Intra- and intermuscular variation in human quadriceps femoris architecture assessed in vivo

Abstract

Despite the functional importance of the human quadriceps femoris in movements such as running, jumping, lifting and climbing, and the known effects of muscle architecture on muscle function, no research has fully described the complex architecture of this muscle group. We used ultrasound imaging techniques to measure muscle thickness, fascicle angle and fascicle length at multiple regions of the four quadriceps muscles in vivo in 31 recreationally active, but non-strength-trained adult men and women. Our analyses revealed a reasonable similarity in the superficial quadriceps muscles, which is suggestive of functional similarity (at least during the uni-joint knee extension task) given that they act via a common tendon. The deep vastus intermedius (VI) is architecturally dissimilar and therefore probably serves a different function(s). Architecture varies significantly along the length of the superficial muscles, which has implications for the accuracy of models that assume a constant intramuscular architecture. It might also have consequences for the efficiency of intra- and intermuscular force transmission. Our results provide some evidence that subjects with a given architecture of one superficial muscle, relative to the rest of the subject sample, also have a similar architecture in other superficial muscles. However, this is not necessarily true for vastus lateralis (VL), and was not the case for VI. Therefore, the relative architecture of one muscle cannot confidently be used to estimate the relative architecture of another. To confirm this, we calculated a value of whole quadriceps architecture by four different methods. Regardless of the method used, we found that the absolute or relative architecture of one muscle could not be used as an indicator of whole quadriceps architecture, although vastus medialis, possibly in concert with VL and the anterior portion of VI, could be used to provide a useful snapshot. Importantly, our estimates of whole quadriceps architecture show a gender difference in whole quadriceps muscle thickness, and that muscle thickness is positively correlated with fascicle angle whereas fascicle length is negatively, although weakly, correlated with fascicle angle. These results are supportive of the validity of estimates of whole quadriceps architecture. These data are interpreted with respect to their implications for neural control strategies, region-specific adaptations in muscle size in response to training, and gender-dependent differences in the response to exercise training.

Figures

Fig 1

Quadriceps femoris scanning sites. Sonographs were obtained at lengths equivalent to 5–73% of thigh length measured from the superior border of the patella to the anterior superior iliac spine. Muscles were scanned at three sites as indicated in the diagram above. The anterior portion of vastus intermedius (VIant, not shown) was scanned at the same sites as RF, while the lateral portion (VIlat) was scanned as per VL; thus, direct comparison can be made between sites 1 and 2 of the anterior portion with sites 2 and 3 on the lateral portion. VL: vastus lateralis, VM: vastus medialis, RF: rectus femoris, VIant: vastus intermedius (anterior portion), VIlat: vastus intermedius (lateral portion). Solid bars show the approximate transducer angles used to obtain images parallel to the fascicles on VL, VM and RF (VI not shown).

Fig 2

Sagittal plane ultrasound scan of vastus lateralis (VL) and the lateral portion of vastus intermedius (VIlat). Landmarks corresponding to aponeuroses (points 1–4) and fascicles (points 5–6) were digitized (see Methods), as in the image above. Muscle thickness was calculated as the mean of the vertical distances between points 1–3 and 2–4. Fascicle angle, measured from 3 to 4 mm above the deep aponeurosis (dashed line) to mid-muscle was calculated as the angle between points 2–4 and 5–6. Aponeurosis angle was calculated as the positive angle between points 3–4 and 1–2.

Fig 3

Intramuscular architecture of the quadriceps femoris. Fascicle angles [measured between the aponeurosis (a) and the fascicle (f)] vary considerably along the lengths of VL, VM and RF, but are relatively constant in VI; the magnitude of fascicle angle is represented as depth of colour and gradient of the representative fascicle (dotted line). Example sonographs are shown immediately below each muscle. Muscle thickness is also relatively variable in VL, VM and RF, but not in VI; muscle thickness is drawn to scale. Distal VM thickness was not measured in the present study so an estimate has been used to aid readability. RF is shown as a shorter muscle than the vastii muscles; however, muscle lengths are not drawn to scale.

Fig 4

Effect of intermuscular fascicle length and angle differences on tendon/aponeurosis excursion. When rectus femoris (RF) fascicles shorten (from FLRF1 to FLRF2, where FL is the fascicle length) and rotate (θRF1 to θRF2, where θ is the fascicle angle) in this example, the aponeurosis or tendon displaces 10 mm. This represents a fascicle shortening of 9.7 mm, or 8.7%. If the vastus intermedius (VI; anterior region) fascicle shortens by the same proportion, 14.0 mm, or 8.7%, and rotates, the aponeurosis or tendon displaces 14.2 mm, which is a difference (Diff.) of 4.2 mm, or 42%. Thus, even when fascicle rotation is accounted for, the differing architectures of RF and VI result in differential displacement of the tendon or aponeurosis. Either RF and VI must be activated uniquely, or there will be a shear force in the tendon or aponeurosis. In this example, it was assumed that the muscle thickness would remain constant given that RF and VI apply opposing forces of similar magnitude on the tendon/aponeurosis.

Fig 5

A planimetric muscle model was constructed, according to Appendix A. The muscle consisted of three segments which were either identical in their architecture (non-varying architecture, A), varied according to normal data for the VL collected in the present study (varying architecture, B), or varied more considerably in the proximal and distal segments than the measurements in the present study (i.e. mean minus 1 SD) (varying architecture, C). Muscle thickness (MT) and fascicle angle (θ) parameters used in the model are shown (parameters correspond to muscle optimum length). As shown in the graph of muscle force vs. muscle length (D), modelling the muscle as three distinct segments makes a relatively small difference to the output of the model when architecture varies only moderately (A vs. B). However, when the muscle's architecture varies considerably (A vs. C), the ability for a uniform muscle model to predict muscle force is significantly reduced.

Fig 6

Relationships between whole quadriceps muscle thickness and fascicle angle (top graph: a), and fascicle angle and fascicle length (bottom graph: b). Whole quadriceps architecture in these examples was calculated by the equal ratio method (see Methods), which was associated with the lowest correlations between the variables when compared with PCSA, volume and estimated contribution methods. Muscle thickness and fascicle angle were positively correlated, while fascicle angle and fascicle length were negatively correlated. Magnitudes are presented as z-scores.