Physiological cost of negative muscular work in humans and in isolated muscles: a search for mechanism

It is easier to walk downhill than uphill. When walking uphill, muscles are shortening and doing work. When walking downhill, the same muscles are stretched. These lengthening muscles are said to be doing "negative work." Why do lengthening contractions utilize less energy than shortening contractions generating the same force? In search for an answer to this question, A. V. Hill and his collaborators preformed experiments measuring the mechanics and energetics of isolated muscles that were stretched during contraction (Abbott BC, Aubert XM, Hill AV. <i>Proc R Soc Lond B Biol Sci</i> 139: 86-104, 1951) and intact muscles that were stretched during human exercise (Abbott BC, Bigland B, Ritchie JM. <i>J Physiol</i> 117: 380-390, 1952). There was at first a false trail based on an incorrect hypothesis. The key to understanding why muscles doing negative work utilize less energy than muscles doing the same amount of positive work is that muscle fibers that are stretched generate more force than shortening muscle fibers while using less energy. Thus, to generate an equal amount of positive and negative work requires activation of more shortening muscle fibers utilizing more energy per fiber than fibers being stretched. This is a fascinating scientific and human-interest story that started with a very colorful demonstration one evening at a soiree of the Royal Society London in 1951.<b>NEW & NOTEWORTHY</b> It is easier to walk downhill than uphill. When walking uphill, muscles are shortening and doing work. When walking downhill, the same muscles are stretched. Why do lengthening contractions utilize less energy than shortening contractions generating the same speed and force? The key to answering this question is that muscle fibers that are stretched generate more force than shortening muscle fibers while using less energy. Thus, to generate an equal amount of positive and negative work requires activation of more shortening muscle fibers utilizing more energy per fiber than fibers being stretched.