Influence of Concentric and Eccentric Resistance Training on Architectural

J Appl Physiol 103: 1565–1575, 2007. First published August 23, 2007; doi:10.1152/japplphysiol.00578.2007.

Inﬂuence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles

Anthony J. Blazevich, Dale Cannavan, David R. Coleman, and Sara Horne Centre for Sports Medicine and Human Performance, School of Sport and Education, Brunel University, Uxbridge, United Kingdom Submitted 30 May 2007; accepted in ﬁnal form 15 August 2007

Blazevich AJ, Cannavan D, Coleman DR, Horne S. Influence of have performed chronic eccentric work (16, 36, 37), whereas concentric and eccentric resistance training on architectural adaptation in decreases (16) or a lack of change (36) is shown in those that human quadriceps muscles. J Appl Physiol 103: 1565–1575, 2007. First worked concentrically. Also, rightward shifts in the force- published August 23, 2007; doi:10.1152/japplphysiol.00578.2007.— length relationship of muscle have been shown after periods of Studies using animal models have been unable to determine the eccentric muscle training (37), which has been suggested to be mechanical stimuli that most influence muscle architectural adapta- attributable to an increase in serial sarcomere number. These tion. We examined the influence of contraction mode on muscle architectural change in humans, while also describing the time course results are strongly indicative of contraction mode being a of its adaptation through training and detraining. Twenty-one men primary stimulus for fiber or fascicle length change, and there and women performed slow-speed (30°/s) concentric-only (Con) or is some acceptance of the proposition that eccentric training eccentric-only (Ecc) isokinetic knee extensor training for 10 wk increases muscle fiber length. Nonetheless, methodological before completing a 3-mo detraining period. Fascicle length of the difficulties involved with clearly establishing the contraction vastus lateralis (VL), measured by ultrasonography, increased simi- mode of the measured muscles [chiefly the rat vastus interme- larly in both groups after 5 wk (⌬Con ϭϩ6.3 Ϯ 3.0%, ⌬Ecc ϭϩ3.1 Ϯ dius (VI)] limit the strength of this evidence (see e.g., Ref. 16). 1.6%, mean ϭϩ4.7 Ϯ 1.7%; P Ͻ 0.05). No further increase was Furthermore, increases in fiber length (or sarcomere number, found at 10 wk, although a small increase (mean ϳ2.5%; not signif- its surrogate when assuming a fixed sarcomere length) have icant) was evident after detraining. Fascicle angle increased in both been reported in muscles that were exercised through large groups at 5 wk (⌬Con ϭϩ11.1 Ϯ 4.0%, ⌬Ecc ϭϩ11.9 Ϯ 5.4%, ϭ Ϯ Ͻ ⌬ ϭϩ Ϯ excursions (34), which is suggestive of muscle excursion range mean 11.5 3.2%; P 0.05) and 10 wk ( Con 13.3 3.0%, (or absolute length) being a primary stimulus. Alternatively, ⌬Ecc ϭϩ21.4 Ϯ 6.9%, mean ϭ 17.9 Ϯ 3.7%; P Ͻ 0.01) in VL only and remained above baseline after detraining (mean ϭ 13.2%); movement velocity has been implicated. In humans, vastus smaller changes in vastus medialis did not reach significance. The lateralis (VL) fascicle length has been shown to be highly similar increase in fascicle length observed between the training predictive of 100-m time in well-trained sprint runners (35), groups mitigates against contraction mode being the predominant and increases in fascicle length were reported both in a group stimulus. Our data are also strongly indicative of 1) a close association of athletes who removed heavy resistance training and in- between VL fascicle length and shifts in the torque-angle relationship creased their high-speed training (9) and in a group of resis- through training and detraining and 2) changes in fascicle angle being tance trainers who performed the concentric phase of their lifts driven by space constraints in the hypertrophying muscle. Thus with maximum velocity (3). Contraction velocity has also been muscle architectural adaptations occur rapidly in response to resis- demonstrated to be an influencing factor in smooth muscle cell tance training but are strongly influenced by factors other than growth (18). Nonetheless, the influence of muscle contraction contraction mode. velocity has yet to be studied in animals, and the elucidation of skeletal muscle; fascicle; muscle adaptation; muscle strength the most significant stimulus for fascicle length adaptation has not been possible with the use of animal models. Thus the possibility remains that a range of mechanical stimuli influence A MUSCLE’S FORCE GENERATING properties are strongly influenced fascicle length. by the architectural arrangement of its fascicles. Therefore, In humans, the measurement of fascicle length in vivo with given that muscle architecture is highly plastic, understanding ultrasonography has revealed marked lengthening in both the mechanical stimuli that influence it is of primary impor- younger (3, 53) and older (47) populations after prolonged tance for those invested in optimizing muscle function and periods of resistance training, and fascicle shortening has been movement performance. In particular, fiber, or fascicle, length reported after gastrocnemius recession in spastic diplegia pa- has a profound effect on muscle excursion range, maximum tients (56). The reliable measurement of fascicle length in shortening velocity (and thus muscle power), and the force- humans offers the opportunity to use human models, which are length relationship. Despite the functional importance of fas- associated with few of the methodological limitations inherent cicle length, the most important mechanical signal required to in animal models. Importantly, contraction mode, muscle ex- stimulate its adaptation has not been identified. cursion, and contraction velocity during a movement can be Examination of the effects of a range of mechanical stimuli easily regulated by using isokinetic dynamometry to system- has typically been performed with animal models. Researchers atically examine the influence of each parameter, and the yet to have reported increases in fiber length in muscles purported to be described temporal response of fascicle length change can

Address for reprint requests and other correspondence: A. J. Blazevich, Centre The costs of publication of this article were defrayed in part by the payment for Sports Medicine and Human Performance, School of Sport and Education, of page charges. The article must therefore be hereby marked “advertisement” Brunel Univ., Uxbridge UB8 3PH, UK (e-mail: [email protected]). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. http://www.jap.org 8750-7587/07 $8.00 Copyright © 2007 the American Physiological Society 1565 1566 MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS be examined since repeated measurements are possible with tric-only (Ecc) knee extension training group. The subjects were noninvasive methods. In lieu of the above, the primary purpose tested for strength, muscle size, and muscle architecture at weeks 0, 5, of the present study was to test the hypothesis that fascicle and 10 of the training period and again after 3 mo (14 wk) of length changes are unique to the training contraction mode. detraining. Tests at 5 and 10 wk of training were conducted 4 (muscle The hypothesis would be confirmed if increases in fasci- architecture), 4–5 (strength testing), and 7 (muscle volume; week 10 only) days after the final training session of that training period; tests cle length result from eccentric training but a decrease or no were performed at the same time of day as at week 0. Three subjects change results from concentric training. Given that the time (2 men and 1 woman) withdrew from the training for reasons unre- course of fascicle length change has yet to be described in lated to the study; 10 and 11 subjects completed Con and Ecc training, humans, we measured, for the first time, fascicle length respectively. changes through periods of training (10 wk) and subsequent Resistance training. The subjects performed four (weeks 1–3), five detraining (3 mo). (weeks 4–7), or six (weeks 8–10) sets of six maximal concentric (Con While fascicle length impacts significantly on the length group) or eccentric (Ecc group) knee extension repetitions three times range and speed of active force production, a muscle’s fiber, or a week on an isokinetic dynamometer (Biodex system 3, Biodex fascicle, angle is also of great functional importance. It affects Medical Systems); in the first three sessions the subjects exercised at force production by allowing a greater amount of contractile 50%, 70%, and then 90% of their pretraining maximum to minimize muscle damage resulting from the unaccustomed heavy exercise. At tissue to attach to a given area of tendon or aponeurosis, and by least 1 day separated each session. The Con group trained by extend- increasing the muscle’s architectural gearing ratio (AGR; ratio ing their knee “as fast and hard as possible,” although the dynamom- ε ε of longitudinal muscle strain to fascicle strain, x/ f, during eter lever arm was set to move at 30°/s, from the maximum knee contraction) to allow fascicles the opportunity to produce flexion angle allowed by the dynamometer-seat setup (ϳ100°) to forces at more optimum lengths and shortening speeds (5, 8, maximum knee extension (5–10°) before returning their leg to the 28, 42, 61). Increases in fascicle angle have been reported after start position with a small knee flexion contraction. The Ecc group periods (14–16 wk) of heavy resistance training in humans (1, performed a small knee extension contraction (ϳ20 Nm) to move the 30), although studies of shorter duration have been unable to leg to an extended (10–15°) position before maximally extending the agree on its temporal response (10, 53). It is also not clear how knee to resist the subsequent downward movement of the lever arm of different muscles within a synergistic group respond to the the dynamometer. The subjects were asked to “stop the dynamometer” by applying a maximum upward force, although the dynamometer same stimulus. With respect to the mechanisms that promote lever arm continued to move at 30°/s throughout; the contractions fascicle angle change, a common theory is that it varies from were completed at a knee angle of ϳ100°. The knee joint ranges of its “genetic set point” concomitantly with muscle size. The motion during the concentric and eccentric training were greater than theory is given credence by the strong relationship shown normally encountered during walking (ϳ25°; Ref. 7), jogging (ϳ55°; between muscle thickness or cross-sectional area and fascicle Ref. 7), and countermovement jumping (ϳ80°; Ref. 11) but only angle (29, 30) and their concordant change with training (1, slightly greater than stair climbing (ϳ88° for 25.5-cm stair; Ref. 4) 30). Alternatively, alterations in AGR resulting from fascicle and so can be considered as being a loading stimulus of a greater than angle adaptations could influence force generation indepen- normal range of motion. One minute of passive rest was allowed dently of hypertrophy, so mechanisms unrelated to hypertro- between sets for both training groups, and repetitions within a set were phy should be considered. A second purpose of the present performed continuously. Knee angles were measured as the angle of a line joining the lateral epicondyle of the tibia to the lateral malleolus study, therefore, was to describe the time course of fascicle and a line joining the lateral condyle of the femur to the greater angle change in two synergist muscles [VL and vastus medialis trochanter. The knee joint center was aligned to the center of rotation (VM)] and to determine whether it is most strongly related to of the dynamometer, and the dynamometer lever arm was securely changes in muscle size rather than being an independent attached to the shank at ϳ50 mm above the lateral malleolus. Straps anatomic adaptation to mechanical loading. were placed firmly across the chest and waist of the subjects to minimize extraneous movement. Individual positioning of the subject METHODS with respect to backrest inclination, seat height, and lever arm length was held constant between test sessions. Loud verbal encouragement Subjects. Thirty-three recreationally active men and women volun- was given for each repetition, and set-by-set feedback of results was teered for the study, with 12 men [age ϭ 24.2 Ϯ 5.7 yr (mean Ϯ SD), provided to aid motivation. These results could be compared with height ϭ 178.7 Ϯ 5.9 cm, weight ϭ 73.6 Ϯ 6.2 kg] and 12 women personal best performances, which were known by the subjects. No (age ϭ 21.3 Ϯ 4.3 yr, height ϭ 160.8 Ϯ 4.3 cm, weight ϭ 63.5 Ϯ strength training was performed during the 3-mo detraining period, 10.3 kg) being assigned to one of two training groups and 4 men and although the subjects maintained their normal daily activities. 5 women being assigned to a nontraining control group. None of the Fascicle strain during training. To determine the fascicle strain subjects had a significant lower limb injury within the previous 5 yr, induced by the training contractions, maximum and minimum fascicle had inflammatory conditions or hypertension, had performed weight lengths were measured at midthigh in the VL in six subjects (3 men training, had manual lifting-oriented occupations, or performed vig- and 3 women) during concentric and eccentric contractions. An orous exercise more than four times a week. All subjects gave written ultrasound transducer (45-mm linear array, 10 MHz; Megas GPX, informed consent before the study, which was approved by the Human Esaote, Italy) was fixed to a foam cast and secured over the midpoint Research Ethics Committee within the School of Sport and Education of the VL by elastic strapping. Sufficient water-soluble gel was at Brunel University and was conducted in accordance with the applied to the transducer to aid acoustic coupling and remove the need Declaration of Helsinki. for dermal contact. The transducer was aligned in the direction of the Study design. After the subjects were familiarized with the testing muscle fascicles; appropriate orientation was achieved when muscle procedures, their concentric and eccentric strength was tested, as fascicles could be traced clearly across the ultrasound image. A series described below. Those allocated to the training groups were paired of 200 images (29-Hz sampling frequency) were taken during each of with respect to their sex and pretraining torque production (mean of three maximal concentric and eccentric knee extension contractions peak concentric and eccentric torque measured at 30°/s) and then for each subject. Sonographs containing images of the muscle fasci- randomly allocated to either the concentric-only (Con) or the eccen- cles at their shortest and longest lengths were used for analysis.

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS 1567 Muscle fascicle length was determined by the procedures described in aid acoustic coupling and remove the need to contact the skin; this Fascicle length measurement below. Strain was calculated as the eliminated deformations of the muscle that can occur when pressure is percent change from the shortest to longest fascicle length. directly applied to the skin and underlying muscle. Scans were Strength testing. After warm-up, maximum concentric and eccen- performed on the right leg with the transducer oriented parallel to the tric knee extension torque was measured at 30°/s with the setup muscle fascicles and perpendicular to the skin. Thus the transducer’s described above. The subjects performed three consecutive contrac- orientation relative to the longitudinal axis of the thigh was different tions with 2 min of rest separating the concentric and eccentric tests. between subjects. Transducer alignment was considered appropriate Torque and position data were calibrated and sampled at a 2,000-Hz when several fascicles could be easily delineated without interruption analog-digital conversion rate and stored on a computer running across the image. Sonographs were taken in the middle of the VL and Spike2 software (Cambridge Electronic Design, Cambridge, UK). The the VM at 50% of the distance from the central palpable point of the data were subsequently filtered with a digital fourth-order, zero-lag greater trochanter to the lateral condyle of the femur. At week 0, Butterworth filter with a 14-Hz cutoff frequency (62); peak torque scanning locations were mapped onto a malleable plastic sheet, along produced during each set was taken as the criterion measure. with other distinguishing landmarks (e.g., border of patella, freckles, Torque-angle relationship. To assess changes in the knee extension scars, etc.) to ensure that repeated scans were taken from the same torque-angle relationship after training, torque was recorded for each site. One difficulty with repeated scanning is that small changes in the 10° of the range of motion for the best concentric and eccentric trials. orientation of the transducer between test occasions can result in Changes in both absolute and normalized torque (i.e., expressed significant variation in the muscle architecture recorded on the image. relative to the peak torque recorded at any angle) were determined at To minimize this, we compared on-screen images at the 5 wk, 10 wk, each angle. This approach, similar to that used by Butterfield and and detraining testing sessions to those obtained at week 0. Echoes Herzog (15) and Lynn et al. (37), was used in place of a measurement from interspaces among the fascicles and heterogeneities in the of the change in angle of peak torque since the torque-angle curves subcutaneous adipose tissue are unique to the transducer orientation generated by the subjects fluctuated slightly throughout the range of (shown in Fig. 1), and these heterogeneities were easily visualized motion, and particularly during the flatter portion of the curve nearing after the training and detraining periods in Ͼ80% of the subjects. Thus peak torque. These small fluctuations substantially affected the reli- the transducer could be oriented so that these markings were the same ability of the measure of angle of peak torque. The average shift in the in both sets of images, which provided confidence that transducer torque-angle relationship for each subject was also calculated by orientation discrepancies were small and were unlikely to account for averaging the normalized concentric and eccentric torque values at measured pre-/posttraining architectural differences. All measure- each angle and then calculating their change from the pretraining ments were carried out by the same experienced sonographer. values; increases at 80 and 90° and decreases at 30, 40, 50, 60, and 70° Fascicle length measurement. Fascicle length was measured only were taken to contribute to positive torque-angle shifts, so the pro- in the VL, as the complex architecture of the VM ensured that the portional change was calculated as: reliability of length measurements was unacceptably low (8, 10). ͑ Ϫ ͒ Fascicle length was defined as the length of the fascicular path ͚ CE80,90°mid-detrain CE80,90°pre between the superficial and deep aponeurosis. In most cases, the Ϫ ͑ Ϫ ͒ fascicles extended off the acquired image. The length of the missing ͚ CE30 – 70°mid-detrain CE30 – 70°mid-detrain portion was estimated by linear extrapolation. This was done by where CE is the average of the normalized concentric and eccentric measuring the linear distance from the identifiable end of a fascicle to torques at a specific movement speed and subscripts 30–90° refer to the intersection of a line drawn from the fascicle and a line drawn the joint angles at which the normalized values were calculated; the from the superficial aponeurosis (see, e.g., Refs. 38, 51). The error subscript pre indicates that the measure was taken at pretraining (i.e., involved with this technique has been shown to be reasonably low 0 wk), whereas the subscript mid-detrain indicates that measures were (ϳ2.3%) in contracted tibialis anterior (46), where fascicle curvature taken at midtraining, posttraining, and detraining (i.e., 5 wk, 10 wk is significant. Given that fascicles in the relaxed VL are relatively and at detraining). The average shift was then recorded for each straight (see Fig. 1), we estimate that our error would be somewhat subject and plotted (see Fig. 10 for example). smaller. Repeated measurements yielded a coefficient of variation Muscle architecture. In vivo muscle architecture was examined (CV) of 1.7% (ϳ1.4 mm) and were performed by a single researcher. with two-dimensional (2D), B-mode ultrasonography (Megas GPX, Fascicle angle measurement. Images were analyzed with publicly Esaote) with a 45-mm linear array transducer (10 MHz). To obtain the available imaging software (ImageJ 1.36b, National Institutes of images, subjects lay supine with their legs fully extended and their Health; free to download from http://rsb.info.nih.gov/ij/). Land- muscles relaxed. A water-soluble gel was applied to the transducer to marks corresponding to the muscle fascicles and aponeurosis were

Fig. 1. Sonographs of vastus lateralis (VL) at 0 wk and 10 wk. Lines delineating the aponeurosis and visible fascicle shown on the 0 wk image (left) are used to measure fascicle length and angle (␪). Arrows on the edges of the image show the muscle thickness (MT; mean of distance between superﬁcial and deep aponeurosis measured at each edge of the sonograph); a slight increase in muscle thickness is apparent between 0 wk and 10 wk for this subject. Adipose and connective tissue marks as well as visible blood vessels are circled on the 10 wk image (right). Visibility of these markings is strongly dependent on the transducer angle and can be used to ensure repeatability of transducer placement across time points.

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org 1568 MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS

Fig. 2. MRI scans of the quadriceps muscles. T2-weighted images were obtained for the measurement of both anatomic cross-sectional area (for later calculation of muscle volume and VL physiological cross-sectional area) and the shift in gray scale (image density), which indicates the level of muscle activity within days of the tests (see METHODS). Perimeters of the 4 vastii muscles are shown: VL, vastus intermedius (VI), rectus femoris (RF), and vastus medialis (VM). In these images, there is an increase in the whole quadriceps area but no change in the gray scale of the image.

digitized (Fig. 1). Two points on each fascicle were digitized, one ϳ3 shifts (38, 43); such shifts have been shown to result both from mm from the deep aponeurosis and the second at 50% of the distance damage to the contractile apparatus as a result of intense exercise (23, from the deep to superficial aponeurosis. This allowed accurate 49, 54) and from activation-dependent myocellular metabolism (2, 31, delineation of the fascicles without incorporating the slightly greater 55). This shift can be easily quantified by examining changes in the fascicle curvature that can occur at the insertion point of the fascicles image density of T2-weighted MRI images. Although subjects were on the deep aponeurosis (58). Repeated measurements yielded a CV asked not to exercise before the testing, we examined the image of 1.6% (ϳ0.32°). density (sum of gray scale values of all pixels in the region of interest Muscle volume and anatomic and physiological cross-sectional divided by total number of pixels) of MRI images by tracing the area. At weeks 0 and 10, axial T2-weighted MRI scans of the thigh whole quadriceps muscles on images taken at 50% of the muscle were obtained at 16-mm intervals from the superior border of the length (i.e., at the same point as muscle architecture measurements) to patella to the greater trochanter [3.0 T Magnetom, Siemens, Berlin, ensure that prior exercise and testing did not influence the cross- Germany; repetition time (TR) 4,260 ms, echo time (TE) 95 ms, sectional area measures. One subject showed a 12.8% shift in image averages: 3, field of view 200 ϫ 200, slice thickness 4 mm, slice density and was omitted from further analysis; the average shift for separation 14 mm, center-to-center slice distance 16 mm] from the the remaining subjects was Ϫ0.49 Ϯ 0.8% (SE), so fluid shifts are training subjects. Technical difficulties with the scanner at 10 wk unlikely to have influenced the results. precluded the acquisition of images from the control subjects with Muscle thickness. In addition to the MRI measurements, muscle sufficient contrast for analysis, although a high stability in MRI-based thickness was also measured at weeks 0, 5, and 10 and after the cross-sectional area measurements has previously been demonstrated detraining period from the obtained 2D ultrasound images. Muscle over a 10-wk period [sum of 7 levels of cross section: pre ϭ 323.7 Ϯ thickness was defined as the mean of the distances between superficial 52.8 (SD), post ϭ 320.9 Ϯ 53.0 cm2] in subjects who do not change and deep aponeurosis measured at the ends of each 45-mm wide their exercise patterns (25). For training subjects, the scans were taken sonograph. The method and its reliability have been reported previ- with a standard body coil, with the subjects lying supine with the legs ously (8, 10). fully extended; example scans are shown in Fig. 2. From these scans, Statistical analysis. Analyses were performed with SPSS Version anatomic muscle cross-sectional area was measured for each slice by 13.0 (SPSS, Chicago, IL). Temporal changes in strength, muscle manually tracing the perimeter of each muscle with Scion Image architecture, and torque-angle variables were examined simulta- for Windows (free to download at http://scioncorp.com/frames/ neously by multivariate analysis of variance with repeated measures. fr_download_now.htm). Care was taken to exclude adipose and Significant main and interaction effects were further examined with connective tissue incursions. In proximal images, clear delineation of paired (for resolving time-related changes)- or independent (for re- the vastii muscles was not always possible because of a lack of solving group-related differences)-samples t-tests. Differences in the observable intermuscular septum. In these cases, a line was drawn change in cross-sectional area measured by MRI at different muscle from the end of the observable septum to a landmark on the muscle’s locations were tested with paired-samples t-tests. Greenhouse-Geisser perimeter where the septum had intersected in distal images. Each adjustment was applied on occasions when the assumption of sphe- slice was measured three times, with the median cross-sectional area ricity was violated (Mauchly’s test of sphericity, P Ͻ 0.05). Unless being taken as representative; repeated measurements were very otherwise stated, all parameters are reported as means Ϯ SE. Statis- reliable (CVVL ϭ 1.5%, CVVM ϭ 1.9%). Whole quadriceps cross- tical significance was set at P Ͻ 0.05, although the results of statistical sectional area was calculated as the sum of each of the four muscle tests associated with an ␣-level of Ͻ0.1 are discussed. cross sections, and individual muscle and whole quadriceps volumes were calculated by summing the product of cross-sectional area and RESULTS slice thickness of all images. For VL only, physiological cross- sectional area (PCSA) was also calculated with the equation: Strength changes. Although there was no change in the control group [⌬ ϭϩ0.1 Ϯ 2.3 Nm (0.5 Ϯ 1.8%); ⌬ ϭ Vol Con Ecc PCSA ϭ ϩ7.5 Ϯ 5.5 Nm (3.0 Ϯ 3.2%)], peak torque recorded in FL ϫ cos␪ concentric and eccentric contractions increased significantly where Vol is the muscle volume, FL is its fascicle length, and ␪ is the after 5 and 10 wk of training in both training groups, as shown fascicle angle. in Fig. 3. The increase in concentric torque was greater in the Intense exercise performed within several days of the MRI scan can Con group (24.1 Ϯ 4.2%) than in the Ecc group (16.4 Ϯ 5.1%) influence muscle volume via osmotically driven intracellular fluid (P Ͻ 0.05), but there was no difference in the increase in

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS 1569 no shifts in the torque-angle relationship for the control subjects. Muscle size. Whole quadriceps volume increased from 2,342.9 Ϯ 111.2 to 2,586 Ϯ 114.8 cm3 (10.2%; P Ͻ 0.001) after 10 wk of training, with no difference between training groups. VL [825.6 Ϯ 40.9 to 916.9 Ϯ 43.2 cm3 (11.1%); P Ͻ 0.001] and VM [486.2 Ϯ 26.8 to 558.3 Ϯ 27.7 cm3 (14.8%); P Ͻ 0.001] volume also increased significantly. These increases in volume were not related to pretraining muscle volume. As a result of both volume and architectural changes, the PCSA of VL increased from 115.1 Ϯ 5.3 to 124.2 Ϯ 4.9 cm2 (7.9%; P Ͻ 0.01). Although the focus of this study was on VL and VM, we took the opportunity to examine region-specific changes in all of the quadriceps muscles by comparing anatomic cross-sectional changes measured at proximal (mean of the 3 slices nearest to 25% of the distance from the proximal end point of Fig. 3. Strength increases (both groups combined) after 10 wk of knee the muscle) to distal (75% from proximal end point of the extension training and 14 wk of detraining. Both concentric and eccentric muscle) locations. Whereas increases in cross section of VL torque increased; the increase in concentric strength was greater in the Ͻ and rectus femoris were relatively consistent along their concentric-only (Con) group than the eccentric-only (Ecc) group (P 0.05; ϭ data not shown). Torque production decreased significantly in eccentric con- lengths, as shown in Table 1, there was a trend (P 0.08) tractions after the detraining period (dashed line) only (P Ͻ 0.05); torque toward a greater increase distally in VM (⌬VMprox ϭϩ1.1 Ϯ Ͻ 2 2 produced after detraining was significantly greater than at 0 wk (P 0.01). 0.4 cm , ⌬VMdist ϭϩ3.0 Ϯ 0.9 cm ). There was also a trend Significant difference from 0 wk to 10 wk: **P Ͻ 0.01, ***P Ͻ 0.001. toward a greater increase distally in VI when calculated as an absolute change (⌬VIprox ϭ 0.0 Ϯ 0.5, ⌬VIdist ϭϩ2.2 Ϯ 0.8 2 eccentric strength between Con and Ecc groups (⌬Con ϭ cm ; P ϭ 0.055), and a significantly greater increase distally ϩ35.9 Ϯ 12.7%; ⌬Ecc ϭϩ38.9 Ϯ 14.2%). when calculated as a relative change (⌬VIprox ϭϩ1.0 Ϯ 2.1%, After 3 mo of detraining, there was a nonsignificant decrease ⌬VIdist ϭϩ13.6 Ϯ 4.8%; P Ͻ 0.05). While individual variation in concentric torque of 5.6 Ϯ 2.7% (P ϭ 0.084) from that recorded at 10 wk for the training subjects (pooled data) and a statistically significant decrease in eccentric torque of 11.4 Ϯ 2.3% (P Ͻ 0.05). There was no difference between the training groups. After detraining, concentric and eccentric torque remained above pretraining levels [⌬Con ϭϩ13.8 Ϯ 3.5% (P Ͻ 0.01); ⌬Ecc ϭϩ17.7 Ϯ 7.1% (P Ͻ 0.05)]. Torque-angle relationship. At 0 wk, greater torque was produced in eccentric, compared with concentric, actions by the training subjects (Figs. 3 and 4). Both peak concentric and eccentric torque were produced at a knee angle of ϳ70° (note: data were taken at each 10° of range of motion, so the optimum knee angle was not specifically determined; see METHODS), with less torque being produced at angles further from optimum. Both absolutely and proportionally, peak eccentric torques exceeded concentric torques at larger knee angles, although normalized torque at smaller angles was the same between contraction modes, so there was a small difference in the stimulus applied to the muscles of the subjects during training. Despite this, there were no between-group differences in either absolute or normalized (to peak) torque-angle relations at any time point in either concentric or eccentric actions. Pooled analyses revealed both an increase in torque production, largely around the angle of peak torque (Fig. 4), and a shift in the normalized torque curve (Fig. 5), which occurred largely within the first 5 wk of training. There was a small and nonsignificant trend toward a reverse shift from 5 to 10 wk. The shift in the torque-angle curve was most prominent in eccentric contractions where greater absolute changes were Fig. 4. Increases in knee angle-specific concentric (top) and eccentric (bottom) found. Interestingly, there was a further shift in the torque- torque with training (pooled data). Increases were greatest near the optimum angle and were not different between the training groups. 0° ϭ full extension. angle curve to more acute knee angles (i.e., longer muscle aSignificant difference between 0 and 5 wk, P Ͻ 0.05; bsignificant difference lengths) with detraining (see Fig. 6). These shifts were only between 0 and 10 wk, P Ͻ 0.05. To improve readability, SE bars are shown for statistically significant for eccentric contractions. There were 90° angle only.

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org 1570 MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS moderately longer (ϳ14 mm) at maximum knee flexion. Rel- ative to the overall length change, however, this difference was small and was not statistically significant (P ϭ 0.30) for the six subjects tested. There was no change in VL fascicle length in control subjects [⌬ϭϪ0.3 Ϯ 0.7 mm (Ϫ0.3 Ϯ 0.9%)] over the 10-wk testing period. A pooled analysis of the training groups revealed a significant increase after 5 wk in the training subjects (4.7 Ϯ 1.7%; P Ͻ 0.05), but no further change to 10 wk (⌬pre-post ϭϩ4.2 Ϯ 1.4%; see Fig. 8). However, there was no difference in the change in fascicle length between the training groups [⌬Con ϭϩ6.3 Ϯ 3.0% (P ϭ 0.039); ⌬Ecc ϭϩ3.1% Ϯ 1.6% (P ϭ 0.056)]. The small mean increase in fascicle length after detraining (⌬post-detraining ϭϩ2.5 Ϯ 2.2%) did not reach statistical significance and was not different between training groups. VM fascicle length was not estimated because its complex architecture rendered the estimates unreliable. There was no change in VL or VM fascicle angle over 10 wk in the control subjects [⌬VL ϭϪ0.24 Ϯ 0.52° (0.4 Ϯ 3.6%); ⌬VM ϭϩ0.40 Ϯ 0.31° (2.5 Ϯ 2.1%)]. A pooled analysis revealed statistically significant VL fascicle angle increases of 11.5 Ϯ 3.2% (P Ͻ 0.05) and 17.9 Ϯ 3.7% (P Ͻ 0.01) after 5 and 10 wk, respectively (mean data are shown in Fig. 9). There was a nonsignificant reduction after detraining such that fasci- Fig. 5. Changes in normalized angle-specific concentric (top) and eccentric cle angle remained greater after detraining than at pretraining (bottom) torque with training (pooled data). Subjects were able to produce (13.2 Ϯ 4.2%). Smaller changes in VM fascicle angle of 4.8 Ϯ relatively greater torque at acute knee angles (i.e., longer muscle lengths) after 2.5% and 8.2 Ϯ 3.4% after 5 and 10 wk were more variable by the training, whereas less torque was produced at larger knee angles (i.e., comparison with VL and did not reach statistical significance. shorter muscle lengths). Greater differences were seen for eccentric contrac- There were also no statistically significant training group- tions where peak torque production was higher. There were no between-group differences. aSignificant change from 0 to 5 wk, P Ͻ 0.05; bsignificant change from0to10wk,P Ͻ 0.05. To improve readability, SE bars are shown for 90° angle only. in the hypertrophic response precluded the greater distal increase in whole quadriceps cross-sectional area from reaching statistical significance (⌬prox ϭ 7.3%, ⌬dist ϭ 12.6%), increases were greater in the distal compared with proximal region (3-fold) in 75% of subjects. To more closely examine the temporal hypertrophic response, muscle thickness measures were also obtained. Whereas no change in muscle thickness was found for control subjects [⌬VL ϭϩ0.56 Ϯ 0.96 mm (2.6 Ϯ 3.6%); ⌬VM ϭ ϩ0.33 Ϯ 0.57 mm (2.5 Ϯ 3.8%)], there was a statistically significant increase in muscle thickness of VL at 5 and 10 wk (P Ͻ 0.05) and of VM at 10 wk (P Ͻ 0.05) (Fig. 7) in the training subjects (both groups combined). Thus the temporal response of the muscles was not the same. The slight decrease in both muscles after detraining was not significant; however, the detraining values were also not different from values at 0 wk. There was no statistical difference in the changes in muscle thickness between Con and Ecc groups [⌬Con ϭϩ25.4 Ϯ 12.6 mm (11.8%); ⌬Ecc ϭϩ18.4 Ϯ 10.4 mm (8.3%)]. Muscle architecture. The mechanical strain of VL fascicles measured at midthigh in three men and three women before training was 105.1 Ϯ 9.0% (62.4 Ϯ 7.5 to 128.3 Ϯ 15.5 mm) Fig. 6. Changes in normalized angle-specific concentric (top) and eccentric and 90.1 Ϯ 12.3% (60.0 Ϯ 4.4 to 114.5 Ϯ 12.0 mm) for (bottom) torque with detraining (pooled data). The subjects were able to concentric and eccentric contractions, respectively. Thus there produce relatively greater torque at acute knee angles (i.e., longer muscle lengths) after detraining, but less torque at greater knee angles. These differ- was a tendency for subjects to produce tension through a ences were significant during concentric contractions, but the small differences slightly longer fascicle length range during concentric contrac- in normalized eccentric strength were not statistically significant. *P Ͻ 0.05. tions, which largely resulted from their VL fascicles being To improve readability, SE bars are shown for 90° angle only.

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS 1571 Table 1. Changes in anatomic cross-sectional area measured proximally (25% from proximal end point) and distally (75% from proximal end point)

Proximal Distal

Muscle 0 wk 10 wk Absolute Change % Change 0 wk 10 wk Absolute Change % Change Quad 76.6Ϯ3.8 82.2Ϯ3.9 5.6Ϯ1.6 7.3 61.0Ϯ3.0 68.7Ϯ3.9 7.7Ϯ2.5 12.6 VL 29.3Ϯ1.4 32.5Ϯ1.4 3.2Ϯ0.7 10.9 17.7Ϯ1.2 20.1Ϯ1.6 2.4Ϯ0.8 13.6 VM 6.14Ϯ0.5 7.24Ϯ0.6 1.1Ϯ0.4 17.9 24.4Ϯ1.2 27.4Ϯ1.3 3.0Ϯ0.9* 12.3 VI 22.6Ϯ1.5 22.6Ϯ1.4 0.0Ϯ0.5 0.0 16.4Ϯ0.8 18.6Ϯ1.1 2.2Ϯ0.8† 13.4‡ RF 18.2Ϯ1.2 19.4Ϯ1.2 1.1Ϯ0.6 6.6 6.0Ϯ0.5 6.5Ϯ0.5 0.5Ϯ0.2 8.3 Values are means Ϯ SE. Quad, quadriceps femoris; VL, vastus lateralis; VM, vastus medialis; VI, vastus intermedius; RF: rectus femoris. Whereas the increases in cross-sectional area were generally greater in the distal, compared to the proximal, quadriceps, statistically significant region-specific hypertrophy was only seen in VI. *Mean difference from proximal, P ϭ 0.08; †mean difference from proximal, P ϭ 0.055; ‡significantly different from proximal, P Ͻ 0.05. dependent differences in either VL or VM fascicle angle the increase in Con was statistically greater than that in Ecc. To change over the training period. For VL, fascicle angle of the our knowledge, such a result has not been reported previously. Ecc group increased by 21.4 Ϯ 7.3% (P ϭ 0.03), whereas Concomitant with the strength change was a significant changes in the Con group did not reach statistical significance increase in muscle volume and VL PCSA. By obtaining T2- (13.3 Ϯ 3.0%; P ϭ 0.06) after 10 wk. The smaller changes in weighted MRI images and measuring the image density in both VM fascicle angle for Con (7.0 Ϯ 4.9%) and Ecc (10.2 Ϯ 0 wk and 10 wk images we were able to confirm that the 5.1%) groups over the same period were not significant. increase in muscle size was not a residual effect of the training or testing contractions performed by the subjects, although the DISCUSSION MRI data for one subject were omitted because of a significant We have examined the relative contribution of the training shift in image density. Thus the training induced significant contraction mode to muscle architectural adaptations in human strength and muscle size gains in both training groups. Inter- VL and VM. While there were no changes in the strength of a estingly, cross-sectional changes were not consistent at differ- control group measured across a 10-wk nontraining period, the ent muscle locations. Most notably, there was a greater in- training induced significant increases in concentric and eccen- crease in cross section of distal, compared with proximal, VI. ϭ tric strength of both concentric-only training (Con) and eccen- There was also a trend (P 0.08) toward a greater distal tric-only training (Ecc) subjects. The knee extensor strength increase in VM. While there was not a statistically different responses to high-resistance training reported in the literature regional change shown for the quadriceps as a whole, a set of vary widely [e.g., compare results from Higbie et al. (25), 16 “responders” (i.e., 75% of the sample) showed a signifi- Ͼ Hortoba´gyi et al. (26) and Seger et al. (52)], although the cantly greater ( 3-fold) increase distally. Thus our data con- magnitude of the change measured in the present study is not firm those of others who have reported a heterogeneous hyper- out of line with these reports, and our finding of a greater trophic response after knee extension training (17, 24, 27, 40), increase in eccentric strength after training has been commonly although there is little agreement as to which regions generally reported (1, 10, 20, 25, 52). Interestingly, training mode spec- show the greatest response. Given that different regions of the ificity was only observed under concentric conditions, where quadriceps muscles are architecturally disparate and the muscles would encounter varying stresses during contraction, it is not unexpected that hypertrophy would vary according to

Fig. 7. Changes in VL and VM muscle thickness (pooled data). Muscle Fig. 8. Changes in VL fascicle length (pooled data). There was a significant thickness increased significantly after 5 wk in VL and after 10 wk in VL and increase from 0 wk to 5 wk (4.7%; P Ͻ 0.05) but no further change in the 2nd VM in training subjects. The decrease after detraining was not significant, 5-wk training period in training subjects. The mean increase in fascicle length although these values also were not statistically different from 0 wk. Muscle in detraining (2.5 Ϯ 2.2%) was not statistically significant. Changes in fascicle thickness changes were not different between the training groups. *P Ͻ 0.05. length were not different between the training groups. *P Ͻ 0.05.

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org 1572 MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS uphill running training (it was not possible to measure VI length change). They confirmed that VL actively lengthens during downhill running and largely shortens during uphill running but found a similar decrease in sarcomere number in the VL of both training groups [downhill group ϭϪ4.0%, not significant (NS); uphill group ϭϪ5.3%, P Ͻ 0.05]. Interest- ingly, their Figures 1 and 2 (Ref. 16) showed that VL is active at short lengths during the period of EMG activity in both uphill and downhill running, which might explain the similar loss of sarcomeres in both training groups. In VI, sarcomere number increased in the downhill-trained rats and decreased in the uphill-trained rats, but there is no evidence (in their study or other studies) that VI operates similarly to VL. Thus some caution must be exercised in interpreting these data as evidence for contraction mode-related alterations in sarcomere number. In another study by the same research group (32), lengthening Fig. 9. Changes in VL and VM fascicle angle (pooled data). VL fascicle angle contractions of the tibialis anterior and extensor digitorum increased significantly after 5 wk of training (11.5%; P Ͻ 0.05) and continued longus of rabbits did not result in significant increases in to increase through to 10 wk (17.9%; P Ͻ 0.01) in training subjects. The slight decrease in fascicle angle after detraining was not statistically significant, and sarcomere number. To further confirm the finding that the it remained above 0 wk levels. The mean increases in VM fascicle angle did training range of motion, rather than contraction mode or not reach statistical significance; changes in VM fascicle angle (not shown) velocity, has the greater effect on fascicle length change, were more variable than changes in VL fascicle angle. Fascicle angle changes examination of fascicle length changes to training using a less Ͻ Ͻ were not different between the training groups. *P 0.05; **P 0.01. than normal contraction length range is required. Furthermore, our data are unable to determine whether the maximum length location (8), although the reason for the different locations of achieved by the muscle or the total range of lengthening it hypertrophic gain reported in these studies requires more experiences is the primary stimulus for range of motion- detailed study. dependent fascicle lengthening, since the fascicle strains en- Stimulus for fascicle length adaptation. A main purpose of countered during the training were not appreciably different. the present research was to test the hypothesis that muscle Time course of fascicle length adaptation. We also sought to contraction mode strongly influences the magnitude of fascicle describe the temporal response of fascicle length change for the length adaptation. Our finding that Con and Ecc groups showed first time in humans. An important finding was that fascicle similar increases (rather than opposite responses) is not sup- length adapted within the first weeks of training, during which portive of it, so factors other than contraction mode must period neural adaptations have traditionally been thought to influence fascicle length. Using our study design, we were able dominate. Our results confirm the rapid adaptation in fascicle to gain some insight into the possible factors underpinning length reported by Seyennes et al. (53) and by others using fascicle length change. We were able to examine the possible animal models (16, 36, 37). We found increases of ϳ4.7% influence of the training range of motion (or muscle excursion) compared with increases of 9.9% reported by Seyennes et al. by having the subjects train through a knee joint range of (53). The lesser increase found in the present study can prob- motion of 95–100°, which is substantially greater than that ably be explained by our measurement of fascicle length with normally encountered during walking (ϳ25°; Ref. 4), jogging the knee fully extended, and the muscle shortened, compared (ϳ55°; Ref. 7), and countermovement jumping (ϳ80°; Ref. with Seyennes et al. (53), who measured fascicle length with 11), although only slightly greater than stair climbing (ϳ88° 80° of knee flexion. Also, their subjects trained three times a for 25.5-cm stair; Ref. 4), and so can be considered as being a week, with testing being conducted at short intervals (10, 20, loading stimulus of greater than normal range of motion. The and 35 days). Thus training and testing were possibly separated finding of a similar increase in fascicle length between the groups by only a few days, and osmotic fluid shifts resulting from the is supportive of the training range of motion (or muscle training stress might have had some impact on the measured excursion range) being the dominant stimulus for fascicle change. We took sonographs at least 4 days after the last length adaptation. It is unlikely that shortening velocity had a training session to minimize the impact of this phenomenon, strong influence because we would have expected that slow yet our results confirm the rapid changes they reported, al- training velocities would cause a reduction (or no change) in though ours were smaller in magnitude. We have shown that fascicle length in both training groups, since muscle loading at these adaptations do not continue past ϳ5 wk in humans, and higher shortening speeds has been associated with fascicle they therefore have a different temporal response to the fascicle length increases in skeletal muscle (3, 9). angle adaptations (see below). The implications of this are that Our results might be somewhat surprising given the data only relatively short periods of training are required to induce suggestive of contraction mode being an important mediating the necessary adaptation, so alterations in muscle function factor for VI sarcomere addition when muscle loading in rats is imposed by the fascicle length changes should also occur provided by downhill running training (16, 36, 37). However, rapidly. in those studies the excursion range of VI was not explicitly One such functional alteration associated with fascicle confirmed. Butterfield et al. (16) analyzed the operating length length change is the shift in the knee extension torque-angle range of the VL in rats by sonomicrometry before measuring relationship. Significant shifts toward longer muscle lengths sarcomere number adaptations to 10 days of either downhill or (i.e., rightward shift) have been shown previously after periods

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS 1573 strong evidence that fascicle length adaptations directly influence force-length relations of humans muscles, and that the range of motion of the training exercises is the strongest influencing factor for fascicle length adaptations. It also con- firms the association between fascicle length changes and the force-length relation shown rarely in humans (e.g., Ref. 47) but consistently shown between sarcomere addition (i.e., fiber lengthening) and changes in force-length relation in animals (14, 15). Fascicle angle adaptation. To test the hypothesis that fascicle angle adaptations would be strongly related to muscle Fig. 10. Temporal patterns of normalized fascicle length (FL) and torque- size, we measured muscle thickness of both VL and VM during angle relationship change (pooled data). Fascicle length change was calculated training and detraining and then compared its temporal re- as a proportion of pretraining values. The shift in the torque-angle relationship was calculated by averaging the normalized concentric and eccentric torques at sponse to that of fascicle angle. In both muscles, there was a each angle for each subject and then calculating the change from pretraining tendency for muscle thickness and fascicle angle to increase values; increases at 80 and 90° and decreases at 30, 40, 50, 60, and 70° with training and then decrease slightly with detraining. As contributed to positive torque-angle relationship shifts. The average shift was shown in Fig. 11, the responses in VL, for which we obtained then recorded for each subject and plotted. There was a similar temporal response of fascicle length and the torque-angle relationship through both measures of the highest reliability, are almost identical. We training and detraining. found a constant ratio of adaptation such that a 1% increase in fascicle angle was associated with a ϳ0.5% increase in muscle thickness. These data are indicative of a strong relationship of knee extension training (17, 47, 50), although in one study between muscle size and fascicle angle, as has been previously an increase in tendon stiffness after training in older subjects reported (29, 30). As expected, the changes in fascicle angle, was suggested to have prevented a shift in the torque-angle which were measured in a single plane, and those of the 2D relationship despite there being a clear shift in the muscle (cross-sectional area) and 3D (volume) measures of muscle length-force relation (47). The idea that architectural adapta- size were not as well related. Our alternative hypothesis was tions might underpin changes in torque-angle relationships has that fascicle angle increases were a separate anatomic adapta- gained momentum since there has been a lack of association of tion to the stress imposed on the muscle during training and neural and torque-angle adaptations, with some authors show- might be unrelated to muscle hypertrophy. Our finding of a ing a concomitant change (57) and others not (47, 59, 60). similar response in the Con group, who produced lesser torque Other authors have also examined relationships between vol- in training, and the Ecc group, who produced greater torque in untary and electrically elicited contractions and found little training, mitigates against this. The slightly greater increase in similarity (32). This has been taken as good evidence that fascicle angle obtained by Ecc subjects was influenced by a mechanical, rather than neural, factors underpin the torque- strong “responder,” and therefore was associated with a greater angle relationship. Given that increases in fiber length resulting SE. Therefore, we are not confident that the greater training from the addition of sarcomeres are typically associated with load imposed on Ecc subjects can account for the small (and the rightward shift of the torque-angle curve in animals (14, nonsignificant) between-group difference. Thus our data are 15), we expected to see a relationship between fascicle length more suggestive that fascicle angle adapts in response to change and the torque-angle shift, which would therefore be muscle hypertrophy, and might therefore be driven by space the same in both training groups. As shown in Figs. 4 and 5, the constraints in the hypertrophying muscle. torque-angle relationship shifted toward the right in the first 5 The temporal response of fascicle angle to training has not wk of training but did not shift (in fact, there was a small trend been previously described. We found that in VL fascicle angle toward a negative shift) from 5 to 10 wk of training; these increased significantly (11.0%; Fig. 9) after 5 wk and contin- changes were not group dependent. Unexpectedly, we found a ued to increase throughout the 10-wk training period (17.9%). further small shift to the right in detraining (Fig. 6). The Previously, Seyennes et al. (53) reported a significant (7.7%) magnitude of increase (2.5%; NS) was more than half of the increase in VL fascicle angle after 5 wk. The smaller magni- increase attributable to the training, although there was some interindividual variability in this response. The reasons for this increase are not clear, although evidence for an increase in fascicle length in VL after the removal of heavy resistance training has been previously documented (9); interestingly, the changes reported in that study also occurred within 5 wk. We take this as evidence that learning responses cannot be solely responsible for the shifts because we would not then have seen a change in the detraining period. Regardless, the temporal response of the torque-angle curve matched the fascicle length response very closely, even to the point of them having a similar response to detraining (Fig. 10). The finding also of a constant ratio of adaptation, such that a 1% increase in fascicle Fig. 11. Temporal patterns of normalized VL fascicle angle (FA) and muscle length was associated with approximately a 1% shift in the thickness (MT) change (pooled data). There was a similar response of fascicle normalized torque-angle relationship, can also be considered as angle and muscle thickness through both training and detraining.

J Appl Physiol • VOL 103 • NOVEMBER 2007 • www.jap.org 1574 MUSCLE ARCHITECTURAL ADAPTATION IN HUMAN QUADRICEPS tude of increase shown in that study might have resulted from In summary, we have confirmed previous findings of rapid their testing of muscle architecture with the knee flexed to 80°, muscle architectural adaptation in humans and show for the where fascicle angle would be smaller and changes possibly first time that the temporal responses of fascicle angle and harder to detect. We have also shown for the first time that length are not the same: changes in fascicle angle continue fascicle angle continues to increase as training progresses, at relatively linearly for the first few months of training, whereas least to the 10th week, where our measurements were com- fascicle length adapts rapidly and does not continue past the pleted. Previous studies have reported significant increases first few weeks. We have also shown that adaptations in after 14- and 16-wk training periods (1, 30), but the pattern of fascicle length are not influenced by contraction mode, but are adaptation had not been examined. Together, our data and most likely influenced by the training range of motion (i.e., those of others strongly suggest that fascicle angle increases fascicle strain); contraction velocity probably has little effect. continually, at least for the first few months of training. Given In contrast, fascicle angle seems to be inextricably linked to that increases in fascicle angle allow a greater amount of muscle hypertrophy. Interestingly, 3 mo of detraining was not contractile tissue to attach to the tendon and aponeurosis and sufficient for muscle thickness, fascicle angle, or fascicle that it promotes an increase in the AGR, which allows the length to return to baseline levels, and in fact there was a small rotating fibers the opportunity to work closer to their optimum increase (not significant) in fascicle length in detraining. Inter- (from both force-velocity and force-length perspectives), this estingly, the changes in fascicle length were closely associated increase in fascicle angle most probably contributes to the with shifts in the torque-angle curve, and because the increases continuing increase in strength over the first months of resis- were essentially the same in both training groups it is likely tance training. that the training range of motion was the most significant Interestingly, changes in VM were typically of lesser mag- influencing factor. Whether the length range of force produc- nitude (8.2%) and more variable. The VM has a complex tion or the absolute muscle length is the greater stimulus cannot architecture (8, 51) and is probably activated differently from be determined from our data; however, we can confirm that the VL, and its activation adaptation progresses differently with genetic and/or signaling basis for fascicle length adaptations is training (21, 22, 44, 45). Our data show that the adaptations in different from that for muscle hypertrophy/fascicle angle ad- fascicle angle are not always consistent between the two aptation in humans. muscles and that the response of VM has more interindividual variability. This is the first study examining changes in synergist muscles with training in humans, so it is not clear whether REFERENCES such intermuscular differences occur routinely. Nonetheless, 1. 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