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Mecca V.I.P.
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Interesting study that I just found and thought I would share. I drew a number of conclusions from the work (full ROM is very important, you still can't isolate but you can get underdeveloped points, muscles are made for movements, etc) and would like to see more.
Muscles within muscles: Coordination of 19 muscle segments within three shoulder muscles during isometric motor tasks
J.M.M. Browna, J.B. Wickhamb, , , D.J. McAndrewa and X.-F. Huanga
Journal of Electromyography and Kinesiology
Volume 17, Issue 1, February 2007, Pages 57-73
Abstract
The aim of the present study was to determine how the intra-muscular segments of three shoulder muscles were coordinated to produce isometric force impulses around the shoulder joint and how muscle segment coordination was influenced by changes in movement direction, mechanical line of action and moment arm (ma).
Twenty male subjects (mean age 22 years; range 18–30 years) with no known history of shoulder pathologies, volunteered to participate in this experiment. Utilising an electromyographic technique, the timing and intensity of contraction within 19 muscle segments of three superficial shoulder muscles (Pectoralis Major, Deltoid and Latissimus Dorsi) were studied and compared during the production of rapid (e.g. approximately 400 ms time to peak) isometric force impulses in four different movement directions of the shoulder joint (flexion, extension, abduction and adduction).
The results of this investigation have suggested that the timing and intensity of each muscle segment’s activation was coordinated across muscles and influenced by the muscle segment’s moment arm and its mechanical line of action in relation to the intended direction of shoulder movement (e.g. flexion, extension, abduction or adduction). There was also evidence that motor unit task groups were formed for individual motor tasks which comprise motor units from both adjacent and distant muscles.
It was also confirmed that for any particular motor task, individual muscle segments can be functionally classified as prime mover, synergist or antagonist – classifications which are flexible from one movement to the next.
1. Introduction
It is now well accepted that motor units, within individual muscle segments of single skeletal muscles, can be independently controlled by the central nervous system (CNS) to produce particular motor outcomes [3] and [21]. This phenomenon, which may be termed ‘functional differentiation’ [18], has been described within a number of individual skeletal muscles, including the Tensor Fascia Latae [18], the Gluteus Maximus and Medius [16], the Triceps Surae [3], the Biceps Brachii [2] and the Pectoralis Major [19]. Ettema et al. [5] has suggested that large absolute differences in moment arms between different segments of a single muscle partially explain this phenomenon.
More recent studies on the Deltoid [24] have shown that skeletal muscle has a greater potential for functional differentiation than hitherto accepted. Wickham and Brown [24] have determined that the Deltoid muscle, commonly described as having only three (anterior, middle and posterior heads) functional muscle segments [10], is composed of at least seven muscle segments which all have the potential to be independently coordinated by the CNS. Functionally independent muscle segments provided the CNS greater flexibility to “fine tune” the activity of its Deltoid motor units when controlling movements of the shoulder joint.
Furthermore, Wickham and Brown [24] have suggested that the seven individual muscle segments of the Deltoid may be functionally classified as either prime mover, synergist or antagonist muscle segments based upon their mechanical lines of action (joint movement most likely from approximation of a segment’s origin and insertion) and periods of activation. Attempts to assign functional classifications to individual muscle segments, classifications hitherto used to describe whole muscle function [1] are useful in characterising the activity of each individual muscle segment. For example, the prime mover segments of the Deltoid were found to have the most efficient mechanical lines of action, the earliest and longest durations of activation and the highest amplitudes of myoelectric activity. Deltoid muscle segments with increasingly divergent mechanical lines of action (synergist segments) were found to have increasingly later onsets, shorter periods of activation and lower intensities of myoelectric activity. Finally, antagonist segments, with mechanical lines of action opposing the movement, were activated last, had the shortest periods of activation and variable amplitudes of myoelectric activity [24].
Applying functional classifications to muscle segments within a single muscle is useful to provide a clearer understanding of how the CNS controls motor unit activity within a muscle during a range of motor tasks. However, there have been few studies into how the CNS controls the muscle segments of individual muscles constituting a muscle group around a particular joint. We do not as yet understand how the muscle segments of individual muscles, within a muscle group, are coordinated together to produce motor tasks or how that coordination is affected by factors such as movement direction and moment arm.
Therefore, the aim of the present study was to determine how the muscle segments of individual shoulder muscles were coordinated together to produce isometric force impulses around the shoulder joint and how that coordination was influenced by movement direction, mechanical line of action and moment arm. This investigation compared the activation of 19 muscle segments within three superficial shoulder muscles (Pectoralis Major, Deltoid and Latissimus Dorsi) during the execution of rapid (e.g. 400 ms time to peak) isometric force impulses in four different movement directions (shoulder-flexion, -extension, -abduction and -adduction). Our intention was to understand how individual muscle segments were coordinated not only within a single muscle, but across a group of muscles that controlled a single joint.
2. Methods
2.1. Procedures
Twenty male subjects (mean age 22 years; range 18–30 years) with no known history of shoulder pathologies, volunteered to participate in this experiment.
The subjects sat in an adjustable dental chair within a wire cage with their extended right upper limb positioned snugly within an arm cast (Fig. 1). The arm cast was immobilised by attachment to the wire cage to permit the subjects to perform a series of isometric shoulder joint tasks. The arm cast, so fitted, ensured that the right upper limb was fixed securely in space and did not move, other than due to unavoidable compression of its soft tissues, during any of the isometric motor tasks investigated.
Fig. 1. The experimental setup. Depicted is one of the subjects seated in the experimental chair with the arm cast set at 20° of abduction in the frontal plane. In this position subjects performed the static tasks of shoulder joint flexion, extension, abduction and adduction.
Each subject performed four isometric tasks; shoulder-abduction, -adduction, -flexion and -extension, at 75% of MVC, a movement time (MT) approximating 400 ms and with an inter-trial period of at least 30 s. Each task was performed with the right upper limb secured in 20° of abduction in the coronal plane with subject feedback on movement accuracy being provided by an oscilloscope.
Ten trials were recorded from each isometric movement task. Following an auditory trigger signal, each subject was asked to match an electronically generated force–time curve on an oscilloscope which provided the subject with feedback on movement direction, movement speed and the force of contraction. The order in which the trials were performed was randomised to minimise muscular fatigue and order effects. To permit normalisation of the intensity data, three MVC contractions were recorded for each movement direction at the beginning of the experiment. The MVC contractions were recorded with an inter-trail interval of 3 min.
2.2. Force recordings
Two load cells, connecting the arm cast to the wire cage, recorded the isometric force produced by the subjects in the coronal (abduction and adduction) and the sagittal (flexion and extension) planes. The output of each load cell was amplified by a DC amplifier.
2.3. Electromyographic recordings
Nineteen miniature gold bipolar surface electrodes (6.5 mm inter-electrode distance; 1.6 mm active plates) were located over the muscle segments of the three shoulder muscles investigated using anatomical landmarks derived through cadaveric dissection (Fig. 2). The anatomical criteria used to identify muscle segments within each of the three muscles may be found in Wickham [23] and Wickham et al. [25]. In short these included, distinctive origins/insertions, architectural differences (strap vs. pennate fibered), intramuscular fascial thickenings and >10° difference in lines of action between adjacent segments. One or more of these criteria needed to be present. In all 19 bipolar surface electrodes were applied to each subject; seven over the Deltoid and six each over the Pectoralis Major and the Latissimus Dorsi (Fig. 1).
Fig. 2. Muscle segments of Pectoralis Major (P), the Deltoid (D) and the Latissimus Dorsi (L). “•” indicates bipolar surface electrode site. Note that in this view segment L6 of the Latissimus Dorsi lies anterior to segment L5. Muscle segments were identified by obvious anatomical segmentation (e.g. Deltoid) or by division of relatively homogenous muscle tissue (e.g. L1 and L2 of Latissimus Dorsi).
Electrode gel was injected into the electrode wells by utilising a syringe coupled to a 1 mm cannula. The surface electrodes were secured to the subject by double-sided tape after the skin had been shaved, abraded and washed with alcohol to reduce skin resistance. Reference surface electrodes (3M paediatric electrodes) were positioned over the acromion, clavicle and the anterior superior iliac spine. The 19 bipolar surface electrodes and their reference electrodes were connected to differential preamplifiers and HUMTEC 100 EMG amplifiers (input impedance of 1 × 1013 Ω, CMRR of 110 db, signal to noise ratio of 1000:1, 1000k gain). The raw EMG signals were amplified and filtered (10 Hz high pass and 1 kHz low pass; Butterworth filters) prior to storage.
The isometric force impulse and the raw EMG waveforms were stored on an IBM compatible microcomputer after A–D conversion at 1 kHz. A 2000 ms recording period, commencing at least 200 ms before the beginning of the each motor task, was recorded for each trial.
2.4. Data analysis
Data analysis of the EMG waveforms utilised a digital signal processing (DSP) package for determinations of muscle segment contraction intensity and timing (Fig. 3). This program permitted the raw EMG signals to be processed (rectified, low passed, high passed, etc.) prior to analysis.
Fig. 3. The analysis screen window that was used to locate the temporal and consequently the intensity parameters of the EMG signals. The top window shows a representative raw EMG signal with its 20 Hz linear envelope displayed in the middle window. The middle window also displays the threshold detector set at 10% of peak segmental intensity (horizontal line) that was used to locate the on/off positions of the EMG signals. Visual detection of the signal was used when there was a low signal to noise ratio and the threshold detector could not determine an appropriate on/off location. The force record from the 100 kg prime load cell is displayed in the bottom window. The duration of each burst was integrated (time reset; 1 ms bins) to give a value of average V/ms (total V ms divided by duration). Representative data from one subject (segment D1) during a 75% MVC shoulder joint flexion task.
2.5. Timing analysis
Firstly, the time of force onset and the timing of force peak were determined with the temporal features of muscle segment activation determined in relation to these values (Fig. 3).
To determine the timing of each muscle segment, the raw EMG waveforms were rectified and smoothed with a 20 Hz low pass filter (Fig. 3). Threshold detectors (10% peak amplitude), combined with visual analysis, were used to locate the onset (ON), peak (PEAK) and end (OFF) of activity within each muscle segment (Fig. 3). From this data the duration of segmental activation could also be determined. ON and OFF were determined in relation to the beginning of the isometric force onset while PEAK was measured in relation to the timing of peak isometric force (Fig. 3).
2.6. Intensity analysis
Each EMG waveform, representing the activity of a segment within a particular trial was integrated to determine the intensity of muscle segment contraction. The EMG waveforms were full wave rectified and then integrated (10 ms bins) to determine the muscle segment’s intensity of activation or discharge rate (DR: mVms/ms). The discharge rate was the average intensity of motor unit contraction throughout the muscle segments period of activation. This value was then normalised against the discharge rate found during the MVC contractions associated with each particular movement direction.
2.7. Biomechanical analysis
Three-dimensional cartesian coordinates of each of the 19 muscle segments were determined through use of a vertical milling machine. This sort of machine, which is commonly used in engineering workshops for shaping metal very accurately (to within 0.01 mm), was considered more than adequate for our biomechanical analysis. By securing a cadaver (bisected at the waist) to a specially designed frame in front of the milling machine, 3D coordinates of each muscle segment and the axis of rotation of the shoulder joint were determined (Fig. 4). This was made possible by securing custom made pointers to the mill vice and then manipulating the milling machine X, Y and Z mill slides to approximate the pointers at each segmental attachment point. A detailed description of the utilisation of the vertical milling machine may be found in Wickham et al. [25]. AutoCAD was utilised to graphically represent the biomechanical relationships (e.g. mechanical lines of action) between each of the muscle segments and the axis of shoulder joint rotation. In addition, moment arms (ma) were determined for each individual segment for both shoulder abduction/adduction and flexion/extension.
Fig. 4. A composite representation (AutoCad) of the lines of action to the humerus for each segment of the Pectoralis Major (P), the Deltoid (D) and the Latissimus Dorsi (L). Coronal view with the upper limb abducted to 20° in the coronal plane. Representative data from one cadaver.
2.8. Functional classifications of muscle segments
The functional classifications of each muscle segment were simplified from those previously proposed by Wickham and Brown [24]. In the present study, functional classifications of muscle segments were applied as followed:
(a) Prime Mover segment: A muscle segment which was activated first and had an agonist moment arm for the intended motor task. Prime mover segments had muscle fibres with mechanical lines of action similar, or identical to, the direction of the intended joint motion.
(b) Synergist segment: A muscle segment, with an agonist muscle arm, which was activated significantly (p < 0.05) later than the prime mover segment/s. Often, the synergist segments had mechanical lines of action divergent away from the prime mover segments and the intended movement direction.
(c) Antagonist segment: A muscle segment with an antagonist moment arm which was activated with, or significantly (p < 0.05) after, the prime mover segment/s. In all cases, antagonist segments had mechanical lines of action and moment arms that opposed the direction of intended joint movement.
The functional classification of a muscle segment was determined after review of all muscles segments’ contributions, from the three muscles investigated, to the motor task. Therefore particular functional classifications (e.g. prime mover segment) for a given motor task may be applied to the muscle segments of one or more muscles.
2.9. Statistical evaluations
Repeated measures analysis of variance and Student Neumann Keuls techniques were used to evaluate the data. Pearson’s correlation coefficients were used to determine the relationship between the timing of activity in muscle segments of adjacent muscles. Statistical evaluations were designed to determine whether the timing and contraction intensity of muscle segment activity varied significantly: (a) within each individual muscle and (b) across all three muscles investigated. The level of significance was set at (p < 0.05).
3. Results
3.1. Biomechanical data
Table 1 provides a biomechanical analysis of each of the 19 muscle segments derived from one representative cadaver. Note that the largest muscle segment cross-sectional areas were found in segments P1 and P2 (clavicular head) of the Pectoralis Major, segment D3 (middle head) of the Deltoid and segment L2 (upper fibres) of Latissimus Dorsi. Within both the Deltoid and the Latissimus Dorsi, the “stronger” muscle segments were found towards the middle of the muscle. In contrast, the upper segments (clavicular head) of the Pectoralis Major had the greatest force generation potential.
The volume was calculated by the mass (g) divided by the density (g/cm3). The muscle length did not include any tendinous components. The volume (cm3) divided by the muscle length (cm) was used to calculate CSA. The percentage of total muscle mass (% of total muscle) column refers to the cross-sectional area (CSA in cm2) column with the segment now expressed as a percentage of the total muscle mass for that muscle. The adjusted CSA (cm2) column has been obtained by dividing a representative figure (cm2) from the literature [22], for the particular muscle, by the percentage of total muscle mass obtained in this study. The above study used 29 deltoid, 16 Pectoralis Major and 18 Latissimus Dorsi specimens. The average of these values was used for each muscle. The size of the cadaver used in this study approximated values obtained by other authors (see text). The force data was obtained by multiplying the adjusted CSA (cm2) by a constant of 30 N [4].
Table 2 illustrates the moment arms for each muscle segment derived for both flexion/extension and abduction/adduction of the shoulder joint. All muscle segments of the Pectoralis Major were found to have both shoulder flexion and shoulder adduction moment arms. Similarly, all muscle segments of the Latissimus Dorsi were shown to have both shoulder extension and shoulder adduction moment arms. In contrast, the muscle segments of the Deltoid were found to have moment arms for all four movement directions; segments D1–D3 (anterior and middle heads) had shoulder flexion moment arms while segments D4–D7 (posterior head) had shoulder extension moment arms. Abductor moment arms were associated with segments D1–D6 while a single segment, D7, was found to have a shoulder adductor moment arm.
The moment arm data is given in millimetres with segment actions also extrapolated and labeled as either shoulder joint flexors/extensors (anterior or posterior to the joint centre respectively) and/or abductors/adductors (superior or inferior to the joint centre respectively). The moment arm data has been determined from both frontal (abductor and adductor) and sagittal (flexor and extensor) plane views. The axis of rotation of the shoulder joint was considered as a fixed centre of rotation located in the middle of the humeral head with this position being used in similar experiments [8]. The coordinates for each segmental attachment point gathered from the milling machine was put into AUTOCAD software were moment arms were calculated. Standard deviations are in brackets. Grand mean data from 20 subjects.
3.2. Shoulder abduction
3.2.1. Timing of muscle segment activation
To produce an isometric shoulder abduction impulse, myoelectric activity was found only within the muscle segments of the Deltoid (Fig. 5 and Fig. 6); all muscle segments of Pectoralis Major and Latissimus Dorsi were myoelectrically silent (<10% MVC activity) during this task. The mean data (Table 3) indicated that the Deltoid’s middle segments, D3 and D4, were activated first more than 40 ms before the initial rise of the force impulse, with adjacent muscle segments being activated successively later (p < 0.05). The postero-medial segment D7 was activated last some 34 ms after the initial rise of the force impulse.
Fig. 5. Shoulder abduction. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. Note the waves of segment activation spreading from D3 to more medial segments. = peak of myoelectric activity in that segment, which contrasted with the myoelectric silence seen in all segments of the Pectoralis Major and the Latissimus Dorsi. Group mean data.
Fig. 6. Shoulder abduction. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note that muscle segment activity is limited to the Deltoid muscle only and more intense in the middle (adductor) segments of the muscle.
The timing of peak myoelectric activity was identical in segments D1–D6 occurring, on average, some 74 ms before the peak of the force impulse (Fig. 5). In contrast, the peak activation of the antagonist segment D7 occurred significantly (p < 0.05) later at 26 ms before the peak of the force impulse (Table 3).
The duration of muscle segment activation within the Deltoid was significantly (p < 0.05) longer in the muscle’s middle segments (D2–D5), those anatomically closer to the most efficient mechanical line of action for shoulder abduction, than its more peripheral obliquely orientated muscle segments (D1, D6 and D7) (Table 3). In all segments the duration of activation was longer than movement time (MT = 408 ms) (Fig. 5).
3.2.2. Intensity of muscle segment activation
As seen in Fig. 6 and Table 3, the intensity (%MVC) of Deltoid segment activation was significantly (p < 0.05) higher in the Deltoid’s middle segments (D2–D5) when compared to the muscles more peripheral muscle segments (D1, D6 and D7).
3.3. Shoulder adduction
3.3.1. Timing of muscle segment activation
The shoulder adduction task elicited segmental activity within all three muscles investigated although this activity was confined to only the two postero-medial segments (D6 and D7) of the Deltoid (Fig. 7 and Fig. 8).
Fig. 7. Shoulder adduction. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. = peak of myoelectric activity in that segment. Note the sequential onset of segment activation, the similar timing of segmental peak activity and the myoelectric silence within the more anterior segments of the Deltoid. Group mean data.
Fig. 8. Shoulder adduction. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note that muscle segment activity included the postero-medial segments of the Deltoid – a muscle normally described as an abductor of the shoulder joint.
As seen in Table 4, the adduction force impulse was initiated by a broad activation of all muscle segments within Latissimus Dorsi (L1–L6) followed significantly later (p < 0.05) by the lower muscle segments of the Pectoralis Major (P4–P6). The mean data indicated that segments L1–L6 and P4–P6 were all activated before the initial rise of the force impulse (FcON) (Table 4). There followed a later (p < 0.05) activation of the upper fibres of the Pectoralis Major (P1–P3), along with the D6 segment of the Deltoid, after the initial rise of the force impulse. In contrast, segment D7 of the Deltoid had a significantly (p < 0.05) earlier activation than segment D6 just 7 ms before FcON (Table 4).
Peak myoelectric activity occurred, in all muscle segments, before the peak of the force impulse (FcPEAK). However, it was found that segments L2, L3, L4 and L6 of the Latissimus Dorsi reached their highest myoelectric activity significantly (p < 0.05) earlier (approximately −117 ms) than all other muscle segments (approximately −65 ms) investigated (Table 4).
The duration of muscle segment activation was found to be longest in segments L1–L6, D7 and P3–P6 (approximately 584 ms). Segments P1, P2 and D6 were all found to have significantly (p < 0.05) shorter periods of activation (approximately 495 ms) during this task (Table 4). All active muscle segments had periods of activity longer than adduction movement time of 390 ms (Table 4).
3.3.2. Intensity of muscle segment activation
The intensities of muscle segment activation (%MVC) were similar throughout the muscle segments of Latissimus Dorsi and the lower segments of the Pectoralis Major (Table 4). All muscle segments of Latissimus Dorsi (L1–L6), and the lower segments of Pectoralis Major (P4–P6) had significantly (p < 0.05) higher intensities of activation (approximately 64% MVC) than the other activated muscle segments (approximately 34% MVC) (Table 4 and Fig. 8).
3.3.3. The sequence of muscle segment activation
Correlation of muscle segment activation times during the adduction motor task (Fig. 9) indicated that each muscle segment, within the three muscles investigated, was activated in a sequence that ignored anatomical boundaries between adjacent muscles. As seen in Fig. 9, the CNS produced three waves of muscle segment activation (sequential activation of muscle segments) during the adduction motor task. Two muscle segment activation waves, centred on segment L3, progressively activated the muscle segments of Latissimus Dorsi as well as the postero-medial segments of the Deltoid. The other wave of muscle segment activation began within segments P5 and P6 (lower fibres) and then progressively activated higher muscle segments of the Pectoralis Major. All three muscle segment activation waves were associated with high correlation coefficients (R2) of between 0.88 and 0.94 (Fig. 9).
Fig. 9. Onset (ON) of muscle segment activation within the Latissimus Dorsi (L), Deltoid (D) and the Pectoralis Major (P) during shoulder adduction. Note the waves of muscle segment activation sweeping out from segment L3 both superiorly to the Deltoid (L3–D6) and inferiorly (L3–L6). Within the Pectoralis Major, the excitation wave passes from inferior (P6) to superior (P1) segments. FcOn = initial rise of the isometric force impulse. Group mean and SEM data. High correlation coefficients (R2) characterised the waves of segment activation.
3.4. Shoulder flexion
3.4.1. Timing of muscle segment activation
The shoulder flexion task was accomplished by widespread activation of the Pectoralis Major (P1–P6), the anterior four segments of the Deltoid (D1–D4) and only one segment (L1) of the antagonist Latissimus Dorsi (Fig. 10). The task was initiated by simultaneous activation of four adjacent muscle segments on the anterior aspect of the shoulder; P1 and P2 (clavicular head) with D1 and D2 (anterior head) (Fig. 10). A significantly (p < 0.05) later activation occurred in segments P3–P6, D3, D4 and L1 (Table 5). The remaining segments (D5–D7; L2–L6) of the Deltoid and the Latissimus Dorsi respectively remained inactive during this task (Fig. 11).
Fig. 10. Shoulder flexion. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. = peak of myoelectric activity in that segment. Note the sequential activation of segments within the Pectoralis major and the (anterior and middle) Deltoid, and the myoelectric silence throughout most of the Latissimus Dorsi and the posterior segments of the Deltoid. Group mean data.
Fig. 11. Shoulder Flexion. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note that the highest intensities of muscle segment contraction were seen in adjacent segments of the Deltoid and the Pectoralis Major. Also note the unique antagonist role played by muscle segment L1.
All active muscle segments across the three muscle investigated, except segment P4, reached their maximum intensity (peak) simultaneously some 73 ms before the peak of the flexion force impulse (FcPK). Segment P4 had a significantly (p < 0.05) later peak activation approximately 46 ms before FcPK (Table 5).
The duration of muscle segment activation was shown to be significantly (p < 0.05) shorter in segments D4 (513 ms) and L1 (349 ms) than in the other activated muscle segments (585 ms). All segments, except the antagonist L1, had durations of activity longer than movement time (MT = 408 ms) (Table 5).
3.4.2. Intensity of muscle segment activation
As seen in Table 5, two of the four initially activated muscle segments (D1 and D2) had significantly (p < 0.05) higher intensities of contraction (approximately 55% MVC) than muscle segments (approximately 29% MVC) with later activation times.
3.5. Shoulder extension
3.5.1. Timing of muscle segment activation
The results for shoulder extension were almost the mirror image of those for shoulder flexion (Fig. 12 and Fig. 13). Shoulder extension was achieved through activation of the Latissimus Dorsi (L1–L6), the posterior five segments of the Deltoid (D3–D7), and the P3 segment of the Pectoralis Major (Fig. 12). The extension force impulse was initiated by synchronous activation of the upper muscle segments of Latissimus Dorsi (L1–L4) in conjunction with the posterior muscle segments of the Deltoid (D5 and D7) and segment P3 of the antagonist Pectoralis Major muscle. Other muscle segments were either activated significantly (p < 0.05) later (D3, D4, D6, L5, L6,) or not activated at all (P1, P2, P4–P6; D1 and D2) (Table 6).
Fig. 12. Shoulder extension. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. = Peak of myoelectric activity in that segment. Note that the pattern of muscle segment activity is almost the reverse of that seen in shoulder flexion (Fig. 9). Group mean data.
Fig. 13. Shoulder extension. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note the unique role of the antagonist muscle segment P3 during the extension task. Segment activity, in shoulder extension, is almost a mirror image of that seen in shoulder flexion (Fig. 10).
The timing of peak muscle activation was reached in all muscle segments before the peak of the force impulse (FcPEAK) (Table 6). Note that segments L3, L6 and P3 had the earliest (p < 0.05) myoelectric peak, approximately 100 ms prior to FcPK compared to between 60 ms and 70 ms prior to FcPK in the other active segments (L1, L2, L4, L5, D3–D7) (Fig. 13).
All active muscle segments within the three investigated muscles, except segment D3, had similar durations of activation (approximately 630 ms). Segment D3 had a significantly (p < 0.05) shorter duration of activation (approximately 574 ms) although all active muscle segments were activated longer than movement time (MT = 430 ms) (Table 6).
3.5.2. Intensity of muscle segment activation
As seen in Table 6, segments L2 and L3 along with segments D5–D7 had significantly (p < 0.05) higher intensities of muscle activation (approximately 73% MVC) when compared with other (L1, L4–L6, D3, D4 and P3) active muscle segments (approximately 42% MVC).
4. Discussion
4.1. Overview
The aim of the present study was to determine how 19 muscle segments within three adjacent superficial shoulder muscles, the Pectoralis Major, the Deltoid and the Latissimus Dorsi, were controlled by the CNS during the production of four rapid isometric shoulder tasks (abduction, adduction, flexion and extension).
Of particular interest was to understand how the timing and intensity of muscle segment activation within and across the three superficial shoulder muscles was influenced by the muscle segments mechanical line of action (joint movement most likely from approximation of a segment’s origin and insertion) and its moment arm. We wished to determine whether functional classification of muscle segments as “prime movers”, “synergists” and “antagonists”, as described previously within the Deltoid muscle [24], was more widely applicable to muscle segments within a group of active muscles.
In general, the results of this investigation indicated that the timing and intensity of each muscle segment’s activation was often determined by the segment’s function through its mechanical line of action, in relation to the intended movement direction, and its moment arm. The results support the hypothesis that the function of each muscle segment, to initiate the motor task (prime mover), to support the motor task’s goal (synergist) or to act in opposition to the motor task (antagonist), determined the muscle segments onset, duration of activity and intensity of activation. Furthermore, our results clearly showed that the activity of muscle segments within adjacent, and more distant muscles, are closely coordinated and, in agreement with Kuechle et al. [12], that the functional classifications of muscle segments were fluid and may change from one motor task to the next. Finally, our results support the contention [2], [19] and [24] that individual skeletal muscles are composed of discrete sub-volumes (segments) of muscle tissue which may be independently controlled by the CNS to produce the desired motor outcome.
4.2. Prime mover, synergist and antagonist muscle segments
Initially we have shown that within the three superficial shoulder muscles investigated, there were muscle segments which had a range of mechanical lines of action and moment arms related to the intended movement direction.
Those muscle segments which were activated first and which tended to have higher contraction intensities and longer periods of activation were termed the prime mover segments [24]. These muscle segments were found to have large agonist moment arms and favourable mechanical lines of action for the intended motor task. The early activation of the prime mover segments to initiate production of the isometric force impulses is consistent with the findings of Flanders and Soechting [6] who have reported that the first “peak” of muscle activation was always close to the mechanical line of action of the muscle.
Muscle segments with more divergent mechanical lines of actions or smaller agonist moment arms than the prime mover segments, the synergist segments, were generally activated next with similar, or smaller, durations and intensities of activation. Most agonist muscles involved in each motor task had both prime mover and synergist muscle segments the exception of the Latissimus Dorsi during shoulder adduction whose six muscle segments (L1–L6) all appeared to have a prime mover function (Fig. 6 and Table 4). This notable exception will be discussed further below.
We have also noted in the results that muscle segments with antagonist moment arms, whether located within an antagonist muscle (e.g. D1–D6 Deltoid during shoulder adduction) or as a single segment within an agonist muscle (e.g. D7 during shoulder abduction), had characteristic periods of activation (Fig. 4, Fig. 6, Fig. 9 and Fig. 11).
In general, antagonist muscle segments tended to have delayed onsets, shorter periods of activity and lower contraction intensities than the prime mover segments (e.g. D7 in shoulder abduction; D6 during shoulder adduction and L1 during shoulder flexion) (Table 3, Table 4 and Table 5). An exception was segment P3 (Pectoralis Major) during shoulder extension which was co-activated with the prime mover segments of the Latissimus Dorsi (Table 6). This was an unexpected result given that numerous reports [11] and [15] of “triphasic” muscle activation patterns during rapid isometric motor tasks have suggested that the antagonist (Ant) muscle burst is always activated after the initial agonist (Ag1) period of activation.
However, the involvement of antagonist muscle segments in these rapid isometric motor tasks is consistent with the findings of Flanders and Soechting [6] who state that antagonist muscle activity, in part, is important to counteract internal joint forces which may cause tissue damage.
In general these results, obtained from the superficial shoulder muscle group, broadly support the previous findings of Wickham and Brown [24] for the Deltoid muscle. These findings, with notable exceptions to these generalisations, will now be discussed in more detail with reference to each movement direction.
4.3. Influence of movement direction
The most simple motor control strategies were employed by the CNS during the shoulder abduction task (Table 3). Here the middle muscle segments of the Deltoid (D3 and D4) were found to have the most favourable mechanical lines of action and the greatest moment arms to produce shoulder abduction in the coronal plane. Shoulder abduction was initiated by activation of the prime mover segments D3 and D4. These segments, along with the adjacent segments D2 and D5, had the longest periods of activation and the highest intensities of contraction within the Deltoid muscle. The more peripheral and divergent segments of this muscle, D1, D6 and D7, all had later onsets, shorter periods of activation and lower contraction intensities reflecting their less favourable mechanical lines of action and smaller abduction moment arms (Table 2).
Interestingly, segment D7 on the postero-medial aspect of the Deltoid was found uniquely to have an antagonist moment arm for shoulder abduction. Accordingly, its period of activation was very late (e.g. 34 ms after FcON), short and of low intensity. Although D7 was anatomically contingent with segment D6, it is clearly seen that the CNS controlled the motor units of D7 independently of those within D6. The difference in moment arms between D7 (antagonist ma = −10.5 mm) and D6 (agonist ma = +8.2 mm) for the shoulder abduction task appeared to explain their contrasting periods of activity.
A more complicated and difficult to explain muscle segment control strategy was seen during shoulder adduction (Table 4). This motor task involved all three superficial muscles including segments of the Deltoid muscle (Fig. 6) – a muscle which Hughes and Kai-Nan [9] had previously predicted should have had no activity for this motor task.
Shoulder adduction was initiated by activation of the entire Latissimus Dorsi (L1–L6), some 52 ms (group mean) before the initial rise of the force–time curve (FcON) (Fig. 6). Therefore, all segments of the Latissimus Dorsi could be considered prime mover segments although their mechanical lines of action and adduction moment arms were variable (Table 1). In contrast, the segments of the Pectoralis Major were all activated as synergists with the lower fibres (P4–P6) and then the upper fibres (P1–P3) being activated in sequence (Table 4). The utilisation of all segments of the Latissimus Dorsi as the prime movers for shoulder adduction, in preference to those of the Pectoralis Major, was an unexpected result which was difficult to explain. Both muscles have large adductor moment arms (Table 2) and muscle segments with effective mechanical lines of action for the motor task. Both muscles also insert into the bicipital groove [7] and have similar cross-sectional areas (Table 1). Possibly the more posterior orientation of the Latissimus Dorsi muscle segments afforded biomechanical advantages to the CNS in the initiation of this motor task. However, further work is required before this result can be fully explained.
During shoulder adduction, all segments of the antagonist Deltoid muscle were myoelectrically silent except for segments D6 (antagonist ma = −8 mm) and D7 (agonist ma = +10.5 mm) (Fig. 6 and Table 4). The onset of segment D7 activation suggested a synergist function, with the lower fibres of the Pectoralis Major (P4–P6), to assist production of the adduction force impulse. In contrast, segment D6 clearly functioned as an antagonist to the motor task. D6 was coactivated with the fibres of the Pectoralis Major although only at a very low (28% MVC) intensity of activation. Similar findings were made by Flanders and Soechting [6] who noted, in the posterior (and medial) Deltoid during isometric motor tasks, that motor units may be directionally tuned in opposite movement directions within the same muscle segment.
Muscle segment function during shoulder flexion and shoulder extension appeared as a mirror image. During shoulder flexion (Table 5), the clavicular head of Pectoralis Major (P1 and P2), along with the anterior head of the Deltoid (D1 and D2), acted as the prime mover segments. All four segments had good mechanical lines of action and large moment arms for the shoulder flexion task (agonist ma = +18 mm to +53 mm). The lower fibres of Pectoralis Major (P3–P6) and the middle fibres of the Deltoid (D3–D4) then acted as synergist segments. These segments all had more divergent mechanical lines of action although their flexion moment arms were still impressive (e.g., P3 agonist ma = 50 mm; P4 agonist ma = 32 mm) (Table 2). It is interesting to note in this motor task that muscle segments with very large agonist moment arms (e.g. P3 and P4) were not necessarily activated as prime mover segments if their mechanical lines of action were too divergent from movement direction.
With an antagonist moment arm of −60 mm, segment L1 was the only segment of the Latissimus Dorsi to be active during the shoulder flexion task. Its late activation, shorter duration of activity and low intensity of activation clearly defined this segment’s antagonist role (Table 5). The horizontal orientation of its muscle fibres may have also produced an optimal ability to oppose the forward translatory motion of the humerus during the flexion motor task.
In contrast shoulder extension (Table 6) was initiated by the upper fibres of Latissimus Dorsi (L1–L4) and two segments of the Deltoid (D5 and D7) (Fig. 11). Again these prime mover segments had good mechanical lines of action for shoulder extension and large extension moment arms (ma range = +63 mm (D7) to +31 mm (L4)) (Table 2). The synergist segments (L5, L6, D6 and D4) were then activated to complete the motor task. Again, these synergist segments had more divergent mechanical lines of action and generally smaller extension moment arms (ma range = +50 mm to +21 mm).
Two antagonist muscle segments were activated during shoulder extension. Segment D3 of the Deltoid, with an antagonist moment arm of −8.3 mm, was activated after the prime mover segments. Its late activation, shorter duration of activity and lower intensity of activation (33% MVC), clearly reflected its antagonist role. In contrast segment P3 of the Pectoralis Major, with an antagonist moment arm of −50 mm, had an onset similar to the prime mover segments. As seen in Table 6, segment P3 was co-activated with the prime mover segments L1–L4, D5 and D7. Its peak intensity and duration of activity (Table 6) were also similar to the prime mover segments although its intensity of activation was significantly (p < 0.05) lower at 11% of MVC. It is difficult to explain why this particular antagonist muscle segment, the only segment of the Pectoralis Major to be activated during shoulder extension, should have such an early activation although its horizontal muscle fibre orientation may be implicated. Activation of the P3 segment may have been required early to protect the anterior shoulder from injury during the vigorous activation (approximately 73% of MVC group mean) of the prime mover segments; a role commonly given to antagonist muscle action [6]. If this hypothesis is true, it is evident that the CNS has considerable flexibility regarding the timing of antagonist muscle activity during the production of motor tasks.
With regard to the peak of muscle segment activation, it is clear that for all muscle segments involved in the four motor tasks investigated, maximal motor unit activation occurred before the peak of the isometric force–time curve. In general, prime mover segments had earlier peak intensities when compared to synergist segments although this was not always the case. There was, however, some limited evidence to suggest that the peak activation of some antagonist muscle segments was significantly (p < 0.05) later than the agonist muscle segments (Table 3).
4.4. Motor unit task groups
It was evident that to produce each of the four movement tasks, motor unit task groups were formed both within, and where appropriate, across the three shoulder muscles, and then activated (timing and intensity) sequentially to produce the movement task. Motor unit task groups may be defined as a group of motor units, from within a muscle or across several muscles, which are active simultaneously for a particular motor task [14]. It is thought that differences in moment arms, or physiological factors such as fibre type, may explain the existence of motor unit task groups, and therefore functionally independent muscle segments within muscle [5].
In the present study, each motor task was accomplished through the formation of at least two, and up to four, different motor unit task groups which often comprised motor units from adjacent, and more distant, muscles. For example, during shoulder abduction two motor unit task groups were formed within the Deltoid to achieve the motor task. The first motor unit task group formed included the prime mover segments (D3, D4), a common feature in all movement tasks in this study. A second motor unit task group was then formed by the remaining synergist and antagonist segments (D1, D2, D5, D6 and D7) which all had smaller abduction moment arms, or in the case of D7, an adduction moment arm. Contrary to the hypothesis of Flanders and Soechting [6], there was no evidence to suggest that the motor units of the middle (D3) and posterior (D4–D7) Deltoid were tightly coupled during this motor task.
Shoulder adduction was accomplished with the formation of three motor unit task groups. The first contained all motor units within the Latissimus Dorsi muscle which acted together as the prime movers for the motor task. A second group was formed by motor units within the lower fibres of Pectoralis Major along with the agonist segment D7 of the Deltoid. A third group was formed by motor units within the upper fibres of the Pectoralis Major along with the antagonist D6 segment of the Deltoid. Fig. 8 clearly shows the three motor unit task groups and confirms that the activation of segments (motor units) within each task group was sequential away from muscle segments with higher agonist moment arms.
Two motor unit task groups were formed during shoulder flexion while three were formed during shoulder extension. In both movement tasks, the first group contained the prime mover segments while the second comprised synergist segments. All motor unit task groups contained motor units from a number of muscles. The antagonist segments either formed their own motor unit task group (shoulder extension) or were distributed either to the first (shoulder extension) or the second (shoulder flexion) motor unit task group.
4.5. Muscle segment function and the CNS
The production of muscle force is a product of moment arm, muscle size, the muscle’s length tension relationship as well as the timing and intensity of motor unit activation; the latter controlled by the CNS [12]. Our results support the suggestion that the CNS, through its upper and lower motoneurons, has the flexibility to “fine tune” and coordinate the timing and intensity of motor unit activity both within a single muscle and between adjacent and more distant muscles, to meet the intended goals of the motor task.
It has been previously demonstrated, in monkey cortex, that pyramidal tract neurons from layer 5 of M1 (the primary motor cortex) directly innervate lower motor neurons in layer IX of the spinal cord [20]. These are the motoneurons which have direct control over the activation of a muscle’s constituent fibres.
Given that there is a proven relationship between the activity of upper motoneurons within a cortical column, and the subsequent EMG activity within an active muscle [17], the results of this study may be used to gain further insight into the strategies used by the CNS to control voluntary movement.
Specifically, our study supports the contention that specific motor columns within the human M1 (primary motor cortex), have the ability to independently control discrete subpopulations of motor units within a single skeletal muscle. This has previously only been confirmed in animal studies [13] and [17]. Therefore, our results give further insight into the complexity of the task faced by the CNS to control each and every muscle involved in even the most simple of motor tasks.
4.6. Limitations
Several limitations in the experimental design may have influenced the results.
Firstly, it should not be concluded that the 19 muscle segments identified in this study represented the “ultimate” design imposed by the CNS. In some instances (e.g. Latissimus Dorsi), the anatomical borders of each muscle segment were found by simple division of relatively homogenous muscle tissue. Even when the muscle segments were clearly defined anatomically (e.g. Deltoid), it may be possible that each segment could be further subdivided into ever smaller functional units. It is not beyond possibility that the “ultimate muscle segment” would be represented by a single muscle spindle and its associated muscle fibers! However, it remains probable that similar findings, to those found here, would have been found if fewer, or more, muscle segments had been investigate. The exciting possibility now exists for the application of a multi-electrode fine-wire EMG technique, to an in vitro analysis of animal muscle, whereby more muscle segments may be investigated and greater clarity provided to their neuromuscular control.
A second limitation was the problem of crosstalk between adjacent bipolar electrode pairs. If detectable levels of crosstalk were present, the ability to differentiate between the activity of adjacent muscle segments would be compromised. Considerable effort was made to minimize the effects of electrode crosstalk. The bipolar electrodes were specifically designed to have small active plates (1.6 mm in diameter) and inter-electrode distances (6.5 mm). This electrode design, using the crosstalk “rule of thumb” reported by Basmajian and DeLuca [1], would suggest meaningful pickup of muscle fiber activity only within approximately 6.5 mm of each bipolar electrode pair. Adjacent bipolar electrode pairs were generally spaced more than 2 cm from each other so as to minimize, as much as practicable, electrode crosstalk. In addition, regardless of possible electrode crosstalk, the results presented here provide strong evidence of the sequential activation of adjacent muscle segments to control these isometric tasks (Fig. 8). It would have been expected that high levels of electrode crosstalk would have negated the possibility of this result.
5. Conclusion
The aim of this study was to determine how 19 muscle segments within the Latissimus Dorsi, Deltoid and Pectoralis Major, were controlled by the CNS to produce four isometric shoulder motor tasks.
The results of this investigation have suggested that the timing and intensity of each muscle segment’s activation were coordinated across muscles and influenced by the muscle segment’s moment arm and its mechanical line of action in relation to the intended shoulder movement direction (e.g. flexion, extension, abduction or adduction). There was also evidence that motor unit task groups were formed for individual motor tasks which comprised motor units from both adjacent and distant muscles. In addition, the results supported the hypothesis that individual muscles segments may be functionally classified as prime mover, synergist or antagonist; functional classifications which were generally determined by the muscles segments moment arm and/or mechanical line of action.
Acknowledgements
The authors wish to thank the University of Wollongong for technical and financial support to Dr. Wickham during his doctoral studies and to Dr. Brown during his sabbatical leave in Germany. Thank you also to Mr. Luke Bones and Mr. Daniel Wickham for assistance with preparation of the illustrations and to the reviewers for the excellent comments and suggestions. The work described in this study was approved by the Human Ethics Committee of the University of Wollongong.
References
[1] J.V. Basmajian and C. DeLuca, Muscles alive; their functions revealed by electromyography (5th ed.), Williams & Wilkins, Baltimore (1985).
[2] J.M.M. Brown, C. Solomon and M.E. Paton, Further evidence of functional differentiation within biceps brachii, Electromyograph Clin Neurophysiol 33 (1993), pp. 301–309. View Record in Scopus | Cited By in Scopus (11)
[3] K.M. Campbell, B.A. Norman, L. Biggs, P.L. Blanton and R.P. Lehr, Electromyographic investigation of the relative activity among four components of the triceps surae, Am J Phys Med 52 (1973) (1), pp. 30–41. View Record in Scopus | Cited By in Scopus (14)
[4] Enoka RM. The neuromechanical basis of kinesiology, 2nd ed. In: Human kinetics, 1994.
[5] G.J.C. Ettema, G. Styles and V. Kippers, The moment arms of 23 muscle segments of the upper limb with varying elbow and forearm positions: Implications for motor control, Human Movement Sci 17 (1998) (2), pp. 201–220. Abstract | Article | PDF (268 K) | View Record in Scopus | Cited By in Scopus (29)
[6] M. Flanders and J.F. Soechting, Arm muscle activation for static forces in three-dimensional space, J Neurophysiol 64 (1990) (6), pp. 1818–1837. View Record in Scopus | Cited By in Scopus (65)
[7] Gray’s Anatomy, The anatomical basis of medicine and surgery, Churchill Livingstone, Sydney (1990).
[8] C. Hogfors, G. Sigholm and P. Herberts, Biomechanical model of the human shoulder – I. Elements, J Biomech 20 (1987) (2), pp. 157–166. Abstract | PDF (1082 K) | View Record in Scopus | Cited By in Scopus (52)
[9] R.E. Hughes and A. Kai-Nan, Force analysis of rotator cuff muscles, Clin Orthopaed Related Res 1 (1996) (330), pp. 75–83. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (45)
[10] D.B. Jenkins,Hollinshead’s functional anatomy of the limbs and back (7th ed.), W.B. Saunders, Sydney (1998).
[11] G.M. Karst and Z. Hassan, Antagonist muscle activity during forearm movements under varying kinematic and loading conditions, Exp Brain Res 67 (1987), pp. 391–401. View Record in Scopus | Cited By in Scopus (35)
[12] D.K. Kuechle, S.R. Newman, E. Itoi, G.L. Niebur, B.F. Morrey and K-N. An, The relevance of the moment arm of shoulder muscles with respect to axial rotation of the glenohumeral joint in four positions, Clin Biomech 15 (2000) (5), pp. 322–329. Abstract | Article | PDF (383 K) | View Record in Scopus | Cited By in Scopus (28)
[13] R. Lemon, The output map of the primate motor cortex, Trends Neurosci 11 (1988), pp. 501–506 1989, erratum appears in Trends Neurosci Apr;12(4):158.. Abstract | PDF (748 K) | View Record in Scopus | Cited By in Scopus (48)
[14] G.E. Loeb, Motorneuron task groups: Coping with kinematic heterogeneity, J Exp Biol 115 (1985), pp. 137–146. View Record in Scopus | Cited By in Scopus (47)
[15] C.D. MacKinnon and J.C. Rothwell, Time-varying changes in corticospinal excitability accompanying the triphasic EMG pattern, J. Physiol. 506P (1998), p. 114P.
[16] Y. Manueddu, W. Blanc and W. Taillard, Study of the functioning of the Gluteus Medius and Maximus: An electromyographic analysis, Ann Kinesither 16 (1989), pp. 193–201.
[17] R.B. Muir and R.N. Lemon, Corticospinal neurons with a special role in precision grip, Brain Res 61 (1983), pp. 312–316. Abstract | PDF (393 K) | View Record in Scopus | Cited By in Scopus (105)
[18] E.B. Pare, J.R. Stern and J.M. Schwartz, Functional differentiation within the tensor fascia latae, J Bone Joint Surg A 63 (1981) (9), pp. 239–246.
[19] M.E. Paton and J.M.M. Brown, An electromyographic analysis of functional differentiation in human pectoralis major muscle, J Electromyograph Kinesiol 4 (1994) (3), pp. 161–169. Abstract | PDF (943 K) | View Record in Scopus | Cited By in Scopus (12)
[20] Y. Shinoda, J. Yokota and T. Futami, Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey, Neurosci Lett 23 (1981), pp. 7–12. Abstract | PDF (808 K) | View Record in Scopus | Cited By in Scopus (84)
[21] G.L. Soderberg and W.F. Dostal, Electromyographic study of three parts of the gluteus medius muscle during functional activities, Phys Therapy 58 (1978) (6), pp. 691–696. View Record in Scopus | Cited By in Scopus (23)
[22] H.E.V. Veeger, F.C.T. VanDerHelm, L.H.V. VanDerWoude, G.M. Pronk and R.H. Rozendal, Inertia and muscle contraction parameters for musculoskeletal modelling of the shoulder mechanism, J Biomech 24 (1991) (7), pp. 615–629. Abstract | PDF (2423 K) | View Record in Scopus | Cited By in Scopus (80)
[23] Wickham JB. Muscles within Muscles: The neuromotor activation patterns of intramuscular segments. PhD thesis, Department of Biomedical Science, University of Wollongong, 2002.
[24] J.B. Wickham and J.M.M. Brown, Muscles within muscles: the neuromotor control of intra-muscular segments, Eur J Appl Physiol 78 (1998), pp. 219–225. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (24)
[25] J.B. Wickham, J.M.M. Brown and D.J. McAndrew, Muscles within muscles: Anatomical and functional segmentation of selected shoulder joint musculature, J Musculoskeletal Res 8 (2004) (1), pp. 57–73. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (5)
Muscles within muscles: Coordination of 19 muscle segments within three shoulder muscles during isometric motor tasks
J.M.M. Browna, J.B. Wickhamb, , , D.J. McAndrewa and X.-F. Huanga
Journal of Electromyography and Kinesiology
Volume 17, Issue 1, February 2007, Pages 57-73
Abstract
The aim of the present study was to determine how the intra-muscular segments of three shoulder muscles were coordinated to produce isometric force impulses around the shoulder joint and how muscle segment coordination was influenced by changes in movement direction, mechanical line of action and moment arm (ma).
Twenty male subjects (mean age 22 years; range 18–30 years) with no known history of shoulder pathologies, volunteered to participate in this experiment. Utilising an electromyographic technique, the timing and intensity of contraction within 19 muscle segments of three superficial shoulder muscles (Pectoralis Major, Deltoid and Latissimus Dorsi) were studied and compared during the production of rapid (e.g. approximately 400 ms time to peak) isometric force impulses in four different movement directions of the shoulder joint (flexion, extension, abduction and adduction).
The results of this investigation have suggested that the timing and intensity of each muscle segment’s activation was coordinated across muscles and influenced by the muscle segment’s moment arm and its mechanical line of action in relation to the intended direction of shoulder movement (e.g. flexion, extension, abduction or adduction). There was also evidence that motor unit task groups were formed for individual motor tasks which comprise motor units from both adjacent and distant muscles.
It was also confirmed that for any particular motor task, individual muscle segments can be functionally classified as prime mover, synergist or antagonist – classifications which are flexible from one movement to the next.
1. Introduction
It is now well accepted that motor units, within individual muscle segments of single skeletal muscles, can be independently controlled by the central nervous system (CNS) to produce particular motor outcomes [3] and [21]. This phenomenon, which may be termed ‘functional differentiation’ [18], has been described within a number of individual skeletal muscles, including the Tensor Fascia Latae [18], the Gluteus Maximus and Medius [16], the Triceps Surae [3], the Biceps Brachii [2] and the Pectoralis Major [19]. Ettema et al. [5] has suggested that large absolute differences in moment arms between different segments of a single muscle partially explain this phenomenon.
More recent studies on the Deltoid [24] have shown that skeletal muscle has a greater potential for functional differentiation than hitherto accepted. Wickham and Brown [24] have determined that the Deltoid muscle, commonly described as having only three (anterior, middle and posterior heads) functional muscle segments [10], is composed of at least seven muscle segments which all have the potential to be independently coordinated by the CNS. Functionally independent muscle segments provided the CNS greater flexibility to “fine tune” the activity of its Deltoid motor units when controlling movements of the shoulder joint.
Furthermore, Wickham and Brown [24] have suggested that the seven individual muscle segments of the Deltoid may be functionally classified as either prime mover, synergist or antagonist muscle segments based upon their mechanical lines of action (joint movement most likely from approximation of a segment’s origin and insertion) and periods of activation. Attempts to assign functional classifications to individual muscle segments, classifications hitherto used to describe whole muscle function [1] are useful in characterising the activity of each individual muscle segment. For example, the prime mover segments of the Deltoid were found to have the most efficient mechanical lines of action, the earliest and longest durations of activation and the highest amplitudes of myoelectric activity. Deltoid muscle segments with increasingly divergent mechanical lines of action (synergist segments) were found to have increasingly later onsets, shorter periods of activation and lower intensities of myoelectric activity. Finally, antagonist segments, with mechanical lines of action opposing the movement, were activated last, had the shortest periods of activation and variable amplitudes of myoelectric activity [24].
Applying functional classifications to muscle segments within a single muscle is useful to provide a clearer understanding of how the CNS controls motor unit activity within a muscle during a range of motor tasks. However, there have been few studies into how the CNS controls the muscle segments of individual muscles constituting a muscle group around a particular joint. We do not as yet understand how the muscle segments of individual muscles, within a muscle group, are coordinated together to produce motor tasks or how that coordination is affected by factors such as movement direction and moment arm.
Therefore, the aim of the present study was to determine how the muscle segments of individual shoulder muscles were coordinated together to produce isometric force impulses around the shoulder joint and how that coordination was influenced by movement direction, mechanical line of action and moment arm. This investigation compared the activation of 19 muscle segments within three superficial shoulder muscles (Pectoralis Major, Deltoid and Latissimus Dorsi) during the execution of rapid (e.g. 400 ms time to peak) isometric force impulses in four different movement directions (shoulder-flexion, -extension, -abduction and -adduction). Our intention was to understand how individual muscle segments were coordinated not only within a single muscle, but across a group of muscles that controlled a single joint.
2. Methods
2.1. Procedures
Twenty male subjects (mean age 22 years; range 18–30 years) with no known history of shoulder pathologies, volunteered to participate in this experiment.
The subjects sat in an adjustable dental chair within a wire cage with their extended right upper limb positioned snugly within an arm cast (Fig. 1). The arm cast was immobilised by attachment to the wire cage to permit the subjects to perform a series of isometric shoulder joint tasks. The arm cast, so fitted, ensured that the right upper limb was fixed securely in space and did not move, other than due to unavoidable compression of its soft tissues, during any of the isometric motor tasks investigated.
Fig. 1. The experimental setup. Depicted is one of the subjects seated in the experimental chair with the arm cast set at 20° of abduction in the frontal plane. In this position subjects performed the static tasks of shoulder joint flexion, extension, abduction and adduction.
Each subject performed four isometric tasks; shoulder-abduction, -adduction, -flexion and -extension, at 75% of MVC, a movement time (MT) approximating 400 ms and with an inter-trial period of at least 30 s. Each task was performed with the right upper limb secured in 20° of abduction in the coronal plane with subject feedback on movement accuracy being provided by an oscilloscope.
Ten trials were recorded from each isometric movement task. Following an auditory trigger signal, each subject was asked to match an electronically generated force–time curve on an oscilloscope which provided the subject with feedback on movement direction, movement speed and the force of contraction. The order in which the trials were performed was randomised to minimise muscular fatigue and order effects. To permit normalisation of the intensity data, three MVC contractions were recorded for each movement direction at the beginning of the experiment. The MVC contractions were recorded with an inter-trail interval of 3 min.
2.2. Force recordings
Two load cells, connecting the arm cast to the wire cage, recorded the isometric force produced by the subjects in the coronal (abduction and adduction) and the sagittal (flexion and extension) planes. The output of each load cell was amplified by a DC amplifier.
2.3. Electromyographic recordings
Nineteen miniature gold bipolar surface electrodes (6.5 mm inter-electrode distance; 1.6 mm active plates) were located over the muscle segments of the three shoulder muscles investigated using anatomical landmarks derived through cadaveric dissection (Fig. 2). The anatomical criteria used to identify muscle segments within each of the three muscles may be found in Wickham [23] and Wickham et al. [25]. In short these included, distinctive origins/insertions, architectural differences (strap vs. pennate fibered), intramuscular fascial thickenings and >10° difference in lines of action between adjacent segments. One or more of these criteria needed to be present. In all 19 bipolar surface electrodes were applied to each subject; seven over the Deltoid and six each over the Pectoralis Major and the Latissimus Dorsi (Fig. 1).
Fig. 2. Muscle segments of Pectoralis Major (P), the Deltoid (D) and the Latissimus Dorsi (L). “•” indicates bipolar surface electrode site. Note that in this view segment L6 of the Latissimus Dorsi lies anterior to segment L5. Muscle segments were identified by obvious anatomical segmentation (e.g. Deltoid) or by division of relatively homogenous muscle tissue (e.g. L1 and L2 of Latissimus Dorsi).
Electrode gel was injected into the electrode wells by utilising a syringe coupled to a 1 mm cannula. The surface electrodes were secured to the subject by double-sided tape after the skin had been shaved, abraded and washed with alcohol to reduce skin resistance. Reference surface electrodes (3M paediatric electrodes) were positioned over the acromion, clavicle and the anterior superior iliac spine. The 19 bipolar surface electrodes and their reference electrodes were connected to differential preamplifiers and HUMTEC 100 EMG amplifiers (input impedance of 1 × 1013 Ω, CMRR of 110 db, signal to noise ratio of 1000:1, 1000k gain). The raw EMG signals were amplified and filtered (10 Hz high pass and 1 kHz low pass; Butterworth filters) prior to storage.
The isometric force impulse and the raw EMG waveforms were stored on an IBM compatible microcomputer after A–D conversion at 1 kHz. A 2000 ms recording period, commencing at least 200 ms before the beginning of the each motor task, was recorded for each trial.
2.4. Data analysis
Data analysis of the EMG waveforms utilised a digital signal processing (DSP) package for determinations of muscle segment contraction intensity and timing (Fig. 3). This program permitted the raw EMG signals to be processed (rectified, low passed, high passed, etc.) prior to analysis.
Fig. 3. The analysis screen window that was used to locate the temporal and consequently the intensity parameters of the EMG signals. The top window shows a representative raw EMG signal with its 20 Hz linear envelope displayed in the middle window. The middle window also displays the threshold detector set at 10% of peak segmental intensity (horizontal line) that was used to locate the on/off positions of the EMG signals. Visual detection of the signal was used when there was a low signal to noise ratio and the threshold detector could not determine an appropriate on/off location. The force record from the 100 kg prime load cell is displayed in the bottom window. The duration of each burst was integrated (time reset; 1 ms bins) to give a value of average V/ms (total V ms divided by duration). Representative data from one subject (segment D1) during a 75% MVC shoulder joint flexion task.
2.5. Timing analysis
Firstly, the time of force onset and the timing of force peak were determined with the temporal features of muscle segment activation determined in relation to these values (Fig. 3).
To determine the timing of each muscle segment, the raw EMG waveforms were rectified and smoothed with a 20 Hz low pass filter (Fig. 3). Threshold detectors (10% peak amplitude), combined with visual analysis, were used to locate the onset (ON), peak (PEAK) and end (OFF) of activity within each muscle segment (Fig. 3). From this data the duration of segmental activation could also be determined. ON and OFF were determined in relation to the beginning of the isometric force onset while PEAK was measured in relation to the timing of peak isometric force (Fig. 3).
2.6. Intensity analysis
Each EMG waveform, representing the activity of a segment within a particular trial was integrated to determine the intensity of muscle segment contraction. The EMG waveforms were full wave rectified and then integrated (10 ms bins) to determine the muscle segment’s intensity of activation or discharge rate (DR: mVms/ms). The discharge rate was the average intensity of motor unit contraction throughout the muscle segments period of activation. This value was then normalised against the discharge rate found during the MVC contractions associated with each particular movement direction.
2.7. Biomechanical analysis
Three-dimensional cartesian coordinates of each of the 19 muscle segments were determined through use of a vertical milling machine. This sort of machine, which is commonly used in engineering workshops for shaping metal very accurately (to within 0.01 mm), was considered more than adequate for our biomechanical analysis. By securing a cadaver (bisected at the waist) to a specially designed frame in front of the milling machine, 3D coordinates of each muscle segment and the axis of rotation of the shoulder joint were determined (Fig. 4). This was made possible by securing custom made pointers to the mill vice and then manipulating the milling machine X, Y and Z mill slides to approximate the pointers at each segmental attachment point. A detailed description of the utilisation of the vertical milling machine may be found in Wickham et al. [25]. AutoCAD was utilised to graphically represent the biomechanical relationships (e.g. mechanical lines of action) between each of the muscle segments and the axis of shoulder joint rotation. In addition, moment arms (ma) were determined for each individual segment for both shoulder abduction/adduction and flexion/extension.
Fig. 4. A composite representation (AutoCad) of the lines of action to the humerus for each segment of the Pectoralis Major (P), the Deltoid (D) and the Latissimus Dorsi (L). Coronal view with the upper limb abducted to 20° in the coronal plane. Representative data from one cadaver.
2.8. Functional classifications of muscle segments
The functional classifications of each muscle segment were simplified from those previously proposed by Wickham and Brown [24]. In the present study, functional classifications of muscle segments were applied as followed:
(a) Prime Mover segment: A muscle segment which was activated first and had an agonist moment arm for the intended motor task. Prime mover segments had muscle fibres with mechanical lines of action similar, or identical to, the direction of the intended joint motion.
(b) Synergist segment: A muscle segment, with an agonist muscle arm, which was activated significantly (p < 0.05) later than the prime mover segment/s. Often, the synergist segments had mechanical lines of action divergent away from the prime mover segments and the intended movement direction.
(c) Antagonist segment: A muscle segment with an antagonist moment arm which was activated with, or significantly (p < 0.05) after, the prime mover segment/s. In all cases, antagonist segments had mechanical lines of action and moment arms that opposed the direction of intended joint movement.
The functional classification of a muscle segment was determined after review of all muscles segments’ contributions, from the three muscles investigated, to the motor task. Therefore particular functional classifications (e.g. prime mover segment) for a given motor task may be applied to the muscle segments of one or more muscles.
2.9. Statistical evaluations
Repeated measures analysis of variance and Student Neumann Keuls techniques were used to evaluate the data. Pearson’s correlation coefficients were used to determine the relationship between the timing of activity in muscle segments of adjacent muscles. Statistical evaluations were designed to determine whether the timing and contraction intensity of muscle segment activity varied significantly: (a) within each individual muscle and (b) across all three muscles investigated. The level of significance was set at (p < 0.05).
3. Results
3.1. Biomechanical data
Table 1 provides a biomechanical analysis of each of the 19 muscle segments derived from one representative cadaver. Note that the largest muscle segment cross-sectional areas were found in segments P1 and P2 (clavicular head) of the Pectoralis Major, segment D3 (middle head) of the Deltoid and segment L2 (upper fibres) of Latissimus Dorsi. Within both the Deltoid and the Latissimus Dorsi, the “stronger” muscle segments were found towards the middle of the muscle. In contrast, the upper segments (clavicular head) of the Pectoralis Major had the greatest force generation potential.
The volume was calculated by the mass (g) divided by the density (g/cm3). The muscle length did not include any tendinous components. The volume (cm3) divided by the muscle length (cm) was used to calculate CSA. The percentage of total muscle mass (% of total muscle) column refers to the cross-sectional area (CSA in cm2) column with the segment now expressed as a percentage of the total muscle mass for that muscle. The adjusted CSA (cm2) column has been obtained by dividing a representative figure (cm2) from the literature [22], for the particular muscle, by the percentage of total muscle mass obtained in this study. The above study used 29 deltoid, 16 Pectoralis Major and 18 Latissimus Dorsi specimens. The average of these values was used for each muscle. The size of the cadaver used in this study approximated values obtained by other authors (see text). The force data was obtained by multiplying the adjusted CSA (cm2) by a constant of 30 N [4].
Table 2 illustrates the moment arms for each muscle segment derived for both flexion/extension and abduction/adduction of the shoulder joint. All muscle segments of the Pectoralis Major were found to have both shoulder flexion and shoulder adduction moment arms. Similarly, all muscle segments of the Latissimus Dorsi were shown to have both shoulder extension and shoulder adduction moment arms. In contrast, the muscle segments of the Deltoid were found to have moment arms for all four movement directions; segments D1–D3 (anterior and middle heads) had shoulder flexion moment arms while segments D4–D7 (posterior head) had shoulder extension moment arms. Abductor moment arms were associated with segments D1–D6 while a single segment, D7, was found to have a shoulder adductor moment arm.
The moment arm data is given in millimetres with segment actions also extrapolated and labeled as either shoulder joint flexors/extensors (anterior or posterior to the joint centre respectively) and/or abductors/adductors (superior or inferior to the joint centre respectively). The moment arm data has been determined from both frontal (abductor and adductor) and sagittal (flexor and extensor) plane views. The axis of rotation of the shoulder joint was considered as a fixed centre of rotation located in the middle of the humeral head with this position being used in similar experiments [8]. The coordinates for each segmental attachment point gathered from the milling machine was put into AUTOCAD software were moment arms were calculated. Standard deviations are in brackets. Grand mean data from 20 subjects.
3.2. Shoulder abduction
3.2.1. Timing of muscle segment activation
To produce an isometric shoulder abduction impulse, myoelectric activity was found only within the muscle segments of the Deltoid (Fig. 5 and Fig. 6); all muscle segments of Pectoralis Major and Latissimus Dorsi were myoelectrically silent (<10% MVC activity) during this task. The mean data (Table 3) indicated that the Deltoid’s middle segments, D3 and D4, were activated first more than 40 ms before the initial rise of the force impulse, with adjacent muscle segments being activated successively later (p < 0.05). The postero-medial segment D7 was activated last some 34 ms after the initial rise of the force impulse.
Fig. 5. Shoulder abduction. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. Note the waves of segment activation spreading from D3 to more medial segments. = peak of myoelectric activity in that segment, which contrasted with the myoelectric silence seen in all segments of the Pectoralis Major and the Latissimus Dorsi. Group mean data.
Fig. 6. Shoulder abduction. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note that muscle segment activity is limited to the Deltoid muscle only and more intense in the middle (adductor) segments of the muscle.
The timing of peak myoelectric activity was identical in segments D1–D6 occurring, on average, some 74 ms before the peak of the force impulse (Fig. 5). In contrast, the peak activation of the antagonist segment D7 occurred significantly (p < 0.05) later at 26 ms before the peak of the force impulse (Table 3).
The duration of muscle segment activation within the Deltoid was significantly (p < 0.05) longer in the muscle’s middle segments (D2–D5), those anatomically closer to the most efficient mechanical line of action for shoulder abduction, than its more peripheral obliquely orientated muscle segments (D1, D6 and D7) (Table 3). In all segments the duration of activation was longer than movement time (MT = 408 ms) (Fig. 5).
3.2.2. Intensity of muscle segment activation
As seen in Fig. 6 and Table 3, the intensity (%MVC) of Deltoid segment activation was significantly (p < 0.05) higher in the Deltoid’s middle segments (D2–D5) when compared to the muscles more peripheral muscle segments (D1, D6 and D7).
3.3. Shoulder adduction
3.3.1. Timing of muscle segment activation
The shoulder adduction task elicited segmental activity within all three muscles investigated although this activity was confined to only the two postero-medial segments (D6 and D7) of the Deltoid (Fig. 7 and Fig. 8).
Fig. 7. Shoulder adduction. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. = peak of myoelectric activity in that segment. Note the sequential onset of segment activation, the similar timing of segmental peak activity and the myoelectric silence within the more anterior segments of the Deltoid. Group mean data.
Fig. 8. Shoulder adduction. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note that muscle segment activity included the postero-medial segments of the Deltoid – a muscle normally described as an abductor of the shoulder joint.
As seen in Table 4, the adduction force impulse was initiated by a broad activation of all muscle segments within Latissimus Dorsi (L1–L6) followed significantly later (p < 0.05) by the lower muscle segments of the Pectoralis Major (P4–P6). The mean data indicated that segments L1–L6 and P4–P6 were all activated before the initial rise of the force impulse (FcON) (Table 4). There followed a later (p < 0.05) activation of the upper fibres of the Pectoralis Major (P1–P3), along with the D6 segment of the Deltoid, after the initial rise of the force impulse. In contrast, segment D7 of the Deltoid had a significantly (p < 0.05) earlier activation than segment D6 just 7 ms before FcON (Table 4).
Peak myoelectric activity occurred, in all muscle segments, before the peak of the force impulse (FcPEAK). However, it was found that segments L2, L3, L4 and L6 of the Latissimus Dorsi reached their highest myoelectric activity significantly (p < 0.05) earlier (approximately −117 ms) than all other muscle segments (approximately −65 ms) investigated (Table 4).
The duration of muscle segment activation was found to be longest in segments L1–L6, D7 and P3–P6 (approximately 584 ms). Segments P1, P2 and D6 were all found to have significantly (p < 0.05) shorter periods of activation (approximately 495 ms) during this task (Table 4). All active muscle segments had periods of activity longer than adduction movement time of 390 ms (Table 4).
3.3.2. Intensity of muscle segment activation
The intensities of muscle segment activation (%MVC) were similar throughout the muscle segments of Latissimus Dorsi and the lower segments of the Pectoralis Major (Table 4). All muscle segments of Latissimus Dorsi (L1–L6), and the lower segments of Pectoralis Major (P4–P6) had significantly (p < 0.05) higher intensities of activation (approximately 64% MVC) than the other activated muscle segments (approximately 34% MVC) (Table 4 and Fig. 8).
3.3.3. The sequence of muscle segment activation
Correlation of muscle segment activation times during the adduction motor task (Fig. 9) indicated that each muscle segment, within the three muscles investigated, was activated in a sequence that ignored anatomical boundaries between adjacent muscles. As seen in Fig. 9, the CNS produced three waves of muscle segment activation (sequential activation of muscle segments) during the adduction motor task. Two muscle segment activation waves, centred on segment L3, progressively activated the muscle segments of Latissimus Dorsi as well as the postero-medial segments of the Deltoid. The other wave of muscle segment activation began within segments P5 and P6 (lower fibres) and then progressively activated higher muscle segments of the Pectoralis Major. All three muscle segment activation waves were associated with high correlation coefficients (R2) of between 0.88 and 0.94 (Fig. 9).
Fig. 9. Onset (ON) of muscle segment activation within the Latissimus Dorsi (L), Deltoid (D) and the Pectoralis Major (P) during shoulder adduction. Note the waves of muscle segment activation sweeping out from segment L3 both superiorly to the Deltoid (L3–D6) and inferiorly (L3–L6). Within the Pectoralis Major, the excitation wave passes from inferior (P6) to superior (P1) segments. FcOn = initial rise of the isometric force impulse. Group mean and SEM data. High correlation coefficients (R2) characterised the waves of segment activation.
3.4. Shoulder flexion
3.4.1. Timing of muscle segment activation
The shoulder flexion task was accomplished by widespread activation of the Pectoralis Major (P1–P6), the anterior four segments of the Deltoid (D1–D4) and only one segment (L1) of the antagonist Latissimus Dorsi (Fig. 10). The task was initiated by simultaneous activation of four adjacent muscle segments on the anterior aspect of the shoulder; P1 and P2 (clavicular head) with D1 and D2 (anterior head) (Fig. 10). A significantly (p < 0.05) later activation occurred in segments P3–P6, D3, D4 and L1 (Table 5). The remaining segments (D5–D7; L2–L6) of the Deltoid and the Latissimus Dorsi respectively remained inactive during this task (Fig. 11).
Fig. 10. Shoulder flexion. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. = peak of myoelectric activity in that segment. Note the sequential activation of segments within the Pectoralis major and the (anterior and middle) Deltoid, and the myoelectric silence throughout most of the Latissimus Dorsi and the posterior segments of the Deltoid. Group mean data.
Fig. 11. Shoulder Flexion. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note that the highest intensities of muscle segment contraction were seen in adjacent segments of the Deltoid and the Pectoralis Major. Also note the unique antagonist role played by muscle segment L1.
All active muscle segments across the three muscle investigated, except segment P4, reached their maximum intensity (peak) simultaneously some 73 ms before the peak of the flexion force impulse (FcPK). Segment P4 had a significantly (p < 0.05) later peak activation approximately 46 ms before FcPK (Table 5).
The duration of muscle segment activation was shown to be significantly (p < 0.05) shorter in segments D4 (513 ms) and L1 (349 ms) than in the other activated muscle segments (585 ms). All segments, except the antagonist L1, had durations of activity longer than movement time (MT = 408 ms) (Table 5).
3.4.2. Intensity of muscle segment activation
As seen in Table 5, two of the four initially activated muscle segments (D1 and D2) had significantly (p < 0.05) higher intensities of contraction (approximately 55% MVC) than muscle segments (approximately 29% MVC) with later activation times.
3.5. Shoulder extension
3.5.1. Timing of muscle segment activation
The results for shoulder extension were almost the mirror image of those for shoulder flexion (Fig. 12 and Fig. 13). Shoulder extension was achieved through activation of the Latissimus Dorsi (L1–L6), the posterior five segments of the Deltoid (D3–D7), and the P3 segment of the Pectoralis Major (Fig. 12). The extension force impulse was initiated by synchronous activation of the upper muscle segments of Latissimus Dorsi (L1–L4) in conjunction with the posterior muscle segments of the Deltoid (D5 and D7) and segment P3 of the antagonist Pectoralis Major muscle. Other muscle segments were either activated significantly (p < 0.05) later (D3, D4, D6, L5, L6,) or not activated at all (P1, P2, P4–P6; D1 and D2) (Table 6).
Fig. 12. Shoulder extension. Timing of muscle segment activation. P = Pectoralis Major; D = Deltoid; L = Latissimus Dorsi. Vertical dotted lines indicate the beginning (FcON) and the peak (FcPEAK) of the isometric force impulse. = Peak of myoelectric activity in that segment. Note that the pattern of muscle segment activity is almost the reverse of that seen in shoulder flexion (Fig. 9). Group mean data.
Fig. 13. Shoulder extension. Intensity of muscle segment contraction in Latissimus Dorsi (L1–L6), Deltoid (D1–D7) and Pectoralis Major (P1–P7). Diagram based on group mean data. Note the unique role of the antagonist muscle segment P3 during the extension task. Segment activity, in shoulder extension, is almost a mirror image of that seen in shoulder flexion (Fig. 10).
The timing of peak muscle activation was reached in all muscle segments before the peak of the force impulse (FcPEAK) (Table 6). Note that segments L3, L6 and P3 had the earliest (p < 0.05) myoelectric peak, approximately 100 ms prior to FcPK compared to between 60 ms and 70 ms prior to FcPK in the other active segments (L1, L2, L4, L5, D3–D7) (Fig. 13).
All active muscle segments within the three investigated muscles, except segment D3, had similar durations of activation (approximately 630 ms). Segment D3 had a significantly (p < 0.05) shorter duration of activation (approximately 574 ms) although all active muscle segments were activated longer than movement time (MT = 430 ms) (Table 6).
3.5.2. Intensity of muscle segment activation
As seen in Table 6, segments L2 and L3 along with segments D5–D7 had significantly (p < 0.05) higher intensities of muscle activation (approximately 73% MVC) when compared with other (L1, L4–L6, D3, D4 and P3) active muscle segments (approximately 42% MVC).
4. Discussion
4.1. Overview
The aim of the present study was to determine how 19 muscle segments within three adjacent superficial shoulder muscles, the Pectoralis Major, the Deltoid and the Latissimus Dorsi, were controlled by the CNS during the production of four rapid isometric shoulder tasks (abduction, adduction, flexion and extension).
Of particular interest was to understand how the timing and intensity of muscle segment activation within and across the three superficial shoulder muscles was influenced by the muscle segments mechanical line of action (joint movement most likely from approximation of a segment’s origin and insertion) and its moment arm. We wished to determine whether functional classification of muscle segments as “prime movers”, “synergists” and “antagonists”, as described previously within the Deltoid muscle [24], was more widely applicable to muscle segments within a group of active muscles.
In general, the results of this investigation indicated that the timing and intensity of each muscle segment’s activation was often determined by the segment’s function through its mechanical line of action, in relation to the intended movement direction, and its moment arm. The results support the hypothesis that the function of each muscle segment, to initiate the motor task (prime mover), to support the motor task’s goal (synergist) or to act in opposition to the motor task (antagonist), determined the muscle segments onset, duration of activity and intensity of activation. Furthermore, our results clearly showed that the activity of muscle segments within adjacent, and more distant muscles, are closely coordinated and, in agreement with Kuechle et al. [12], that the functional classifications of muscle segments were fluid and may change from one motor task to the next. Finally, our results support the contention [2], [19] and [24] that individual skeletal muscles are composed of discrete sub-volumes (segments) of muscle tissue which may be independently controlled by the CNS to produce the desired motor outcome.
4.2. Prime mover, synergist and antagonist muscle segments
Initially we have shown that within the three superficial shoulder muscles investigated, there were muscle segments which had a range of mechanical lines of action and moment arms related to the intended movement direction.
Those muscle segments which were activated first and which tended to have higher contraction intensities and longer periods of activation were termed the prime mover segments [24]. These muscle segments were found to have large agonist moment arms and favourable mechanical lines of action for the intended motor task. The early activation of the prime mover segments to initiate production of the isometric force impulses is consistent with the findings of Flanders and Soechting [6] who have reported that the first “peak” of muscle activation was always close to the mechanical line of action of the muscle.
Muscle segments with more divergent mechanical lines of actions or smaller agonist moment arms than the prime mover segments, the synergist segments, were generally activated next with similar, or smaller, durations and intensities of activation. Most agonist muscles involved in each motor task had both prime mover and synergist muscle segments the exception of the Latissimus Dorsi during shoulder adduction whose six muscle segments (L1–L6) all appeared to have a prime mover function (Fig. 6 and Table 4). This notable exception will be discussed further below.
We have also noted in the results that muscle segments with antagonist moment arms, whether located within an antagonist muscle (e.g. D1–D6 Deltoid during shoulder adduction) or as a single segment within an agonist muscle (e.g. D7 during shoulder abduction), had characteristic periods of activation (Fig. 4, Fig. 6, Fig. 9 and Fig. 11).
In general, antagonist muscle segments tended to have delayed onsets, shorter periods of activity and lower contraction intensities than the prime mover segments (e.g. D7 in shoulder abduction; D6 during shoulder adduction and L1 during shoulder flexion) (Table 3, Table 4 and Table 5). An exception was segment P3 (Pectoralis Major) during shoulder extension which was co-activated with the prime mover segments of the Latissimus Dorsi (Table 6). This was an unexpected result given that numerous reports [11] and [15] of “triphasic” muscle activation patterns during rapid isometric motor tasks have suggested that the antagonist (Ant) muscle burst is always activated after the initial agonist (Ag1) period of activation.
However, the involvement of antagonist muscle segments in these rapid isometric motor tasks is consistent with the findings of Flanders and Soechting [6] who state that antagonist muscle activity, in part, is important to counteract internal joint forces which may cause tissue damage.
In general these results, obtained from the superficial shoulder muscle group, broadly support the previous findings of Wickham and Brown [24] for the Deltoid muscle. These findings, with notable exceptions to these generalisations, will now be discussed in more detail with reference to each movement direction.
4.3. Influence of movement direction
The most simple motor control strategies were employed by the CNS during the shoulder abduction task (Table 3). Here the middle muscle segments of the Deltoid (D3 and D4) were found to have the most favourable mechanical lines of action and the greatest moment arms to produce shoulder abduction in the coronal plane. Shoulder abduction was initiated by activation of the prime mover segments D3 and D4. These segments, along with the adjacent segments D2 and D5, had the longest periods of activation and the highest intensities of contraction within the Deltoid muscle. The more peripheral and divergent segments of this muscle, D1, D6 and D7, all had later onsets, shorter periods of activation and lower contraction intensities reflecting their less favourable mechanical lines of action and smaller abduction moment arms (Table 2).
Interestingly, segment D7 on the postero-medial aspect of the Deltoid was found uniquely to have an antagonist moment arm for shoulder abduction. Accordingly, its period of activation was very late (e.g. 34 ms after FcON), short and of low intensity. Although D7 was anatomically contingent with segment D6, it is clearly seen that the CNS controlled the motor units of D7 independently of those within D6. The difference in moment arms between D7 (antagonist ma = −10.5 mm) and D6 (agonist ma = +8.2 mm) for the shoulder abduction task appeared to explain their contrasting periods of activity.
A more complicated and difficult to explain muscle segment control strategy was seen during shoulder adduction (Table 4). This motor task involved all three superficial muscles including segments of the Deltoid muscle (Fig. 6) – a muscle which Hughes and Kai-Nan [9] had previously predicted should have had no activity for this motor task.
Shoulder adduction was initiated by activation of the entire Latissimus Dorsi (L1–L6), some 52 ms (group mean) before the initial rise of the force–time curve (FcON) (Fig. 6). Therefore, all segments of the Latissimus Dorsi could be considered prime mover segments although their mechanical lines of action and adduction moment arms were variable (Table 1). In contrast, the segments of the Pectoralis Major were all activated as synergists with the lower fibres (P4–P6) and then the upper fibres (P1–P3) being activated in sequence (Table 4). The utilisation of all segments of the Latissimus Dorsi as the prime movers for shoulder adduction, in preference to those of the Pectoralis Major, was an unexpected result which was difficult to explain. Both muscles have large adductor moment arms (Table 2) and muscle segments with effective mechanical lines of action for the motor task. Both muscles also insert into the bicipital groove [7] and have similar cross-sectional areas (Table 1). Possibly the more posterior orientation of the Latissimus Dorsi muscle segments afforded biomechanical advantages to the CNS in the initiation of this motor task. However, further work is required before this result can be fully explained.
During shoulder adduction, all segments of the antagonist Deltoid muscle were myoelectrically silent except for segments D6 (antagonist ma = −8 mm) and D7 (agonist ma = +10.5 mm) (Fig. 6 and Table 4). The onset of segment D7 activation suggested a synergist function, with the lower fibres of the Pectoralis Major (P4–P6), to assist production of the adduction force impulse. In contrast, segment D6 clearly functioned as an antagonist to the motor task. D6 was coactivated with the fibres of the Pectoralis Major although only at a very low (28% MVC) intensity of activation. Similar findings were made by Flanders and Soechting [6] who noted, in the posterior (and medial) Deltoid during isometric motor tasks, that motor units may be directionally tuned in opposite movement directions within the same muscle segment.
Muscle segment function during shoulder flexion and shoulder extension appeared as a mirror image. During shoulder flexion (Table 5), the clavicular head of Pectoralis Major (P1 and P2), along with the anterior head of the Deltoid (D1 and D2), acted as the prime mover segments. All four segments had good mechanical lines of action and large moment arms for the shoulder flexion task (agonist ma = +18 mm to +53 mm). The lower fibres of Pectoralis Major (P3–P6) and the middle fibres of the Deltoid (D3–D4) then acted as synergist segments. These segments all had more divergent mechanical lines of action although their flexion moment arms were still impressive (e.g., P3 agonist ma = 50 mm; P4 agonist ma = 32 mm) (Table 2). It is interesting to note in this motor task that muscle segments with very large agonist moment arms (e.g. P3 and P4) were not necessarily activated as prime mover segments if their mechanical lines of action were too divergent from movement direction.
With an antagonist moment arm of −60 mm, segment L1 was the only segment of the Latissimus Dorsi to be active during the shoulder flexion task. Its late activation, shorter duration of activity and low intensity of activation clearly defined this segment’s antagonist role (Table 5). The horizontal orientation of its muscle fibres may have also produced an optimal ability to oppose the forward translatory motion of the humerus during the flexion motor task.
In contrast shoulder extension (Table 6) was initiated by the upper fibres of Latissimus Dorsi (L1–L4) and two segments of the Deltoid (D5 and D7) (Fig. 11). Again these prime mover segments had good mechanical lines of action for shoulder extension and large extension moment arms (ma range = +63 mm (D7) to +31 mm (L4)) (Table 2). The synergist segments (L5, L6, D6 and D4) were then activated to complete the motor task. Again, these synergist segments had more divergent mechanical lines of action and generally smaller extension moment arms (ma range = +50 mm to +21 mm).
Two antagonist muscle segments were activated during shoulder extension. Segment D3 of the Deltoid, with an antagonist moment arm of −8.3 mm, was activated after the prime mover segments. Its late activation, shorter duration of activity and lower intensity of activation (33% MVC), clearly reflected its antagonist role. In contrast segment P3 of the Pectoralis Major, with an antagonist moment arm of −50 mm, had an onset similar to the prime mover segments. As seen in Table 6, segment P3 was co-activated with the prime mover segments L1–L4, D5 and D7. Its peak intensity and duration of activity (Table 6) were also similar to the prime mover segments although its intensity of activation was significantly (p < 0.05) lower at 11% of MVC. It is difficult to explain why this particular antagonist muscle segment, the only segment of the Pectoralis Major to be activated during shoulder extension, should have such an early activation although its horizontal muscle fibre orientation may be implicated. Activation of the P3 segment may have been required early to protect the anterior shoulder from injury during the vigorous activation (approximately 73% of MVC group mean) of the prime mover segments; a role commonly given to antagonist muscle action [6]. If this hypothesis is true, it is evident that the CNS has considerable flexibility regarding the timing of antagonist muscle activity during the production of motor tasks.
With regard to the peak of muscle segment activation, it is clear that for all muscle segments involved in the four motor tasks investigated, maximal motor unit activation occurred before the peak of the isometric force–time curve. In general, prime mover segments had earlier peak intensities when compared to synergist segments although this was not always the case. There was, however, some limited evidence to suggest that the peak activation of some antagonist muscle segments was significantly (p < 0.05) later than the agonist muscle segments (Table 3).
4.4. Motor unit task groups
It was evident that to produce each of the four movement tasks, motor unit task groups were formed both within, and where appropriate, across the three shoulder muscles, and then activated (timing and intensity) sequentially to produce the movement task. Motor unit task groups may be defined as a group of motor units, from within a muscle or across several muscles, which are active simultaneously for a particular motor task [14]. It is thought that differences in moment arms, or physiological factors such as fibre type, may explain the existence of motor unit task groups, and therefore functionally independent muscle segments within muscle [5].
In the present study, each motor task was accomplished through the formation of at least two, and up to four, different motor unit task groups which often comprised motor units from adjacent, and more distant, muscles. For example, during shoulder abduction two motor unit task groups were formed within the Deltoid to achieve the motor task. The first motor unit task group formed included the prime mover segments (D3, D4), a common feature in all movement tasks in this study. A second motor unit task group was then formed by the remaining synergist and antagonist segments (D1, D2, D5, D6 and D7) which all had smaller abduction moment arms, or in the case of D7, an adduction moment arm. Contrary to the hypothesis of Flanders and Soechting [6], there was no evidence to suggest that the motor units of the middle (D3) and posterior (D4–D7) Deltoid were tightly coupled during this motor task.
Shoulder adduction was accomplished with the formation of three motor unit task groups. The first contained all motor units within the Latissimus Dorsi muscle which acted together as the prime movers for the motor task. A second group was formed by motor units within the lower fibres of Pectoralis Major along with the agonist segment D7 of the Deltoid. A third group was formed by motor units within the upper fibres of the Pectoralis Major along with the antagonist D6 segment of the Deltoid. Fig. 8 clearly shows the three motor unit task groups and confirms that the activation of segments (motor units) within each task group was sequential away from muscle segments with higher agonist moment arms.
Two motor unit task groups were formed during shoulder flexion while three were formed during shoulder extension. In both movement tasks, the first group contained the prime mover segments while the second comprised synergist segments. All motor unit task groups contained motor units from a number of muscles. The antagonist segments either formed their own motor unit task group (shoulder extension) or were distributed either to the first (shoulder extension) or the second (shoulder flexion) motor unit task group.
4.5. Muscle segment function and the CNS
The production of muscle force is a product of moment arm, muscle size, the muscle’s length tension relationship as well as the timing and intensity of motor unit activation; the latter controlled by the CNS [12]. Our results support the suggestion that the CNS, through its upper and lower motoneurons, has the flexibility to “fine tune” and coordinate the timing and intensity of motor unit activity both within a single muscle and between adjacent and more distant muscles, to meet the intended goals of the motor task.
It has been previously demonstrated, in monkey cortex, that pyramidal tract neurons from layer 5 of M1 (the primary motor cortex) directly innervate lower motor neurons in layer IX of the spinal cord [20]. These are the motoneurons which have direct control over the activation of a muscle’s constituent fibres.
Given that there is a proven relationship between the activity of upper motoneurons within a cortical column, and the subsequent EMG activity within an active muscle [17], the results of this study may be used to gain further insight into the strategies used by the CNS to control voluntary movement.
Specifically, our study supports the contention that specific motor columns within the human M1 (primary motor cortex), have the ability to independently control discrete subpopulations of motor units within a single skeletal muscle. This has previously only been confirmed in animal studies [13] and [17]. Therefore, our results give further insight into the complexity of the task faced by the CNS to control each and every muscle involved in even the most simple of motor tasks.
4.6. Limitations
Several limitations in the experimental design may have influenced the results.
Firstly, it should not be concluded that the 19 muscle segments identified in this study represented the “ultimate” design imposed by the CNS. In some instances (e.g. Latissimus Dorsi), the anatomical borders of each muscle segment were found by simple division of relatively homogenous muscle tissue. Even when the muscle segments were clearly defined anatomically (e.g. Deltoid), it may be possible that each segment could be further subdivided into ever smaller functional units. It is not beyond possibility that the “ultimate muscle segment” would be represented by a single muscle spindle and its associated muscle fibers! However, it remains probable that similar findings, to those found here, would have been found if fewer, or more, muscle segments had been investigate. The exciting possibility now exists for the application of a multi-electrode fine-wire EMG technique, to an in vitro analysis of animal muscle, whereby more muscle segments may be investigated and greater clarity provided to their neuromuscular control.
A second limitation was the problem of crosstalk between adjacent bipolar electrode pairs. If detectable levels of crosstalk were present, the ability to differentiate between the activity of adjacent muscle segments would be compromised. Considerable effort was made to minimize the effects of electrode crosstalk. The bipolar electrodes were specifically designed to have small active plates (1.6 mm in diameter) and inter-electrode distances (6.5 mm). This electrode design, using the crosstalk “rule of thumb” reported by Basmajian and DeLuca [1], would suggest meaningful pickup of muscle fiber activity only within approximately 6.5 mm of each bipolar electrode pair. Adjacent bipolar electrode pairs were generally spaced more than 2 cm from each other so as to minimize, as much as practicable, electrode crosstalk. In addition, regardless of possible electrode crosstalk, the results presented here provide strong evidence of the sequential activation of adjacent muscle segments to control these isometric tasks (Fig. 8). It would have been expected that high levels of electrode crosstalk would have negated the possibility of this result.
5. Conclusion
The aim of this study was to determine how 19 muscle segments within the Latissimus Dorsi, Deltoid and Pectoralis Major, were controlled by the CNS to produce four isometric shoulder motor tasks.
The results of this investigation have suggested that the timing and intensity of each muscle segment’s activation were coordinated across muscles and influenced by the muscle segment’s moment arm and its mechanical line of action in relation to the intended shoulder movement direction (e.g. flexion, extension, abduction or adduction). There was also evidence that motor unit task groups were formed for individual motor tasks which comprised motor units from both adjacent and distant muscles. In addition, the results supported the hypothesis that individual muscles segments may be functionally classified as prime mover, synergist or antagonist; functional classifications which were generally determined by the muscles segments moment arm and/or mechanical line of action.
Acknowledgements
The authors wish to thank the University of Wollongong for technical and financial support to Dr. Wickham during his doctoral studies and to Dr. Brown during his sabbatical leave in Germany. Thank you also to Mr. Luke Bones and Mr. Daniel Wickham for assistance with preparation of the illustrations and to the reviewers for the excellent comments and suggestions. The work described in this study was approved by the Human Ethics Committee of the University of Wollongong.
References
[1] J.V. Basmajian and C. DeLuca, Muscles alive; their functions revealed by electromyography (5th ed.), Williams & Wilkins, Baltimore (1985).
[2] J.M.M. Brown, C. Solomon and M.E. Paton, Further evidence of functional differentiation within biceps brachii, Electromyograph Clin Neurophysiol 33 (1993), pp. 301–309. View Record in Scopus | Cited By in Scopus (11)
[3] K.M. Campbell, B.A. Norman, L. Biggs, P.L. Blanton and R.P. Lehr, Electromyographic investigation of the relative activity among four components of the triceps surae, Am J Phys Med 52 (1973) (1), pp. 30–41. View Record in Scopus | Cited By in Scopus (14)
[4] Enoka RM. The neuromechanical basis of kinesiology, 2nd ed. In: Human kinetics, 1994.
[5] G.J.C. Ettema, G. Styles and V. Kippers, The moment arms of 23 muscle segments of the upper limb with varying elbow and forearm positions: Implications for motor control, Human Movement Sci 17 (1998) (2), pp. 201–220. Abstract | Article | PDF (268 K) | View Record in Scopus | Cited By in Scopus (29)
[6] M. Flanders and J.F. Soechting, Arm muscle activation for static forces in three-dimensional space, J Neurophysiol 64 (1990) (6), pp. 1818–1837. View Record in Scopus | Cited By in Scopus (65)
[7] Gray’s Anatomy, The anatomical basis of medicine and surgery, Churchill Livingstone, Sydney (1990).
[8] C. Hogfors, G. Sigholm and P. Herberts, Biomechanical model of the human shoulder – I. Elements, J Biomech 20 (1987) (2), pp. 157–166. Abstract | PDF (1082 K) | View Record in Scopus | Cited By in Scopus (52)
[9] R.E. Hughes and A. Kai-Nan, Force analysis of rotator cuff muscles, Clin Orthopaed Related Res 1 (1996) (330), pp. 75–83. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (45)
[10] D.B. Jenkins,Hollinshead’s functional anatomy of the limbs and back (7th ed.), W.B. Saunders, Sydney (1998).
[11] G.M. Karst and Z. Hassan, Antagonist muscle activity during forearm movements under varying kinematic and loading conditions, Exp Brain Res 67 (1987), pp. 391–401. View Record in Scopus | Cited By in Scopus (35)
[12] D.K. Kuechle, S.R. Newman, E. Itoi, G.L. Niebur, B.F. Morrey and K-N. An, The relevance of the moment arm of shoulder muscles with respect to axial rotation of the glenohumeral joint in four positions, Clin Biomech 15 (2000) (5), pp. 322–329. Abstract | Article | PDF (383 K) | View Record in Scopus | Cited By in Scopus (28)
[13] R. Lemon, The output map of the primate motor cortex, Trends Neurosci 11 (1988), pp. 501–506 1989, erratum appears in Trends Neurosci Apr;12(4):158.. Abstract | PDF (748 K) | View Record in Scopus | Cited By in Scopus (48)
[14] G.E. Loeb, Motorneuron task groups: Coping with kinematic heterogeneity, J Exp Biol 115 (1985), pp. 137–146. View Record in Scopus | Cited By in Scopus (47)
[15] C.D. MacKinnon and J.C. Rothwell, Time-varying changes in corticospinal excitability accompanying the triphasic EMG pattern, J. Physiol. 506P (1998), p. 114P.
[16] Y. Manueddu, W. Blanc and W. Taillard, Study of the functioning of the Gluteus Medius and Maximus: An electromyographic analysis, Ann Kinesither 16 (1989), pp. 193–201.
[17] R.B. Muir and R.N. Lemon, Corticospinal neurons with a special role in precision grip, Brain Res 61 (1983), pp. 312–316. Abstract | PDF (393 K) | View Record in Scopus | Cited By in Scopus (105)
[18] E.B. Pare, J.R. Stern and J.M. Schwartz, Functional differentiation within the tensor fascia latae, J Bone Joint Surg A 63 (1981) (9), pp. 239–246.
[19] M.E. Paton and J.M.M. Brown, An electromyographic analysis of functional differentiation in human pectoralis major muscle, J Electromyograph Kinesiol 4 (1994) (3), pp. 161–169. Abstract | PDF (943 K) | View Record in Scopus | Cited By in Scopus (12)
[20] Y. Shinoda, J. Yokota and T. Futami, Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey, Neurosci Lett 23 (1981), pp. 7–12. Abstract | PDF (808 K) | View Record in Scopus | Cited By in Scopus (84)
[21] G.L. Soderberg and W.F. Dostal, Electromyographic study of three parts of the gluteus medius muscle during functional activities, Phys Therapy 58 (1978) (6), pp. 691–696. View Record in Scopus | Cited By in Scopus (23)
[22] H.E.V. Veeger, F.C.T. VanDerHelm, L.H.V. VanDerWoude, G.M. Pronk and R.H. Rozendal, Inertia and muscle contraction parameters for musculoskeletal modelling of the shoulder mechanism, J Biomech 24 (1991) (7), pp. 615–629. Abstract | PDF (2423 K) | View Record in Scopus | Cited By in Scopus (80)
[23] Wickham JB. Muscles within Muscles: The neuromotor activation patterns of intramuscular segments. PhD thesis, Department of Biomedical Science, University of Wollongong, 2002.
[24] J.B. Wickham and J.M.M. Brown, Muscles within muscles: the neuromotor control of intra-muscular segments, Eur J Appl Physiol 78 (1998), pp. 219–225. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (24)
[25] J.B. Wickham, J.M.M. Brown and D.J. McAndrew, Muscles within muscles: Anatomical and functional segmentation of selected shoulder joint musculature, J Musculoskeletal Res 8 (2004) (1), pp. 57–73. Full Text via CrossRef | View Record in Scopus | Cited By in Scopus (5)
