A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture

Abstract

1. In human pennate muscle, changes in anatomical cross-sectional area (CSA) or volume caused by training or inactivity may not necessarily reflect the change in physiological CSA, and thereby in maximal contractile force, since a simultaneous change in muscle fibre pennation angle could also occur. 2. Eleven male subjects undertook 14 weeks of heavy-resistance strength training of the lower limb muscles. Before and after training anatomical CSA and volume of the human quadriceps femoris muscle were assessed by use of magnetic resonance imaging (MRI), muscle fibre pennation angle (theta(p)) was measured in the vastus lateralis (VL) by use of ultrasonography, and muscle fibre CSA (CSA(fibre)) was obtained by needle biopsy sampling in VL. 3. Anatomical muscle CSA and volume increased with training from 77.5 +/- 3.0 to 85.0 +/- 2.7 cm(2) and 1676 +/- 63 to 1841 +/- 57 cm(3), respectively (+/- S.E.M.). Furthermore, VL pennation angle increased from 8.0 +/- 0.4 to 10.7 +/- 0.6 deg and CSA(fibre) increased from 3754 +/- 271 to 4238 +/- 202 microm (2). Isometric quadriceps strength increased from 282.6 +/- 11.7 to 327.0 +/- 12.4 N m. 4. A positive relationship was observed between theta(p) and quadriceps volume prior to training (r = 0.622). Multifactor regression analysis revealed a stronger relationship when theta(p) and CSA(fibre) were combined (R = 0.728). Post-training increases in CSA(fibre) were related to the increase in quadriceps volume (r = 0.749). 5. Myosin heavy chain (MHC) isoform distribution (type I and II) remained unaltered with training. 6. VL muscle fibre pennation angle was observed to increase in response to resistance training. This allowed single muscle fibre CSA and maximal contractile strength to increase more (+16 %) than anatomical muscle CSA and volume (+10 %). 7. Collectively, the present data suggest that the morphology, architecture and contractile capacity of human pennate muscle are interrelated, in vivo. This interaction seems to include the specific adaptation responses evoked by intensive resistance training.

Figure 1

Sagital ultrasound image obtained in the quadriceps femoris muscle at 50 % femur length. VL muscle fibre pennation angle (θ_p) was determined as the angle between vastus lateralis muscle fibre fascicles and the deep aponeurosis separating vastus lateralis and vastus intermedius.

Figure 3

Axial MRI images of the thigh obtained at 50 % femur length (proximal slice, bottom panel) and 30 % femur length (distal slice, top panel). Axial images were obtained at 20, 30, 40, 50, 60, 70 and 80 % femur length, before and after the period of training. Quadriceps femoris muscle volume was calculated by stacking of successive axial images.

Figure 2

Muscle biopsy cross section stained for myofibrillar ATPase after preincubation at pH 4.6. Type I, IIA and IIX muscle fibers are marked for illustration. Type I and II muscle fibre area, average fibre area, fiber type composition and myosin heavy chain (MHC) isoform composition was determined before and after the period of resistance training.

Figure 4

Muscle fibre pennation angle obtained in vastus lateralis at 50 % femur length by use of ultrasound sonography imaging, before and after the period of training. Open symbols and column show pre-training individual values and group mean value, respectively, and s.e.m. is indicated by error bars. Closed symbols and hatched column show post-training values. Pre- to post-training differences, **P < 0.001.

Figure 5

Single muscle fibre cross-sectional area, (CSA), before and after the period of training. A, average muscle fibre CSA, B, type I fibre CSA, C, type II fibre CSA. CSA_fibre was measured in biopsy samples obtained from the vastus lateralis muscle. Open symbols/column show pre-training individual values and group mean value, respectively, and s.e.m. is indicated by error bars. Filled symbols and the hatched column show post-training values. Pre- to post-training differences: **P < 0.001. A trend towards an increase in type I fibre CSA was observed post training (P = 0.074).

Figure 6

Anatomical quadriceps muscle CSA measured at 50 % femur length by use of MRI, before and after the period of training. Open symbols show individual values, open column shows group mean value prior to training, and s.e.m. is indicated by error bars. Filled symbols and hatched column show individual values and group mean value, respectively, following training (n = 11). Pre- to post-training differences: **P < 0.001.

Figure 7

Quadriceps muscle volume measured by MRI. Open symbols and column show pre-training individual values and group mean value, respectively, and s.e.m. is indicated by error bars. Filled symbols and hatched column show post training values. Pre- to post-training differences: **P < 0.001.

Figure 8

Maximal isometric quadriceps strength (MVC), before and after training. Open symbols and column show pre-training individual values and group mean value, respectively, and s.e.m. is indicated by error bars. Filled symbols and hatched column show post-training values. Pre- to post-training differences: **P < 0.001.