Coordination amongst quadriceps muscles suggests neural regulation of internal joint stresses, not simplification of task performance

Significance Our study overturns a common hypothesis about how the nervous system produces movement. According to this hypothesis, muscles with complementary contributions to overt task performance (e.g., similar joint torques and endpoint forces) are controlled as a single functional unit, often referred to as a “muscle synergy,” and so the activation of muscles with similar task-related actions should strongly covary. Our results do not support this hypothesis and, instead, suggest that covariation patterns amongst muscles better reflect the control of low-level aspects of limb mechanics, such as the stresses and strains within joints. In addition to arguing against this standard interpretation of muscle covariation patterns, our experiments also highlight the critical role of the nervous system in regulating internal joint mechanics. Many studies have demonstrated covariation between muscle activations during behavior, suggesting that muscles are not controlled independently. According to one common proposal, this covariation reflects simplification of task performance by the nervous system so that muscles with similar contributions to task variables are controlled together. Alternatively, this covariation might reflect regulation of low-level aspects of movements that are common across tasks, such as stresses within joints. We examined these issues by analyzing covariation patterns in quadriceps muscle activity during locomotion in rats. The three monoarticular quadriceps muscles (vastus medialis [VM], vastus lateralis [VL], and vastus intermedius [VI]) produce knee extension and so have identical contributions to task performance; the biarticular rectus femoris (RF) produces an additional hip flexion. Consistent with the proposal that muscle covariation is related to similarity of muscle actions on task variables, we found that the covariation between VM and VL was stronger than their covariations with RF. However, covariation between VM and VL was also stronger than their covariations with VI. Since all vastii have identical actions on task variables, this finding suggests that covariation between muscle activity is not solely driven by simplification of overt task performance. Instead, the preferentially strong covariation between VM and VL is consistent with the control of internal joint stresses: Since VM and VL produce opposing mediolateral forces on the patella, the high positive correlation between their activation minimizes the net mediolateral patellar force. These results provide important insights into the interpretation of muscle covariations and their role in movement control.