| | Muscles within muscles: Coordination of 19 muscle segments within three shoulder muscles during isometric motor tasksReceived 10 April 2005; received in revised form 24 September 2005; accepted 26 October 2005. published online 03 February 2006. 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], [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. 400ms 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. Each subject performed four isometric tasks; shoulder-abduction, -adduction, -flexion and -extension, at 75% of MVC, a movement time (MT) approximating 400ms and with an inter-trial period of at least 30s. 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 3min. 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 (6.5mm inter-electrode distance; 1.6mm 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). Electrode gel was injected into the electrode wells by utilising a syringe coupled to a 1mm 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 1×1013Ω, CMRR of 110db, signal to noise ratio of 1000:1, 1000k gain). The raw EMG signals were amplified and filtered (10Hz high pass and 1kHz 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 1kHz. A 2000ms recording period, commencing at least 200ms 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. 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 20Hz 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 (10ms 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 0.01mm), 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. 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: 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 3.2. 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, 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 40ms 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 34ms after the initial rise of the force impulse. | | |  | | On (ms) | Peak (ms) | Duration (ms) | Intensity (%MVC) | |
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| | x | s.d. | x | s.d. | x | s.d. | x | s.d. | |
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| D1 | −04∗ | 26 | −68 | 43 | 554∗ | 96 | 38∗ | 24 | | | D2 | −35∗ | 19 | −85 | 58 | 617 | 87 | 83 | 33 | | | D3 | −53 | 19 | −82 | 37 | 636 | 76 | 87 | 17 | | | D4 | −42 | 23 | −81 | 31 | 657 | 96 | 88 | 20 | | | D5 | −24∗ | 24 | −59 | 31 | 624 | 81 | 73 | 23 | | | D6 | −05∗ | 21 | −66 | 41 | 560∗ | 84 | 58∗ | 30 | | | D7 | 34∗ | 26 | −26∗ | 66 | 528∗ | 70 | 51∗ | 30 | | | | |
The timing of peak myoelectric activity was identical in segments D1–D6 occurring, on average, some 74ms 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 26ms 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=408ms) (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, Fig. 8). 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 7ms before FcON (Table 4). | | | | | On (ms) | Peak (ms) | Duration (ms) | Intensity (%MVC) | |
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| | x | s.d. | x | s.d. | x | s.d. | x | s.d. | |
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| P6 | −24 ▴ | 37 | −61 ▴ | 40 | 587 | 119 | 62 | 15 | | | P5 | −25 ▴ | 26 | −72 ▴ | 51 | 588 | 153 | 66 | 20 | | | P4 | −15 ▴ | 23 | −58 ▴ | 51 | 579 | 112 | 56 | 19 | | | P3 | 11 ▴∗ | 36 | −53 ▴ | 31 | 540 | 107 | 41 ▴ | 18 | | | P2 | 21 ▴∗ | 48 | −56 ▴ | 34 | 511 ▴∗ | 100 | 34 ▴∗ | 18 | | | P1 | 26 ▴∗ | 34 | −50 ▴ | 47 | 498 ▴∗ | 83 | 33 ▴∗ | 26 | | | | | | | | | | | | | | D1 | | | | | | | | | | | D2 | | | | | | | | | | | D3 | | | | | | | | | | | D4 | | | | | | | | | | | D5 | | | | | | | | | | | D6 | 22 ▴# | 46 | −62 ▴ | 46 | 477 ▴ | 133 | 28 ▴ | 18 | | | D7 | −7 ▴ | 28 | −70 ▴ | 35 | 536 | 89 | 47 ▴ | 36 | | | | | | | | | | | | | | L1 | −43 | 23 | −87 ▴∧ | 53 | 612 | 109 | 55 | 34 | | | L2 | −53 | 32 | −100 | 52 | 601 | 99 | 56 | 22 | | | L3 | −66 | 30 | −132 | 56 | 600 | 112 | 79 | 39 | | | L4 | −58 | 25 | −128 | 75 | 594 | 123 | 67 | 24 | | | L5 | −48 | 28 | −86 ▴∧ | 46 | 594 | 130 | 64 | 25 | | | L6 | −46 | 25 | −109 | 35 | 596 | 134 | 70 | 31 | | | | |
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 −117ms) than all other muscle segments (approximately −65ms) investigated (Table 4). The duration of muscle segment activation was found to be longest in segments L1–L6, D7 and P3–P6 (approximately 584ms). Segments P1, P2 and D6 were all found to have significantly (p<0.05) shorter periods of activation (approximately 495ms) during this task (Table 4). All active muscle segments had periods of activity longer than adduction movement time of 390ms (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). 3.4. Shoulder flexion 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, 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). | | | | | On (ms) | Peak (ms) | Duration (ms) | Intensity (%MVC) | |
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| | x | s.d. | x | s.d. | x | s.d. | x | s.d. | |
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| P6 | | | | | | | | | | | P5 | | | | | | | | | | | P4 | | | | | | | | | | | P3 | −34 | 19 | −83 | 57 | 629 | 51 | 11 ▴ | 29 | | | P2 | | | | | | | | | | | P1 | | | | | | | | | | | | | | | | | | | | | | D1 | | | | | | | | | | | D2 | | | | | | | | | | | D3 | 43 ▴# | 27 | −45 ▴ | 57 | 574 ▶ | 116 | 33 ▴# | 10 | | | D4 | −5 ▴ | 29 | −53 ▴ | 49 | 622 | 126 | 50 ▴# | 17 | | | D5 | −25 | 27 | −60 ▴ | 36 | 641 | 99 | 63# | 14 | | | D6 | −14 ▴ | 30 | −79 ▴ | 48 | 595 | 87 | 81 | 25 | | | D7 | −37 | 30 | −62 ▴ | 39 | 637 | 100 | 84 | 30 | | | | | | | | | | | | | | L1 | −45 | 28 | −62 ▴∧ | 46 | 670 | 135 | 58 ▴ | 22 | | | L2 | −39 | 27 | −80 ▴∧ | 44 | 633 | 127 | 67 | 19 | | | L3 | −49 | 31 | −126 | 71 | 664 | 155 | 71 | 31 | | | L4 | −28 | 25 | −78 ▴∧ | 61 | 624 | 74 | 59 ▴ | 13 | | | L5 | −7 ▴∧ | 45 | −61 ▴∧ | 31 | 608 | 96 | 42 ▴∧ | 20 | | | L6 | 3 ▴∧ | 39 | −92 | 56 | 612 | 73 | 43 ▴∧ | 15 | | | | |
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 100ms prior to FcPK compared to between 60ms and 70ms 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 630ms). Segment D3 had a significantly (p<0.05) shorter duration of activation (approximately 574ms) although all active muscle segments were activated longer than movement time (MT=430ms) (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], [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, 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, 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], [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. 34ms 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=−10.5mm) and D6 (agonist ma=+8.2mm) 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 52ms (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=−8mm) and D7 (agonist ma=+10.5mm) (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=+18mm to +53mm). 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=50mm; P4 agonist ma=32mm) (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 −60mm, 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=+63mm (D7) to +31mm (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=+50mm to +21mm). Two antagonist muscle segments were activated during shoulder extension. Segment D3 of the Deltoid, with an antagonist moment arm of −8.3mm, 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 −50mm, 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], [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 (1.6mm in diameter) and inter-electrode distances (6.5mm). 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 6.5mm of each bipolar electrode pair. Adjacent bipolar electrode pairs were generally spaced more than 2cm 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]. [1]Basmajian JV, DeLuca C. Muscles alive; their functions revealed by electromyography. 5th ed.. Baltimore: Williams & Wilkins; 1985;. [2]. [2]Brown JMM, Solomon C, Paton ME. Further evidence of functional differentiation within biceps brachii. Electromyograph Clin Neurophysiol. 1993;33:301–309. [3]. [3]Campbell KM, Norman BA, Biggs L, Blanton PL, Lehr RP. Electromyographic investigation of the relative activity among four components of the triceps surae. Am J Phys Med. 1973;52(1):30–41. 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[25]. [25]Wickham JB, Brown JMM, McAndrew DJ. Muscles within muscles: Anatomical and functional segmentation of selected shoulder joint musculature. J Musculoskeletal Res. 2004;8(1):57–73.  Mark Brown has a Doctoral qualification from the University of Queensland and is currently a Senior Lecturer and Assistant Dean at the University of Wollongong. He was Head of the Department of Biomedical Science between 1997 and 2001 and is the immediate past Vice President (exercise science) of Australia’s professional Exercise Science association (AAESS). His research interests include functional segmentation of skeletal muscle and sustainable transport.  James Wickham received a Bachelor of Sports Science (exercise science) from the University of New South Wales in 1992 and a Diploma of Education (physical education) in 1993 from the same institution. In 1995 he received an Honours Degree from the University of Wollongong and a PhD in 2002. Since 1999 James has been employed as an Anatomy Lecturer at La Trobe University in Melbourne. His research interests include using electromyography to quantify shoulder muscle activation patterns and functional differentiation within skeletal muscles.  Darryl McAndrew received a Bachelor of Science (Human Movement Science) from the University of Wollongong in 1993 and is currently an Associate Lecturer within the Department of Biomedical Science, UoW. He is concurrently completing a PhD focusing on the fibre type characteristics of segmental muscle and a M.Sc. in OH & S, specialising in Occupational Hygeine. His research interests include identifying muscle fibre type characteristics via mechanomyography and occupational exposure to industrial noise.  Xu-Feng Huang received his PhD degree from the University of New South Wales in 1992. He is currently an Associate Professor in the Department of Biomedical Science and the Director of Neurobiology Research Centre for Metabolic and Psychiatric Disorders in the University of Wollongong. His research interest includes the central regulation of energy balance. a Department of Biomedical Science, University of Wollongong, Wollongong 2500, Australia b Department of Anatomy and Physiology, School of Human Biosciences, La Trobe University, Vic. 3086, Australia  Corresponding author. Tel.: +61 3 94795725; fax: +61 3 94795784.
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