Firas Massaad, Thierry M Lejeune, Christine Detrembleur
Rehabilitation and Physical Medicine Unit, Université catholique de Louvain, Brussels, Belgium

https://doi.org/10.36866/pn.71.25

You are watching TV, when you suddenly notice a mass of brainy heads bobbing up and down in a walking crowd. Walking accounts for 20% of their energy budget and brainy heads account for another 20%. So why are these ‘expensive ’ heads moving further? Puzzled, you take a stroll while carefully holding a cup full of boiling coffee, and here with each step the coffee bobs up and spills out of your cup. Unconsciously, you flex your legs to walk smoothly; but why does this bobbing occur when you have the ability to walk flat?

Interestingly, this vertical bobbing was noticed 2400 years ago by Aristotle, who had a habit of walking around the lyceum while talking. He curiously stated in the first known written reference to walking analysis in 350 BC: ‘If a man were to walk parallel to a wall in sunshine, the line described (by the shadow of his head) would be not straight but zigzag, becoming lower as he bends, and higher when he stands and lifts himself up’. Ironically, even his school was named later Peripatetic, meaning to walk up and down the shaded walks. Hence, could that be but a shadow?

Why do we bob up and down?

‘… man, the only erect animal …’

Aristotle again hinted, and indeed it is all in our legs. Humans walk on straight legs. Consequently, our body’s centre of mass (CM) rises as the supporting leg becomes vertical and descends again so as to arc upwards with each step (Fig. 1). This vertical movement enables humans to save energy by reducing the muscle work because we slow down as we rise and speed up as we fall, thus passively recovering kinetic energy into gravitational potential energy and back again as in an inverted pendulum (Cavagna, 1963). In straight walking, the line of action of our weight passes close to the leg joints, which also decreases the need for large forces in our leg muscles.

Human walking is unique so even the apes – our closest relatives – bend their legs when walking on two legs, which reduces the rise of the CM (i.e. flat gait) (Alexander, 1992). This is, however, paramount for arboreal locomotion because it enhances stability on branches. Accordingly, scientists postulated that our common ancestors with apes, approximately 7 million years ago (Ma), may also have walked flat as the first transition to terrestrial bipedality (Schmitt, 2003). However, recent computer modelling suggested that the australo-pithecines (represented by the 3.2 million year old ‘Lucy’) already walked straight and moved up and down. Therefore, our bobbing is more ancient than we previously thought.

We make war so that science may live in peace

Our CM kept out of the limelight until after the Second World War, when masses of people were lumbering with stiff straight legs, bobbing extensively and were out of breath. Suddenly, the realisation dawned that although relatively straight legs may save energy, the straighter we walk, the more we bob and the more energy we consume. Hence, a landmark article postulated that if humans walked flat like the CM of a wheel (Fig. 1), muscle work and energy consumption would be minimized because bouncy walking with excessive vertical bobbing would waste energy to redirect and raise the CM against gravity (Saunders et al. 1953). However, recent human experiments showed that flat walking costs more energy than normal walking (Ortega & Farley, 2005). Recent breakthrough in computer modelling also concluded that work requirements would be minimized by normal bobbing (Srinivasan & Ruina, 2006).

Why is our natural bobbing optimal?

Therefore, we asked healthy adults to walk on a treadmill (1 to 6 km h–1) while they were provided with their CM displacement feedback (Massaad et al. 2007). For each speed, they walked normally, with minimum vertical CM displacement (flat walking), and with maximum displacement (bouncy walking). We measured the total mechanical work provided by their muscles (Wtot), their oxygen consumption as energy cost (Cnet), their muscle efficiency (η=Wtot/Cnet), and the EMG activity for their leg muscles .We also calculated their vertical CM amplitude (Av) and the ‘recovery’ percent of mechanical energy exchanged between gravitational potential and kinetic energies of the CM.

The subjects were able to decrease Av in flat walking. However, Wtot was normal, Cnet nearly doubled with a sharp decrease in η (Fig. 2). In bouncy walking, Wtot and Cnet dramatically increased but η remained normal. In both flat and bouncy walking, the recovery decreased and muscle co-contraction timing increased (i.e. when antagonistic muscles are working against each other).

The optimal combination of ~3 cm in Av at ~ 4 km h–1 minimized Cnet, corresponding to normal human walking. In bouncy walking, Cnet increased slightly with a quite large increase of Av from the optimum, whereas in flat walking, Cnet was highly sensitive to reductions of Av (Fig. 3).

Wasteful flat, exuberant bouncy

Thus, the energy cost increased in both flat and bouncy walking. This increase was unexpectedly sharpest in flat walking where muscles provided little work but wasted energy. In bouncy walking, muscle provided extra work but conserved energy. Indeed, walking flat is like an experienced old man driving a rusty car using too much fuel although he drives straight, while bouncy walking is like a reckless teenager with a well-oiled car using the necessary fuel, but going through exuberant zigzags.

Despite the prediction of Srinivasan & Ruina’s model that normal walking would minimize work, we found no significant difference in work requirements between flat and normal walking. However, our muscles are inefficiently working in flat walking in opposition to bouncy walking. Therefore, not only do humans bob up and down in normal walking to save energy via a pendulum-like mechanism, as commonly thought since the 1960s, but they also load their muscles more efficiently this way.

Efficient locomotion is when most of the metabolic energy input is transformed into mechanical work. Flat walking like a wheel (the most efficient tool of motion) is inefficient probably because energy losses may have occurred due to muscle co-contraction and the need for high muscle forces due to flexed legs. However, in bouncy walking, the muscle co-contraction did not affect muscle efficiency. Hence, it seems that efficiency determinants remain a mystery because it is not yet possible to measure the force and the energy consumed by individual muscles during walking. Would another war resolve this mystery?

Efficiency was settled first

Even after probably 7 million years of ancestry with apes, we are still close to a flat walking (Fig. 3). This suggests that reducing our bobbing is indeed important, but to certain limits. Nature may ultimately have chosen the best compromise between safe flat locomotion that requires little work and bouncy ‘risky’ locomotion that turns walking into a ‘series of falls’ but improves muscle efficiency.

Straight legs are efficient. This was probably a primary criterion likely achieved if the short ‘Lucy’ already walked straight. The increase in leg length seen in H. erectus 1.8 Ma would have made it possible to cover longer distances more effectively at high speeds. Thus, nature may have maximized muscle efficiency (rusty to well-oiled) millions of years before reducing energy consumption at higher speed which was probably vital. This recalls Peter Drucker’s famous quotes: ‘Efficiency is doing better what is already being done’… ‘Efficiency is doing things right; effectiveness is doing the right things’. He was obviously not the first father of management!

Carefree of age, our CM is heading the future

Mankind specialization is basic as vertical bobbing appeared since quadrupedal terrestrial locomotion emerged ~400 Ma (i.e. since legs were adopted). However, early sprawling vertebrates like salamanders lumbered and bobbed excessively than cursorial animals that move gracefully like dogs; hence, our perception of lumbering exists (Reilly et al. 2006).

Modern humans, however, take advantage of both flat and bobbing walking. They shortcut millions of years of evolution in a few seconds to carefully hold their beloved coffee and walk flat to achieve impressive walking speeds in competition. Our natural bobbing is also used to generate electricity to power portable devices and is now tracked by satellites to assess human walking in daily life.

Recent humanoid robots also rival human walking by bobbing with simple control of actuators while some state-of-the-art robots still use sophisticated motor control to walk flat with excessive energy consumption. This echoes what we have found as physiological determinants of optimal bipedalism.

In conclusion, our results showed that our natural bobbing loads our muscles efficiently. This may have a direct implication in robotics to walk flat no longer and rehabilitation of pathological gait to bob excessively no longer either. You may now wonder how disastrous it would be for future humans to walk while holding their coffee if they were heading towards further head bobbing. However for now, 2400 years after Aristotle, we can eventually assert that our bounciness is not but a walking shadow (Fig. 4). Still, like Shakespeare, we say ‘Life is but a walking shadow.’

Acknowledgements

This work was funded by the Belgian Fonds National de la Recherche Scientifique and the grant of a ‘Coopération au Développement ’ fellowship from the UCL. We thank M Roegiers for her skilful help in graphic design and S Hatem for her insightful reading of this paper. We are also grateful to R McNeill Alexander for his precious comments on our article in The Journal of Physiology.

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