a squatting monkey at
least enables considerations of neuromuscular strategies and cervical
biomechanics in a species inclined to adopt a human-like posture.
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ACKNOWLEDGMENTS |
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We thank D. Hamburger, A. Lablans, K. Moore, and C. Wellstood for excellent technical assistance and A. Bell and Y. Uchiyama for help in collecting portions of the data. D. P. Munoz is a Medical Research Council (MRC) scientist and a fellow of the EJLB Foundation.
This work was supported by a group grant from the MRC of Canada. B. D. Corneil was supported by an Ontario Graduate Scholarship and a doctoral award from the MRC. E. Olivier was supported by a short-term fellowship from the Human Frontier Science Program.
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FOOTNOTES |
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Present address and address for reprint requests: B. D. Corneil, Div. of Biology, California Institute of Technology, MC 216-76, Pasadena, CA 91125 (E-mail: brian{at}vis.caltech.edu).
Received 4 December 2000; accepted in final form 5 July 2001.
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REFERENCES |
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