Muscles do more positive than negative work in human locomotion

Abstract

Muscle work during level walking and ascent and descent ramp and stairway walking was assessed in order to explore the proposition that muscles perform more positive than negative work during these locomotion tasks. Thirty four healthy human adults were tested while maintaining a constant average walking velocity in the five gait conditions. Ground reaction force and sagittal plane kinematic data were obtained during the stance phases of these gaits and used in inverse dynamic analyses to calculate joint torques and powers at the hip, knee and ankle. Muscle work was derived as the area under the joint power vs time curves and was partitioned into positive, negative and net components. Dependent t-tests were used to compare positive and negative work in level walking and net joint work between ascent and descent gaits on the ramp and stairs (P<0.010). Total negative and positive work in level walking was -34 J and 50 J, respectively, with the difference in magnitude being statistically significant (P<0.001). Level walking was therefore performed with 16 J of net positive muscle work per step. The magnitude of the net work in ramp ascent was 25% greater than the magnitude of net work in ramp descent (89 vs -71 J m(-1), P<0.010). Similarly, the magnitude of the net work in stair ascent was 43% greater than the magnitude of net work in stair descent (107 vs -75 J step(-1), P<0.000). We identified three potential causes for the reduced negative vs positive work in these locomotion tasks: (1) the larger magnitude of the accelerations induced by the larger ground reaction forces in descending compared to ascending gaits elicited greater energy dissipation in non-muscular tissues, (2) the ground reaction force vector was directed closer to the joint centers in ramp and stair descent compared to ascent, which reduced the load on the muscular tissues and their energy dissipating response, and (3) despite the need to produce negative muscle work in descending gaits, both ramp and stair descent also had positive muscle work to propel the lower extremity upward and forward into the swing phase movement trajectory. We used these data to formulate two novel hypotheses about human locomotion. First, level walking requires muscles to generate a net positive amount of work per gait cycle to overcome energy losses by other tissues. Second, skeletal muscles generate more mechanical energy in gait tasks that raise the center of mass compared to the mechanical energy they dissipate in gait tasks that lower the center of mass, despite equivalent changes in total mechanical energy.

Figures

Fig. 1

Joint powers in shoulder (A) and squat (B) movements. Both cyclic activities had positive and negative joint powers that were associated with lowering and raising either one upper extremity or all body mass above the ankles. (C) Total positive and negative joint work were virtually identical in the negative and positive phases of the shoulder and squat tasks (i.e. differences were less than 1%). These data strongly suggest that positive and negative joint and muscle work can be equivalent in certain uni- and multi-joint, cyclic movements.

Fig. 2

(A,C) Summed joint torque (A) and joint power (C) and (B,D) individual hip (broken line), knee (solid line) and ankle (dotted line) joint torques (B) and joint powers (D) during the stance phase of level walking averaged across all subjects. Positive torques are extensors and positive powers are energy generation. Summed torque showed extensor bias throughout most of stance that was produced primarily by hip and knee extensor torques in early stance and ankle plantarflexor torque in late stance. Individual joint powers showed that each joint torque generated and dissipated energy during the stance phase. Summed joint power showed alternating positive and negative work phases, with the largest power magnitude being the positive power in late stance.

Fig. 3

Mean hip, knee, ankle and total joint work in level walking across all subjects. Values are means ± s.d. Muscles at each joint produced both negative and positive work during the stance phase of level walking. Net work was negative at the knee but positive at the hip and ankle. Total net work was positive at 16.2 J. The magnitudes of negative and positive work were significantly different at each joint; the asterisk indicates the larger value (P<0.010).

Fig. 4

Individual and summed joint torque (A) and power (B) curves during the stance phases of ramp descent (broken lines) and ascent (solid lines) walking, averaged across all subjects. Positive torques are extensors and positive powers are energy generation. Summed torques were similar in shape and magnitude and showed that both gaits were produced by net extensor torques across all joints. Hip and ankle extensor torques were larger in ascent vs descent, whereas knee extensor torque was larger in descent. Summed powers in ramp descent and ascent were nearly entirely negative and positive, respectively. The individual joint powers, however, showed that muscles crossing each joint contributed both negative and positive power and work to both movements. Negative power occurred primarily at the knee and then ankle joints in descent whereas positive power occurred primarily at the ankle and hip joints in ascent. Ramp descent had a 15% shorter stance phase, partially leading to reduced area under the joint power curves and reduced muscle work compared to ramp ascent.

Fig. 5

Mean joint work in ramp gait across all subjects. Values are means ± s.d. Knee muscles were the primary energy dissipaters in ramp descent, performing 58% and 81% of the negative and net muscular work, respectively. Ankle and hip muscles were the primary energy generators in ramp ascent combining to perform 86% and 95% of the positive and net work, respectively. Negative work in ramp ascent was relatively evenly distributed among the muscle groups, whereas positive work in descent was produced primarily (i.e. 62%) by the ankle muscles.

Fig. 6

Individual and summed joint torque (A) and power (B) curves during the stance phases of stair descent (broken lines) and ascent (solid lines) walking averaged across all subjects. Positive torques are extensors and positive powers are energy generation. Summed torques were similar in shape and showed that both gaits were produced by net extensor torques across all joints. Hip and ankle torques were similar in the stair gaits, whereas knee torque had one larger extensor phase in ascent and two smaller extensor phases in descent. As in ramp gait, summed powers in stair descent and ascent were nearly entirely negative and positive, respectively. In contrast to ramp gait, there was minimal power and work at the hip on the stairs. Energy dissipation in stair descent was done at the ankle joint in early stance and at the knee joint in later stance. Stair ascent was produced by positive power and work at the knee joint in early stance and at the ankle joint in later stance. Stair descent had an 8% shorter stance phase, partially leading to reduced area under the joint power curves and reduced muscle work compared to stair ascent.

Fig. 7

Mean joint work in stair gait across all subjects. Values are means ± s.d. Knee and ankle muscles were the primary energy dissipators and generators in stair descent and ascent. They performed 92% and 95% of the negative and net muscular work in descent, respectively and 85% and 87% of the positive and net muscular work in ascent, respectively. As in ramp walking, negative work in ramp ascent was relatively evenly distributed among the muscle groups, whereas positive work in descent was produced primarily (i.e. 73%) by the ankle muscles.

Fig. 8

Mean total joint work in both ascending and descending gaits (in |J| m−1 for ramp, and |J| step−1 for stairs) across all subjects. Values are means ± s.d. Ascent work was 25% (*P<0.010) and 43% (*P<0.000) greater than descent work in ramp and stair gait, respectively.

Fig. 9

Mean normal GRFs (N) for ramp and stairway walking averaged across all subjects. Descending gaits had larger first maximum forces and greater rates of force application during the initial portion of the stance phase. These forces produced higher accelerations of the body mass compared to those in the ascending gaits.