Human balance, the evolution of bipedalism and dysequilibrium syndrome

https://doi.org/10.1016/j.mehy.2006.01.042Get rights and content

Summary

A new model of the uniqueness, nature and evolution of human bipedality is presented in the context of the etiology of the balance disorder of dysequilibrium syndrome. Human bipedality is biologically novel in several remarkable respects. Humans are (a) obligate, habitual and diverse in their bipedalism, (b) hold their body carriage spinally erect in a multisegmental “antigravity pole”, (c) use their forelimbs exclusively for nonlocomotion, (d) support their body weight exclusively by vertical balance and normally never use prehensile holds. Further, human bipedalism is combined with (e) upper body actions that quickly shift the body’s center of mass (e.g. tennis serves, piggy-back carrying of children), (f) use transient unstable erect positions (dance, kicking and fighting), (g) body height that makes falls injurious, (h) stiff gait walking, and (i) endurance running. Underlying these novelties, I conjecture, is a species specific human vertical balance faculty. This faculty synchronizes any action with a skeletomuscular adjustment that corrects its potential destabilizing impact upon the projection of the body’s center of mass over its foot support. The balance faculty depends upon internal models of the erect vertical body’s geometrical relationship (and its deviations) to its support base. Due to the situation that humans are obligate erect terrestrial animals, two frameworks – the body- and gravity-defined frameworks – are in constant alignment in the vertical z-axis. This alignment allows human balance to adapt egocentric body cognitions to detect body deviations from the gravitational vertical. This link between human balance and the processing of geometrical orientation, I propose, accounts for the close link between balance and spatial cognition found in the cerebral cortex. I argue that cortical areas processing the spatial and other cognitions needed to enable vertical balance was an important reason for brain size expansion of Homo erectus. A novel source of evidence for this conjecture is the rare autosomal recessive condition of dysequilibrium syndrome. In dysequilibrium syndrome, individuals fail to learn to walk bipedally (with this not being due to sensory, vestibular nor motor coordination defects). Dysequilibrium syndrome is associated with severe spatial deficits that I conjecture underlie its balance dysfunction. The associated brain defects and gene mutations of dysequilibrium syndrome provide new opportunities to investigate (i) the neurological processes responsible for the human specific balance faculty, and (ii) through gene dating techniques, its evolution.

Introduction

Humans are biologically novel in several respects including language, dexterity and complex culture. One trait which tends to get overlooked is bipedality. This is perhaps because two legged locomotion is biologically common. However, the manner in which humans stand, walk and run only occurs in our own species.

Briefly, the human body is arranged vertically such that the head, trunk, legs and feet and their links in the neck, spine, pelvis, knees, and ankles dynamically balance together to form an upright “antigravity pole”. Since these segments and their points of articulation are not fixed, and the downward force of gravity never stops, the erect body exists always an inch or two away from falling. There is no locomotive use of holds, as with other primates. That the body is constantly upright is due to the unending skeletomuscular adjustment of posture (in the manner of a segway scooter or iBOT wheelchair). The habitual stance of no other animal has this total dependence upon the maintenance of vertical balance.

Here I propose a new theory about the nature and evolutionary uniqueness of the balance faculty responsible for human erectness, and the etiology of a rare autosomal recessive condition, dysequilibrium syndrome, in which this balance faculty is developmentally defective. The core of my theory concerns the evolution of a novel addition to the primate balance processes that enables humans to engage in their proficient bipedality: the internal models of the nongravitational z-axis body image.

The separate processing of gravitational and nongravitational information by the human balance faculty has already been established by neurologists [1], [2], and by those studying the biomechanics of human balance [3]. Building upon this, I propose that:

  • (a)

    the z-axis body image arose from the unique geometrical situation of terrestrial bipeds. In such bipeds, the constant perpendicular uprightness of body axis to the ground support (egocentric geometry) is put in direct alignment with the gravitational vertical (allocentric geometry);

  • (b)

    that the advantages of this alignment only came to be fully exploited for balance when hominid brain size expanded with the evolution of Homo erectus;

  • (c)

    that it has a close integration with higher cognition. As a result, the bipedal balance faculty has the same species specific relationship to humans as other higher cognition dependent faculties such as language or dexterity;

  • (d)

    that it is a defect in this balance faculty that underlies the rare autosomal recessive balance disorder of dysequilibrium syndrome [4], [5], [6];

  • (e)

    and that the cognitive, neurological, and genetic impairments of dysequilibrium syndrome and other developmental balance disorders provides a window with which science can study the information processing, neurology and evolution of human bipedality.

Section snippets

Human bipedalism

Bipedalism, as a descriptive term for the use of two legs for standing and locomotion, can be applied to a variety of animals. These include, as an occasional method of locomotion, primates (such as macaques, chimpanzees, bonobos, gorillas), birds (in general, and as a specialization in flightless ones such as penguins, ostriches and emus), extinct reptiles (Tyrannosaurus rex), certain lizards and even cockroaches [7]. However, human bipedal posture and anatomy are unique in four fundamental

Internal models

If the body’s center of mass goes outside its base of support, body instability starts within 100 ms [21]. Since it takes longer than 100 ms for the brain to detect an instability and then make compensating changes to posture, well-organized balance corrections must be initiated in advance. The nature of such forward feed corrections will invariably be complex. Consider an arm lifted from the side of the body to reach an object. This will need the skeletomuscular system to slightly shift back the

Dysequilibrium syndrome

Given the central role of the balance faculty in human biped standing and locomotion, it might be expected that it could be impaired during developmental. The impairment of this faculty would, however, not underlie all individuals with balance problems since balance can also be affected by dysfunction to sensory input or the motor coordination needed to make balance adjustments.

Only one developmental condition exists that can be directly attributed to the central impairment of the balance

Is bipedally primary an anatomical adaptation?

The anatomy of primates, particularly apes, can readily adapt to bipedal locomotion, in spite of its evolution for quadrupedalism. As noted above, great apes as part of their locomotive repertory occasionally walk bipedally, and can even do this permanently following forelimb injury or developmental defect. In the opposite direction, the recent Turkish cases of dysequilibrium syndrome demonstrate that the human skeletomuscular framework though evolved for bipedality retains the ability to

Neurology

At present, acquired brain lesions have allowed neurologists to locate the gravitational and nongravitational components of human balance respectively to (i) the cerebellar-cerebral circuits centered upon the vestibular area in the posterior insular cortex, and (ii) the ventral posterior and lateral posterior nuclei of the posterolateral thalamus and the associated cortical projections [2]). MRI scans of the brain abnormalities of those with dysequilibrium syndrome will be able to confirm this

Acknowledgements

The author thanks Nick Humphrey, Rob Seymour and the past and present directors of CoMPLEX (LSE) and CPNSS (UCL) for their support and collaboration.

References (41)

  • H.O. Karnath et al.

    The neural representation of postural control in humans

    Proc Natl Acad Sci USA

    (2000)
  • H.C. Glass et al.

    Autosomal recessive cerebellar hypoplasia in the Hutterite population

    Dev Med Child Neurol

    (2005)
  • B. Hagberg et al.

    The dysequilibrium syndrome in cerebral palsy. Clinical aspects and treatment

    Acta Paediatr Scand Suppl

    (1972)
  • V. Schurig et al.

    Nonprogressive cerebellar disorder with mental retardation and autosomal recessive inheritance in Hutterites

    Am J Med Genet

    (1981)
  • R.M. Alexander

    Bipedal animals, and their differences from humans

    J Anat

    (2004)
  • A.H. Schultz

    Conditions for balancing the head in primates

    Am J Phys Anthropol

    (1944)
  • C.V. Ward et al.

    Human evolution and the development of spondylolysis

    Spine

    (2005)
  • M.W. Marzke

    Precision grips, hand morphology, and tools

    Am J Phys Anthropol

    (1997)
  • P.W. Hodges et al.

    Coexistence of stability and mobility in postural control: evidence from postural compensation for respiration

    Exp Brain Res

    (2002)
  • S. Vogel

    Comparative biomechanics: life’s physical world

    (2003)
  • Cited by (56)

    • Footedness and Postural Asymmetry in Amateur Dressage Riders, Riding in Medium Trot on a Dressage Simulator

      2021, Journal of Equine Veterinary Science
      Citation Excerpt :

      This difference was seen only during the braking phase of the walking stride [41], although the rider is not required to support their whole bodyweight in the stirrup it could be that increased stirrup force is required to brake the lateral roll of the body on the side of increased trunk lean. Humans as a biped are attuned to maintaining their centre of mass over the foot, and will therefore alter weight distribution over their feet to adjust to balance issues when the option is available [42-44] so it is likely that riders are using the stirrups and the feet to counterbalance trunk movement rather than the seat. The significant negative correlation between pelvic obliquity and shoulder tilt demonstrates that as the pelvis rotates in one direction, the shoulders will usually remain closer to central or tilt in the opposite direction, with 59% of the sample population showing the pelvic obliquity and shoulder tilt in opposite directions.

    • Evolution of bipedalism

      2020, Comparative Kinesiology of the Human Body: Normal and Pathological Conditions
    • Scoring system for optimal management of acute traumatic patellar dislocation: A multicenter study

      2020, Journal of Orthopaedic Science
      Citation Excerpt :

      Fourth, the causes of recurrence are multifactorial. Particularly, neuroproprioception may greatly influence recurrence because humans can adapt according to structure and movement via neuroproprioception [24]. Yet, in a clinical setting, there are no simple parameters for neuroproprioception; therefore, this was not included in the scoring system.

    View all citing articles on Scopus
    View full text