(adapted from section 5, "Respiratory, postural and spatio-kinetic motor stabilization, internal models, top-down timed motor coordination and expanded cerebello-cerebral circuitry: a review".)
While the term “dexterity” is exclusively used of humans, the term “bipedality” is not. The simple act of positioning the body on two legs is widespread amongst terrestrial vertebrates (Alexander 2004). Humans are, however, unique amongst extant animals in three respects. Humans use
(i) a biped bauplan (literally “building plan”) based upon anatomical vertical alignment (Borelli 1989/1680, proposition CXXXV),
(ii) this fully extended upright posture is strongly robust against vigorous or disruptive perturbation, including those that occur when such bipedality is combined with expert upper body actions (such as accurate throwing, carrying saucers of easily spilt fluids), or when footing is temporarily or potentially lost (during trips and fights), and
(iii) this upright arrangement is constantly accompanied by an unconscious musculoskeletal “dance” of anticipatory and feedforward postural adjustments (Belen'kii, Gurfinkel et al. 1967; Gelfand, Gurfinkel et al. 1971; Gurfinkel, Kots et al. 1971; Cordo and Nashner 1982; Bouisset and Zattara 1987; Massion 1992; Hodges, Gurfinkel et al. 2002).
Here it is argued that it is the uniquely enhanced capacity of humans for predictive internal models that by enabling continuous timed stabilizing adjustments, that allows humans, and only humans, to uniquely stand and move their body carriage in fully extended vertical alignment. Further, and again uniquely, that this allows humans to have the capacity to engage with robust stability in secondary (and quick center of mass shifting) upper and lower body part expert actions. Whether, and far, these traits characterized Australopiths is also discussed.
Anatomical vertical alignment bauplan
The human body is structured nearly entirely upon the compressive anatomical arrangement of bones, ligaments, joints and cartilage support "pads" (menisci). As a result, the human body lacks flexion between each of the body carriage segments—head, thorax, thigh, shank—as they are stacked in vertical alignment above each other. The ankle and metatarsophalangeal articulation in the feet are the only joints that humans properly flex normally in standing stance, and in the ground contact stages of walking. In running, the knee also is flexed but this links to the separate factor in which the running leg functions as a shock absorber when it hits the ground (Nigg, Bahlsen et al. 1987). Remarkably, this anatomical vertical compressive alignment bauplan is not employed, even occasionally, by any other extant terrestrial biped. Penguins and meerkats (temporarily) may appear to be spinally erect but they balance with a tripod use of their tails, and their bodies and legs are, on close examination, in fact flexed. Changes to foot anatomy (which reduced its flexion and enhanced its compressive stability) suggest the full development of such alignment dates at least to 2.2-2.36 myr and early Homo (Gebo and Schwartz 2006).
In contrast to humans, all nonhuman bipeds (birds, extinct dinosaurs and primates) use a variety of flexion biped bauplan in which the body carriage segments are angled relative to each other. In the case of nonhuman primates when they occasionally stand or walk bipedally, their limbs are flexed and their thorax is bent forward (Okada 1985; Schmitt 2003; Alexander 2004). As a result, when upright they flex their legs and thorax in a "bent-knee, bent hip" or compliant manner (Okada 1985; Schmitt 2003; Alexander 2004). Even anatomically aligned ratites such as ostriches limit such alignment to only one of their four leg joints (their extended “knee”—actually the joint between their tibia and tarso-metatarsus), and this in spite of appearances is slightly flexed with its body weight being only partial transmitted compressively directly down the joint (personal communication, Jonas Rubenson). Large ≥900 kg “graviportal” quadruped animals (Gregory 1912) use alignment and compression but again this is confined to the legs, and they, of course, have the benefit of the stability that comes from a four cornered quadruped “support”.
Instability and bipedal risk of falls
Borelli (1989/1680) was the first to note that the anatomical vertical alignment bauplan is intrinsically unstable and so needs constant musculoskeletal adjustment if fall and injury are not to occur: “the erect position is unstable as a result of the slipperiness of the joints.... They [humans] need their muscles to correct displacements and prevent falling” Borelli (1989/1680: p. 130) (see also Skoyles submitted).
This lack of stability and the need for constant postural adjustment particularly in fast walking and running puts the body at risk of postural and locomotive interruption due to falls, and more importantly, creates the risk of severe leg injury, and as a result, temporary or even permanent immobilization. This is because the kinetic energy held in the upright adult human body compared to that needed to break a femur bone is “an order of magnitude greater than the maximum value of the work to fracture and nearly twenty times the average work to fracture (Lotz and Hayes 1990: p. 698). In addition to this, as humans get taller in stature, the strength of their long support bones fails to keep up in their osteological strength with the forces that impact upon them from standing height falls. A child can fall, for example, with only a bruise but an adult can suffer a substantial injury. (The effect is marked and nonlinear: osteological strength decreases at the square root relative to increased height; for a review of the riskiness of bipedally see Skoyles submitted).
Stability and engineering
The flexion biped bauplan, in contrast to anatomically aligned bipedality, provides opportunities for low-level self-stabilizing. When upright, putting support limbs or the body at an angle allows that shifts of the body’s center of mass over its support base can be corrected by changing slightly that angle. Even simple spring arrangements such as found in articulated (anglepoise) lamps can be arranged to do this automatically (French and Widden 2000). Not only does flexion allow this greater opportunity for quick equilibrium management, but flexed limbs and thorax, can be further initially angled such that preflexes and spinal adjustment reflexes are to optimal for aiding this automatic adjustment. This option to stabilize the upright body, however, does not exist if limbs and the thorax are not angled. Instead, the extended erect body to maintain its centre of mass over its feet must actively and constantly shift masses distant to the legs including changing the posture of the spine and thorax (Hodges, Gurfinkel et al. 2002). The need for such changes due to the precariousness of human unflexed uprightness is illustrated by the fact that they are even made to correct the shifts in the centre of mass projection created by respiration (Gurfinkel, Kots et al. 1971; Hodges, Gurfinkel et al. 2002).
Utility of the human bauplan
The anatomical vertical alignment bauplan of humans would not have arisen without advantages that compensate for its intrinsic instability and unsafeness. These are significant. Notably, humans can economically stand erect for long periods since they use only 7% more energy standing than when laying down; in contrast a 10 kg dog when quadrupedally standing uses 70% more than when supine (Abitbol 1988). This is because anatomical alignment does not require energy expenditure to maintain muscles in a state of flexion. A further utility of the anatomically aligned bauplan is that when walking, the stiff compressive axis through the upright body allows it to temporarily store potential energy (in the form of a raised center of mass at midstance) from forward kinetic energy (such locomotion is also known as strident or inverted pendulum walking) (Cavagna, Thys et al. 1976). In such strident walking, the stiff leg temporarily vaults up the mass of the body and so stores potential energy that can be reused to swing forth the leg to make the next step. In contrast, bent knee, bent hip walking used by other primates in their occasional bipedalism requires about four times the energy due to the need in addition to moving the body forward of maintaining flexed muscles in a constant state of tension (Sockol, Raichlen et al. 2007). There are also likely to be other advantages linked to enhanced maneuverability of the upper body (Skoyles, in preparation).
The existence of these advantages raises the problem of why evolution has only exploited them in one extant primate. Given the instability of bipedal anatomical alignment, this suggests that evolution has only found in the particular case of Homo, an effective means to balance constantly such an intrinsically unsteady and difficult to stabilize anatomical aligned posture, particularly when engaging in complex forms of bipedality such as rough ground running and doing upper body actions (such as carrying and throwing). It is suggested here that this was linked to brain expansion, and the consequently increased ability to constantly engage in top-down anticipatory postural adjustments.
Considerable controversy exists over the nature of Australopithecine terrestrial bipedality as to whether it was stiff gait (and so anatomically aligned) (Latimer 1991; Ohman, Krochta et al. 1997; Lovejoy 2006), or compliant (Susman, Stern et al. 1984; Stern 2000). Evidence arguing for anatomical alignment and stiff gait are musculoskeletal features such as femoral bicondylar angle, and the increase in total cancellous bone in primary joints of lower limbs (Latimer 2005). Another factor is the biomechanical modeling of the efficiency of hominin walking (Crompton, Yu et al. 1998). A further factor is that macaques after initial training in bipedal erect standing can be trained successfully in semi-anatomical aligned strident walking (Hirasakia, Ogiharab et al. 2004). This argues that the primate engagement in stiff gait walking is only to a limited extent related to lack of anatomical adaptation, otherwise it could not be acquired by behavioral modification as in macaques. This suggests other nonanatomical factors (such as ecological utility) are responsible for its hominin adoption, with anatomical changes being secondary to these behavioral ones.
The above listed instability factors are greatest for fast walking and running, that are specific to Homo. Foot anatomy of preHomo (unlike Homo) suggests that their feet (Berillon 2004; Gebo and Schwartz 2006) were not optimal for running, as was the lack of the lateral stabilization provided by a Homo-like gluteus maximus, (Lieberman, Raichlen et al. 2006). Bramble and Lieberman (2004) have identified diverse musculoskeletal adaptations needed for endurance running in Homo that are absent in preHomo hominins. Thus, the stabilization problem faced by Homo is much more severe than that faced by Australopiths. Since the balancing for slow walking can be acquired by modern trained bipedal macaques (Hirasakia, Ogiharab et al. 2004)), this level of postural stabilization is likely to be within the already existing postural capacities of preHomo brains.
Further, Australopiths were less at risk from falls than Homo.
These habitus factors (that Australopiths share with other apes) have been argued elsewhere (submitted) relate to the need to minimize the injury risk of arboreal falls. However, they would have also as a side consequence allowed Australopiths to be bipedal without also needing an highly developed capacity to stabilize the upright body. In contrast, Homo individuals when running without the protective habitus of earlier hominins and arboreal apes would place themselves at constant risk, given the body’s momentum, of immobilization if they slipped or tripped injuring a lower limb. Preventing this requires considerable motor skill not only in controlling body falls in such circumstances, but also the ability to integrate into locomotion visual and other information about the rough ground ahead to constantly make safe footings.
How might we understand Australopith bipedality? An important factor here is that human bipedality even in simple walking and standing radically changes after childhood as internal model competence expands, in terms of motor qualities such as greater postural robustness (Hirschfeld and Forssberg 1992), and stabilization of the head and vision (Assaiante and Amblard 1995). This changes involves a reorganization in how the erect body is controlled (Assaiante and Amblard 1995). An adult flexibly adapts their balance mobility across their head, upper arms, lower arms, hands, thorax and any held objects. However, they are "locked together" in children as they lack the sophisticated adult ability needed to stabilize and control all their separate degrees of freedom as a single kinematic mobility (Assaiante and Amblard 1995). Early Homo show minor anatomical changes such as to the distal femur at adolescence (Tardieu 1998) that suggest this change to a more sophisticated stabilization of balance only occurred in Homo evolution. The more simple "locked together" anatomical alignment found in modern children not present before Homo adolescence would have been adequate for the more limited locomotion needs of Australopiths. Thus, while anatomical aligned bipedality may be unique to hominins, the combination of this with highly developed internal model based postural adjustment might be a developmental limited to adult and adolescent Homo.
Vertical alignment bauplan, internal models and cerebello-cerebral circuits
Research since the 1960s shows that humans (as Borelli suggested three centuries earlier) stabilize their upright bodies by continuous musculoskeletal adjustment (Belen'kii, Gurfinkel et al. 1967; Gelfand, Gurfinkel et al. 1971; Gurfinkel, Kots et al. 1971; Cordo and Nashner 1982; Bouisset and Zattara 1987; Massion 1992; Hodges, Gurfinkel et al. 2002). In this, motor commands that will cause a forward displacement of body mass such as moving an arm forward to reach an object, are accompanied by top-down timed anticipatory postural adjustments that ensure that it is accompanied by an equal and opposite counter-positioning of body mass (Cordo and Nashner 1982). Not only do such adjustments stabilize the body but such timed postural submovements accompanying walking steps help to propel them and make locomotion more steady and efficient (MacKinnon, Bissig et al. 2007). Feedforward processes incorporating sensory inputs into internal models (Desmurget and Grafton 2000) are also likely to be particularly important, where anticipation is limited such when making stepping reactions if erectness is threatened (Zettel, McIlroy et al. 2002; Marigold, Bethune et al. 2003; Hughey and Fung 2005; Pai, Yang et al. 2006); and the organized control of body collapse so it falls in a manner that minimises injury (Hsiao and Robinovitch 1998).
Consistent with this dependence of human bipedality upon continuous timed postural adjustment, there is considerable evidence that normal human bipedality is supraspinal and involves the cerebellum working with the cerebral cortex. Dual-tasks, for example, show that postural adjustment requires cognitive resources used by other motor faculties such as vocal articulators (repeating syllables, talking) (Lundin-Olsson, Nyberg et al. 1997; Yardley, Gardner et al. 2000; de Hoon, Allum et al. 2003; VanderVelde, Woollacott et al. 2005), dexterity (Ebersbach, Dimitrijevic et al. 1995), and even higher cognitions such as spatial tasks, mathematics and Stroop (Woollacott and Shumway-Cook 2002; Hauer, Pfisterer et al. 2003; VanderVelde, Woollacott et al. 2005; Maki and McIlroy 2007). The close study of maintaining stance and walking shows that it is stabilized by central control (Morasso and Schieppati 1999), and involves cerebello-cerebral cortex circuits (Jacobs and Horak 2007; Maki and McIlroy 2007). It can include—if balance is particularly challenging—also the involvement of the prefrontal cortex, for example, when people walk on treadmills (Suzuki, Miyai et al. 2004), or if a person stands in a virtual reality that lacks visual clues as to the floor and the ceiling (Slobounov, Wu et al. 2006). People can motor empathize with the postural upright stability in other individuals (Slobounov, Tutwiler et al. 2000; Cheng, Tzeng et al. 2005), and this occurs through cortical mirror neurons (Cheng, Tzeng et al. 2005). This is all suggestive or consistent with a dependence upon postural adjustment based upon cerebello-cerebral cortex predictive internal models.
Noninternal model bipedal alternatives
Anticipatory postural adjustments and such internal model based top-down stabilization, it needs to be noted, is not required, however, for all forms of bipedal stiff standing and walking. Mechanical toys and robots can be designed such that their passive mechanical properties can cause them to walk in a human-like stiff manner on flat surfaces (Fallis 1888; Collins, Ruina et al. 2005). Empirical research suggests that stable upright posture can be achieved with only an open loop ankle stiffness control (Winter, Patla et al. 1998), or a closed loop involving muscle spindle and monosynaptic spinal feedback mechanisms (He, Levine et al. 1991). Robots have even been designed that can recover from perturbations during walking with only open loop methods of stabilization (Mombaur, Bock et al. 2005). Consistent with this, people with cerebellar agenesis or cerebellar dysfunction (developmental, lesion, or alcohol intoxication) can stand and walk with compromised supraspinal processes (Titomanlio, Romano et al. 2005, see particularly the associated video to this case report), as can those with spinal cord injuries when given partial hoist support following intensive multi-year physiotherapy (van Hedel, Wirth et al. 2005).
However, from an evolutionary perspective, the existence of such non-top-down supraspinal internal model based bipedal stabilization mechanisms is less relevant than it might appear. This is because such mechanisms are too limited in their perturbation resistance to enhance an individual’s survival fitness, as would have happened when the evolution of human motor abilities occurred during the Pleistocene. People who are “drunk”, for example, maybe able to stand and walk but such inebriated individuals lack exact temporal organization in their movements, and as a result, they are, in many respects disabled, as they easily fall, or are limited in what they can do in a stable manner. Modern human locomotion, moreover, is much easier in terms of maintaining upright balance than it was in Pleistocene times: the modern walking environment is mostly paved, flat, often carpeted, and kept clear of footing hazards by health and safety legal requirements to minimize accidents. In contrast, the Pleistocene environment was rough and full of unexpected footing hazards that could potentially trip or slip up walkers and runners. The concern in this review is exclusively with the processes that enable the exquisite and highly robust balance shown by human adults when engaged in evolutionarily exacting upper body biped skills (such as accurate throwing), or challenging circumstances (avoiding trips and slips where there are footing hazards as when rough ground running), as only these are relevant to the past selection of human specific bipedal motor functions.
Summary of human bipedality and internal models
This brief discussion of human bipedality provides preliminary evidence to suggest that like dexterity, its uniqueness derives from anticipatory timed motor stabilization based upon internal models. Another source of evidence is that neuroanatomically, like dexterity, lesion and neuroimaging shows that it depends upon the cerebello-cerebral cortex circuits (Morton and Bastian 2004; Ioffe, Chernikova et al. 2007; Jacobs and Horak 2007; Maki and McIlroy 2007) including prefrontal ones (Suzuki, Miyai et al. 2004; Slobounov, Wu et al. 2006) that underlie such internal models.
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