The 'muscular wisdom' fatigue hypothesis: historical perspectives and contemporary challenges

Identifying mechanisms of force loss (i.e., muscle fatigue) has been of long-standing interest. The muscular wisdom hypothesis (promulgated circa 1970) states the declining motor unit firing rates during a sustained maximal voluntary contraction do not contribute to force loss, but rather, i) lower rates provide appropriate excitation as contractile speed slows with fatigue, and ii) provides protection against peripheral conduction failure. This theory was predominant until further scrutiny and experimental evidence in the ensuing decades made it less clear whether the hypothesis was justified properly. Therefore, a central tenet in our understanding is whether the declining firing rates observed during maximal contractions are causative or preventative of force loss. Here we provide a historical perspective of the studies antecedent to the original hypothesis and an up-to-date comprehensive review of the factors involved. Overall, we summarize and evaluate the evidence as to whether force loss during maximal contractions is due to inadequate neural input or impairments in peripheral contractility. Alterations in motor unit function, (as 'the final common pathway') are the focus to explore these concepts from an integrated approach. Although some aspects may have been originally overstated, due mostly to a lack of a fuller understanding of various factors at the time, we conclude the decline in motor unit firing rates are preventive and not causative of force loss during sustained maximal contractions. Overall, the muscle wisdom hypothesis is a classic example of the capable adjustments in response to stress by mitigating impairments at one site through adaptations at another.