head-neck motor system, the simultaneous activation ... Key words: Neck muscles - Head stabilization - ..... described for these muscles in standard anatomy.
Exp.erimental BrainResearch
Exp Brain Res (1989) 75:335-344
9 Springer-Verlag 1989
Neck muscle activation patterns in humans during isometric head stabilization E.A. Keshner 1'2, D. Campbell 1, R.T. Katz 3, and B.W. Peterson 1'2 aSensory-Motor Performance Program, Rehabilitation Institute of Chicago, 2Department of Physiology and 3Department of Rehabilitation Medicine, Northwestern University Medical School, 303 East Chicago Avenue, Chicago, IL 60611, USA
Summary. A musculoskeletal system with more muscles than there are motions could be programmed in alternative ways to produce a single movement. In this case, the muscles would have the potential to be maximally responsive in multiple directions rather than responding preferentially in a single direction. To determine the response patterns of muscles in the head-neck motor system, the simultaneous activation of four of the 23 neck muscles acting on the head was recorded with both surface and intramuscular electrodes. Fifteen human subjects were tested during an isometric head stabilization task. When the EMG response patterns were plotted, each muscle demonstrated a preferred direction of activation. This preferred activation direction was consistent in all of the subjects for three of the muscles tested. The fourth muscle, splenius, was preferentially activated during neck flexion in half of the subjects and during neck extension in the other half. Increasing the force parameters of the task suggested a linear relationship between force and the EMG output in the preferred response directions. Responses in the nonpreferred directions were produced by a nonlinear change in EMG activation of the muscle. This finding could have implications for theories of how reciprocal activation and cocontraction patterns of response are elicited. Results from this study, that the CNS programs neck muscles to respond in specific orientations rather than generating an infinite variety of muscle patterns, are in agreement with our findings in the cat.
Key words: Neck muscles - Head stabilization Polar plots - Electromyography - Activation patterns
Offprint requests to: E.A. Keshner (address see above)
Introduction The head-neck motor system is a highly complex musculoskeletal linkage composed of multiple joints, and more muscles than there are degrees of freedom of head motion. Although the head represents only 7% of the body's total weight (Gowitzke and Milner 1980), 23 different muscles directly link the skull on either side of midline to the vertebral skeleton (Sherk and Parke 1983). The multiple muscle attachments might not be so surprising if the head were involved in the fine motor control and variety of motions found in the hand and fingers. Motions of the head relative to the trunk, however, are primarily directed toward orienting and stabilizing the position of the eyes and head in space (Outerbridge and Melvill Jones 1971; Goldberg and Peterson 1986), even during the fine motor activities such as eating and scanning the environment. When you consider that a recent fluoroscopic study of free head movements in several animals, including monkeys, cats, and rabbits, suggested that only a small number of the available degrees of freedom in the cervical column are used for lowering or raising the head (Vidal et al. 1986), the quantity of muscles available for controlling the head seems even more extraneous. It is theoretically possible that individual head movements are produced by a variety of muscle patterns, thus requiring many muscles to satisfy all the possible combinations. In that case, the central nervous system (CNS) could then choose from a number of possible combinations to produce the desired outcome (Crowninshield and Brand 1981). It has been seen in both decerebrate and alert cats, however, that for any particular task, the maximal excitation of each neck muscle is related to a specific direction of motion. In fact, each voluntary and reflex head movement in the cat was produced by an
336
identifiable and repeatable pattern of neck muscle activation during orienting and stabilizing behaviors (Baker et al. 1985; Keshner and Peterson 1988). Movements generated in a particular direction by the voluntary motor system used different muscle patterns than the same movements generated by the neck reflexes. Correspondingly, the maximal response of individual muscles occurred at different orientations for the two tasks. This would imply that each head motion task is executed by a specific muscular pattern that is not repeated in any other direction. Concomitant studies in humans have been impeded by the methodology required to isolate individual neck muscle responses. In the above studies, as well as in previous studies on the human neck (Vitti et al. 1973; Takebe et al. 1974), experimenters have mostly relied upon the implantation of fine wire electrodes, believed to be the only method that could distinguish between the overlapping neck muscles. There is reluctance on the part of human subjects, however, to undergo invasive procedures with needle or wire electrodes, and these studies have only been able to measure the response of one muscle at any given time. Measurement of a single muscle during any given head movement limits the conclusions than can be drawn concerning the programming of synergistic patterns of action. For example, Zangemeister et al. (1982) recorded from two pairs of neck muscles with surface electrodes during ballistic head rotations, and found that initial head position strongly influenced their results on the functional interaction of the two muscles. Apparently, delineation of the combined activation patterns of the muscles during each controlled head movement is necessary to reveal how the CNS programs this complex motor system. The purpose of this study was to measure the concurrent responses of several of the muscles acting on the head during any single direction of motion in order to explore: 1) whether the neck muscles demonstrate preferential responses to specific directions of motion, and 2) whether the directional parameters of a movement are the determinant factors in choosing a central program for neck muscle responses. To this end, we simultaneously recorded the activation of four neck muscles using surface electrodes during an isometric head stabilization task. Since the use of surface electrodes will always leave open to question the actual muscle groups recorded, we have verified the actual muscle and its response pattern with bipolar needle electrodes in a small group of subjects. Robustness of the directional response properties was also measured by altering the force parameters in the head stabilization task.
Methods Fifteen subjects (ages 22-44) of either sex who had no history of neck injury or neurological deficit participated in this study. Three of those subjects gave informed consent to be tested in the same paradigm with bipolar needle electrodes to verify the surface electrode placements and resultant electromyographic (EMG) activation patterns of each muscle. Only muscles of the neck that acted directly on the head, and that could be palpated superficially were selected for study (see Daniels and Worthingham (1972) and Kapandji (1974) for descriptions of the origins and insertions of each muscle).
Procedures Subjects wore a motorcycle helmet that was tightly fitted to the head. A 360~ universal joint was attached to the top of the helmet approximately over the center of the subject's head. A cord was connected to this joint, and extended over a low friction pulley placed 80 cm away from the subject. This pulley arrangement could be moved in a 180~ circumference around the subject. Subjects sat facing the pulley for four trials, and then were turned 180~ so that the pulley arrangement was behind the subject. The pulley position was shifted by 22~ or 45~ on each trial so that frontal plane measures were taken in either eight or 16 different directions. A weight was suspended from the other end of the cord in order to supply a force against which the subject could stabilize the head. For the purposes of this study, orientations refer to the action of the subject's head, which was opposite to the direction of the applied force. Thus, according to our conventions, zero degrees (0~ represented a head stabilizing action in pitch extension. 180~ was head stabilization in pitch flexion. Right lateral flexion (right roll) of the head was positive (+)90 ~, and left roll was negative (-)90 ~. Yaw (right and left lateral rotation) was produced by arranging two weight and pulley systems so that one pulled forward on a hook on one side of the helmet, while the other pulled backward on a hook on the other side. An angular torque was thereby placed on the helmet, against which the subject's head was stabilized.
Surface electrode recordings. Pairs of Ag-Ag CI electrodes, 4 mm in diameter and spaced 1 cm apart, were placed over four muscles on the right side. Potential surface electrode placements were determined through an anatomical analysis of the neck muscles in cadavers, and manual palpation of each subject. Sternocleidomastoid (SCM) is a flexor and lateral rotator of the head. It is easily palpated when the subject pushes, against resistance to the chin, in a lateral direction contralateral to that of the muscle. Electrodes were placed over the muscle belly, approximately one third of its length rostral to its sternal attachment. Trapezius (TRAP) is classically described as a scapular muscle, and is easily palpated by asking the subject to elevate the shoulder against resistance. TRAP might also participate in head extension since the superior fibers of that muscle originate on the external occipital protuberance (Lockhart et al. 1972), although anatomical examination reveals that the muscle fibers become very sparse and essentially disappear around the level of the fourth cervical vertebrae. Electrodes were placed over the palpated muscle belly about the level of C6-C7 and dorsal to its insertion on the lateral third of the clavicle. Splenius capitis (SPL) acts as an extensor and lateral flexor of the head. Almost all of SPL lies underneath the TRAP and SCM muscles, except for a rectangular area on the lateral portion of the neck where SPL is the most superficial muscle (see Lockhart et al. (1972), Fig. 276). This muscle can be palpated between the SCM
337 and TRAP when resistive head extension and lateral rotation are performed in the same direction as the muscle. Electrode placements for the SPL muscle were determined by measuring 6 cm rostral to the bony prominence at C7 (approximately the C4 level), 6--8 cm lateral, and palpating for the muscle belly. Finally, semispinalis capitis (SEMI) is a head extensor muscle that participates minimally during ipsilateral lateral flexion. Anatomical examination reveals that most of SEMI lies close to midline and can be palpated by resisting head extension. The muscle is covered by either SPL or TRAP except for a small area extending from its insertion to about the level of the second cervical vertebrae. Electrodes were placed 2 cm below the occipital bone at approximately C1-C2, and 2 cm lateral to midline over the palpated muscle belly. The amount of force applied to each subject was chosen by observing the muscle activity in the +90 ~ direction on an oscilloscope, while gradually incrementing the weight until all four muscles responded. The next lower weight was then selected for the experiment (all of our subjects were given from three to five pounds (1.4 to 2.3 kg). In this way we were able to elicit reciprocal activation rather than cocontraction responses during stabilization. Subjects sat comfortably, and were asked to look straight ahead and to keep the head still. Visual feedback was supplied to assist the subject in maintaining a stable head position. As seen by the strain gauge output (lower trace of Fig. 1A), force was slowly applied to the head and maintained for a ten second period, three times on each trial, and then removed for twenty seconds. There was a three to four minute rest period between each trial while the pulley position was shifted. Linearity of the EMG response in relation to the applied force was tested on three of the subjects. Surface electrode recordings were taken in the four primary directions: pitch extension (0~ roll right (90~ pitch flexion (180~ and roll left (-90 ~) using weights of two, four, six, and eight pounds (0.9, 1.8, 2.7, and 3.6 kg, respectively). The procedure for applying the weights and recording the data was the same as the other surface EMG recordings.
Intramuscular recordings. Three of the subjects were also tested with a single bipolar needle electrode (EMG Associates, Conn.). Unlike the surface recordings, only one muscle was tested at a time. The intramuscular electrode was inserted into the muscle at the same anatomical location as the surface electrode placements for the SEMI and SPL muscles. For the TRAP muscle, the electrode was inserted closer to midline, but at the same cervical levels, to be certain of recording from the upper fibers of trapezius. Since SCM is a large superficial muscle that is easily isolated, we did not believe that it was necessary to record from the SCM with the needle electrode. For each muscle tested with the bipolar needle electrode, the weight was applied once per trial at every 45~interval in the frontal plane. The direction that elicited maximal EMG activity was repeated between every other direction in order to insure that the electrode position had not shifted. Yaw was tested once in each direction. The experimenter's hands were placed on either side of the helmet, and the subjects turned their heads to the right and left against the resistance exerted by the experimenter.
Data analysis Surface EMG potentials of the four neck muscles were amplified, bandpass filtered (10-200 Hz), full-wave rectified, and integrated (1 s time constant) before the data were digitized at 10 Hz on a PDP11 computer system for later analysis. A strain gauge signal was also collected, indicating when the force produced by the weight was actually applied to the head. EMG amplitude was measured from the response to the weight when fully applied, and
not during the period of application and removal (see Fig. 1A). Magnitude of EMG activation was obtained for each direction by subtracting the baseline activity level from the average amplitudes of the three response peaks in each trial. The maximum EMG response of each muscle (excluding the response in yaw) was identified for the subject, and then responses elicited in each direction of applied force were expressed as a percentage of this maximum. Responses normalized in this way were plotted on polar plots to determine the directional response properties of each muscle. Means and standard deviations of the percent maximum response for the entire group of subjects were calculated and also plotted on polar plots to determine consistency of response patterns within the group. Bipolar needle electrode recordings were amplified and filtered (50-500 Hz) prior to storing EMG and strain gauge output in analog form on magnetic tape. EMG spike potentials were then passed through a window discriminator which issued a pulse whenever an action potential traversed two windows set to accept any spikes that fired above the voltage level of background noise and any undifferentiated tonic background muscle activity. Even with this wide window of acceptance, no more than three motor units were sampled by the intramuscular electrodes in any direction of head stabilization. These pulses were stored in digital form with a 0.1 ms resolution on a P D P l l computer system for later analysis. Rate of motor unit firing was counted over a 3 s period, beginning 2 s after the weight was suspended. Calculated EMG spike rate in each direction of applied force was then plotted on a polar plot for comparison with surface EMG recordings.
Results
Directional preferences of the neck muscles F i g u r e 1 is a t y p i c a l p i c t u r e o f o n e s u b j e c t ' s E M G r e s p o n s e p a t t e r n in 16 f r o n t a l p l a n e s a n d t w o y a w directions. All of the muscles produced some tonic a c t i v i t y in t h e r e s t i n g s t a t e , a n d E M G a c t i v i t y g r a d u ally i n c r e a s e d as t h e r e s p o n s e d i r e c t i o n m o v e d c l o s e r to t h e p r e f e r r e d d i r e c t i o n o f t h a t m u s c l e . T h e n t h e r e was a d e c r e a s e o f t h e r e s p o n s e , a n d a n a r e a o f n u l l r e s p o n s e in t h a t m u s c l e . S u b j e c t s w e r e i n f o r m e d as to w h e r e a n d w h e n t h e f o r c e w a s to b e a p p l i e d t o t h e h e a d . It is p o s s i b l e t h a t t h e o b s e r v e d d i r e c t i o n a l selectivity was a result of the subject's expectation of p e r t u r b a t i o n to t h e h e a d , r a t h e r t h a n a d i r e c t i o n a l l y s e l e c t i v e r e s p o n s e to d e s t a b i l i z a t i o n . I f i n c r e a s i n g E M G a c t i v i t y in a m u s c l e w a s t h e r e s u l t o f p r e d i c t i v e mechanisms, then a corresponding EMG increase s h o u l d a p p e a r in t h e l e v e l o f b a s e l i n e t o n i c activity. T h e r e w a s i n d e e d a s i g n i f i c a n t i n c r e a s e in t o n i c a c t i v a t i o n o f all b u t t h e T R A P m u s c l e as a r e s u l t o f d i r e c t i o n ( S C M : t ( 1 0 ) = 3.29, p < 0 . 0 1 ; S E M I : t(10) = 3.52, p < 0.005; S P L : t ( 1 0 ) = 2.30, p < 0.05), s u g g e s t i n g a p r e d i c t i v e c o m p o n e n t in t h e r e s p o n s e p r i o r to t h e a p p l i c a t i o n o f f o r c e . C o r r e l a t i o n s b e t w e e n t h e c h a n g e in t o n i c a c t i v a t i o n a n d t h e m e a n E M G r e s p o n s e f o l l o w i n g f o r c e a p p l i c a t i o n in each frontal plane orientation were then tested. Coefficients of variation, generated by a linear
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Fig. 1A-C. E M G response of the right SCM muscle in one subject for sixteen directions of force application in the frontal plane, and two directions of yaw rotation. A Data collected from one trial demonstrates coordination of strain gauge output (lower trace) and E M G output (upper trace). The downward deflection of the strain gauge indicates application of force to the head. B The three E M G responses of each trial were overlapped in the rest of the figure to show the consistency of E M G activation for each head orientation. In the frontal plane, the direction of pull is opposite to the direction required for head stabilization. Thus 0~ is pure head extension, 90 ~ is right roll, 180 ~ is head flexion, -90 ~ is left roll. Note that the input signal to the rectifier was switched off at beginning of trace, and then on at approximately 10 s to reveal background activity level. Abscissa indicates time in s; each tick mark equals 12.5 s. Ordinate represents amplitude of rectified EMG; each tick mark equals 3 kg. C Left indicates head turning (yaw) to the left; right is yaw to the right
339 regression and significant at the 0.01 level, indicated that variations in E M G output in each direction were not fully explained by the variance in baseline activity (SCM: r 2 = 0.02; SEMI: r 2 = 0.13; SPL: r 2 = 0.42), thus implying that E M G responses were not altered simply as a result of preparation for head stabilization. As seen in Fig. 1B, SCM produced its maximum E M G response as the subject responded to a force that was pulling the head to the left and towards extension, so that the subject had to produce a right lateral rotation and flexion response (157 ~ direction). There was a gradual buildup of activity extending from 45 ~ to 180 ~. The muscle response then rapidly diminished, and a null response was produced from -112 ~ to 22 ~ All SCM muscles exhibited some responsiveness in both directions of yaw, however, a significantly larger response appeared in one direction (yaw left) as compared to the other (Fig. 1C). The other muscles exhibited the same tendency of response in both directions of yaw, but with a preferentially larger response in one of the two directions. In Fig. 2, the mean percentage of maximum activation across all of the subjects plus and minus one standard deviation is plotted on a polar plot for each muscle. The filled area on the plot clearly demonstrates the variability present in the preferred directions of activation and the directions of null response for each muscle. Thus, the right SEMI was equally activated in pitch extension and in the direction falling halfway between pure extension and pure rightward roll (45~ SCM was equally maximally responsive in the directions from pitch flexion to roll (90 ~ to 180~ T R A P was the least activated muscle for head stabilization. As seen in the figure, this muscle also had the greatest scatter and a larger area of variation in its preferred response. When T R A P did respond, its maximal E M G activity occurred between rightward roll with extension and pure roll (45 ~ to 90~ Actually, the T R A P surface and intramuscular E M G responses were largest when the subject was asked to perform isolated movements of the shoulder joint (horizontal adduction of the arm or shoulder elevation). It is our impression that the T R A P was actually performing scapular depression in order to stabilize the scapula during head movements rather than acting directly on the head. Finally, SPL exhibited a stronger rightward roll response with a surprising split preference between flexion with roll in eight of the subjects (135 ~) and extension with roll in the other seven subjects (45~ It might be supposed that we were actually recording from SCM in the subjects that exhibited a preference toward rotation with flexion in SPL.
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Fig. 2. Mean percent of maximum EMG activationplus and minus one standard deviation (shaded area) for the group was plotted as a polar plot in the frontal plane for each muscle. The bold lines surrounding the shaded area indicate the boundary of EMG activation plus one standard deviation (line closer to circumference) and less one standard deviation (line closer to axis). A narrow shaded area indicates less variability among the subjects. Head orientations are the same as described in Fig. 1. Note the dual preference of SPL in this figure, and the diffuse and variable response of TRAP when pure head movements are required
Excitation behavior in the SPL muscle was verified through bipolar intramuscular electrode recordings where care was taken to record from the most superficial muscle fibers in the region where SPL lies in the surface muscle layer. Figure 3 presents the raw E M G output of the SPL muscle for two subjects at every 45 ~ in the frontal plane and in the two yaw directions. Maximal spike activity can be seen alternately in the bottom trace at 90 ~ and 45 ~ (roll with extension), and for the top trace at 135 ~ (roll with flexion) and 90 ~. Maximal activation in yaw also differed in these two subjects. The subject in the bottom trace exhibited a preferential activation when turning to the right, and the subject in the top trace when turning to the left. These observed directional preferences in yaw were consistent for the group. Those subjects that produced greater SPL E M G activity in roll with extension also produced greater activity when turning to the right; subjects with greater E M G activation of SPL in roll with flexion also demonstrated greater activation when turning to the left. In all other directions of head stabilization, the E M G output of SPL reflected the activation patterns demonstrated by the whole group in Fig. 2.
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A test of the reliability of the surface electrode placements and for the presence of crosstalk between the surface electrodes was accomplished by plotting the intramuscular EMG output as a polar plot for each muscle and comparing it to the polar plots of the surface electrode recordings for the same subject. General conclusions about the preferred directions of activation for each muscle were supported by intramuscular recordings. SEMI and SPL exhibited very similar spatial preferences with the two techniques, with minor differences that probably reflected the more precise sampling of motor units with bipolar intramuscular electrodes. For the subject portrayed in Fig. 4, intramuscular recording from SEMI yielded a broader spatial pattern, with stronger electrical activity in directions where SEMI was weakly activated when recorded with surface EMG electrodes. SEMI activation was observed on intramuscular recordings to be in all directions involving head extension and right lateral rotation. There was also a stronger response in extension with a left rotation component @45~ In contrast, SPL had a narrower spatial pattern with intramuscular recording in this subject. SPL was more specifically
Fig. 3A, B. Raw spike data from bipolar needle electrode recordings of SPL is presented for two subjects (upper and lower EMG trace, respectively) in the frontal (A) and yaw (B) planes. A Directions and EMG activity are placed in the orientation of the weight, and opposite the direction of muscle action. Thus at 0~ the weight was placed in front of the face, and the subject produced a pure head extension response with a small response of SPL in subject two (lower trace), and no response in subject one (upper trace). 90~was right roll, 180~ was head flexion, and -90 ~ was left roll. B EMG traces from the two subjects are in the same position (upper or lower trace) as in A. The EMG response is placed in the direction that the illustrated head turns. Thus, subject one has a larger response in left yaw, and subject two responds more to right yaw. Axes in lower right of both A and B equal 100 ms (x-axis) and 1 mV (y-axis)
active in right lateral rotation with extension, rather than in pure roll. Intramuscular responses of TRAP differed from the diffuse pattern picked up with surface electrodes for the group (see Fig. 2). In this subject, the TRAP muscle demonstrated its best activation in the diagonal plane directions that incorporate lateral rotation with head flexion (135 ~ and -135 ~ or extension (-45~ TRAP in the other subject tested with intramuscular electrodes demonstrated activation only in the -45 ~ direction. The greater participation of TRAP in combined planes of action again suggests that this muscle responded best when attempting to stabilize the scapula against movements of the head instead of directly producing those head movements.
Relationship between EMG activation and force To test the linearity of the relationship between the muscle response and the applied force, we tested three of our subjects with four different weights in four directions of head stabilization. We expected that a simple linear increase in muscular effort would
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result from a linear addition of force to the stimulus. The EMG amplitudes of each neck muscle in two subjects are plotted for each direction and weight in Fig. 5. Values of EMG response were normalized so that, for each subject, the largest EMG response of the muscle was given a value of one. With a linear increase of stimulus force in the preferred directions, EMG activation of the muscles steadily increased in a linear fashion. Although response magnitude was often altered in directions that previously exhibited a null response (e.g. SEMI and SPL at -90 ~ and to a lesser extent, SCM at -90~ this was not a linear change. Nonlinear changes in the EMG response were accomplished in a variety of ways by the three subjects. In the first subject portrayed in Fig. 5 ($1), EMG responses of the neck muscles either remained silent in the directions in which they previously did not participate (e.g. SCM) or, with an increase in the applied force, suddenly jumped from a null response to a very strong EMG response (e.g., SEMI and SPL). This nonlinear increment occurred in the muscle as the force to be resisted increased from 6 to 8 pounds. In the second subject ($2), nonlinear changes in the EMG response occurred as the weight increased from 4 to 6 pounds, and again from 6 to 8 pounds (e.g., 0~ and -90 ~ in SCM). In this subject, EMG activation decreased after the non-linear increase, so that the muscle becoming activated in its nonpreferred direction suddenly dropped out of the response pattern. The
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Fig. 5. Muscle EMG responses of two subjects ($1 and $2) in four directions of head stabilization when weights were 180 incremented at 2, 4, 6, and 8 lbs. Names at the top of the 90 figure identify the muscle in each column. Numbers to the right of each line indicate the orientation of the imposed force. Amplitude of muscle electrical activity has been nor0 malized for each subject so that -90 the largest response in the four orientations was given a value , of one 8 8
342 third subject presented the same direction of activation as the first subject, but with smaller increases in EMG amplitude in the nonpreferred directions. This subject was a large man, who was able to perform the original stabilization task with a five pound weight as opposed to three pounds for the other two subjects. It is probable that nonlinear increments of the muscles would be more evident in this subject if the weight had been increased beyond the eight pound limit. A statistical test for linearity (Edwards 1968) on the mean EMG amplitude of each muscle for all of the subjects supported the observation of linearity in preferred response orientations. This test examines whether the treatment sums (i.e., EMG amplitude) are functionally related to the different values of the treatment variable (i.e., weight) by determining the fit of a first, second, and third order polynomial to the trend of the treatment sums. As expected from Fig. 5, SEMI was significantly linear (p < 0.05) in the two directions of preferred response: 0~ (F(1,9) = 7.9) and 90~ (F(1,9)= 6.9). Changes in amplitude with changes in weight appeared approximately as a constant additive function in the two subjects. The test for linearity was not significant in the other two directions. SPL exhibited significantly linear responses (p < 0.05) at both 0~ (F(1,9) = 5.7) and 180~ (/7(1,9) = 7.7), as well as at 90~ (F(1,9) = 8.2). Linearity in both the flexion and extension directions reflects the dual spatial preferences of this muscle (the third subject responded to neck rotation with extension, and the other subjects to neck rotation with flexion). SPL linearity was not significant at -90 ~ SCM exhibited significant linearity (p < 0.05) in 90~ (F1,9)= 7.1) and 180~ (F(1,9) = 7.6), its two preferred directions. SCM was also significantly linear in -90 ~ (F(1,9 = 6.7), but the very low EMG amplitudes (see Fig. 5) suggest poor participation of this muscle when stabilizing the head in this orientation. SCM was not significantly linear at 0~ an orientation that elicited no response of this muscle. Hence, with increasing torques to the head, we see a nonlinear coactivation in the off directions for SEMI and SPL, but not in SCM. Although SCM was not strongly activated in its nonpreferred directions, there are neck flexors lying in the deeper muscle layers (e.g., scaleni and longus capitis) that might be coactivated in these orientations.
Discussion
Our findings support the hypothesis of well defined directions of best activation for an individual muscle
(Zangemeister et al. 1982; Baker et al. 1985). As evidenced by the dual directional preferences of the splenius muscle, preferred directions recorded in this study were not always in agreement with previous reports of muscle directional properties (Vitti et al. 1973; Takebe et al. 1974). Directional preferences also did not always align with the pulling directions described for these muscles in standard anatomy texts (Lockhart et al. 1972). One explanation for these differences is that, previously, EMG activity was measured from only one muscle at a time, and then only in the pure pitch and roll directions. Human neck muscles may be programmed like the neck muscles in the cat rather than like human arm muscles. In the upper limb, activation directions have been reported to be closely aligned with pulling directions (Buchanan et al. 1986). In the neck, preferred activation and pulling directions can differ (Baker and Wickland 1988), and voluntary response patterns of a muscle can vary between animals (Keshner and Peterson 1988) A second explanation is that all of these studies examine different tasks. The head or limb has been either free to move in space (Vitti et al. 1973; Zangemeister et al. 1982; Keshner and Peterson 1988), stabilized isometrically against resistance (Vitti et al. 1973; Buchanan et al. 1986), or rotated with the body so that no neck angular deviation occurs (Baker and Wickland 1988). This study is based on a static stabilization of the head against a continuous, steady displacing force. Normally, head stabilization would take place under conditions where either the body position has been changed, or the head is reorienting in space. It is possible that the central programs are task dependent, and a different central program might emerge for each of these conditions. Regardless of the task, the spatial organization of the muscles relative to their anatomical arrangement must await precise measurements of the anatomy of the musculoskeletal system of the human neck. Directional properties of the task do not appear to be the only component of the task that determines which CNS motor program should be issued. Our attempts at increasing the force requirements for head stabilization resulted not only in an increase in EMG activation, but also in a shift from a pattern of reciprocal activation to one of cocontraction. Accompanying this change in motor program was a nonlinear shift in EMG output with increased force output in directions that previously produced no EMG response. Non-linearity in the directional parameters of the response raises some question about how the CNS programs the commands for reciprocal activation and coactivation. Fel'dman (1987) states
343 that the two central programs (reciprocal activation and coactivation) are switched on simultaneously when producing limb movements. Stable equilibrium of a limb following application of a load is then maintained through a proportional change in the agonist and antagonist muscle activation (Fel'dman 1980). If a proportional change in gain were the requisite of both programs in response to changes in load, then with linear changes in load we would expect a linear variation in activation levels of both agonist and antagonist muscles regardless of the direction of applied force (Nicholls and Houk 1976). The sudden jump from a null to a strongly activated response in the nonpreferred direction of a neck muscle (e.g. SEMI at -90 ~ in Fig. 2), would therefore require an equal increase in the activation level of whichever muscle was acting in its preferred direction. Even at maximum loading of a muscle, increases of equal magnitude were not seen in the preferred directions. The sudden EMG activity in the non-preferred directions could be. the result of recruiting a different population of motor units from the same muscle as the force demands increased. Directional preferences in motor unit response and recruitment have been observed previously in the arm (ter Haar Romeny et al. 1982; Denier van der Gon et al. 1985), where it was suggested that different motor units within the same muscle could be programmed to have different directional preferences. Another possibility is that the ratio of fiber composition in the muscles is variable, resulting in different force generation properties for different parts of the muscle (DeLuca et al. 1982). Failure to record EMG activity for sternocleidomastoid in any but the preferred directions could then be explained by the fact that this muscle was more isomorphic than the other three recorded muscles, and might therefore be programmed to act in a single functional direction. Single motor unit studies of various parts of each neck muscle might, in future, support this explanation. From this study, it would appear that at some critical force level, there is a change to an alternate central command that produces the cocontraction response rather than the imposition of a simple cocontraction pattern that increases the activity of all muscles by an equal amount (Fel'dman 1974, 1980). In cats, changing the task produces a shift between central programs. The same head movement is achieved by an entirely different pattern of muscle response depending upon whether the task is one of reflex stabilization or voluntary tracking of the head (Keshner and Peterson 1988). While response patterns for each muscle during voluntary head movement are quite consistent for an individual cat over
several months of testing, they differ much more from animal to animal than the reflex muscle patterns, suggesting that the kinematics of voluntary head movements depend more upon learned central programs than do those of the head stabilizing reflexes. Learning may also play a part in the directional variability observed in this study. Specifically, one explanation for the use of splenius in flexion rather than extension by some subjects could rest in the past motor experiences and particular morphology of those individuals. Before accepting the results of the current study, two potential problems of the surface EMG recording techniques used in this study need to be addressed. First, because the recorded muscles were not directly visualized, mistakes may be made in placing the electrodes. Our electrode placement procedures were developed from careful anatomical studies and cadaver dissections to minimize this problem. The consistency of the results for the group (Fig. 2), and the verification of the muscle activation patterns by bipolar needle electrode recordings, suggest that we were able to record from the selected muscles in each subject. The second problem is that of picking up crosstalk from nearby muscles. Cross talk would not change our observation of complex force-activation curves which would hold even if signals from a combination of several muscles were being observed. It would, however, alter the assignment of precise maximal activation directions to specific muscles. Directional preferences recorded with surface EMG electrodes over semispinalis and splenius were similar with intramuscular recordings. Any variations in specificity of the response were probably a result of the more localized recordings achieved with bipolar needle electrodes. Apparently, the closely spaced surface electrodes helped to minimize crosstalk and it was not a problem in this study. Only trapezius exhibited a completely different response pattern that could be the result of changing the recording site to get a better picture of upper trapezius fiber activity. Intramuscular recordings thus helped to emphasize that trapezius is more tightly related to scapular than to head movement. Definitive conclusions about specific muscles recorded will require confirmation of our electrode placements with better in vivo anatomical measures such as was done in the upper extremity using ultrasound techniques (Ikai and Fukunaga 1968). Despite these constraints, the results of this study suggest that, as in ballistic head rotations (Zangemeister et al. 1982), muscle activation patterns for head stabilization are preprogrammed. Differences between patterns of activation in preferred as compared to non-preferred directions may
344
be due to the optimization of different parameters in the central motor program (Crowninshield and Brand 1981; Zangemeister et al. 1982), or the physiological composition of the muscle (DeLuca et al. 1982; Denier van der Gon et al. 1985).
Acknowledgement.
This work was supported by NIH grant
NS22490.
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Received April 25, 1988 / Accepted September 14, 1988
