Chasing footprints in time – reframing our understanding of human foot function in the context of current evidence and emerging insights

In this narrative review we evaluate foundational biomechanical theories of human foot function in light of new data acquired with technology that was not available to early researchers. The formulation and perpetuation of early theories about foot function largely involved scientists who were medically trained with an interest in palaeoanthropology, driven by a desire to understand human foot pathologies. Early observations of people with flat feet and foot pain were analogized to those of our primate ancestors, with the concept of flat feet being a primitive trait, which was a driving influence in early foot biomechanics research. We describe the early emergence of the mobile adaptor–rigid lever theory, which was central to most biomechanical theories of human foot function. Many of these theories attempt to explain how a presumed stiffening behaviour of the foot enables forward propulsion. Interestingly, none of the subsequent theories have been able to explain how the foot stiffens for propulsion. Within this review we highlight the key omission that the mobile adaptor–rigid lever paradigm was never experimentally tested. We show based on current evidence that foot (quasi-)stiffness does not actually increase prior to, nor during propulsion. Based on current evidence, it is clear that the mechanical function of the foot is highly versatile. This function is adaptively controlled by the central nervous system to allow the foot to meet the wide variety of demands necessary for human locomotion. Importantly, it seems that substantial joint mobility is essential for this function. We suggest refraining from using simple, mechanical analogies to explain holistic foot function. We urge the scientific community to abandon the long-held mobile adaptor–rigid lever paradigm, and instead to acknowledge the versatile and non-linear mechanical behaviour of a foot that is adapted to meet constantly varying locomotory demands.     

The tenacity of the limpet, Patella vulgata L.: An experimental approach

It has been shown that adhesion of the limpet, Patella vulgata L. is influenced by both physical and physiological factors. The tenacity is sensitive to surface properties of the substratum, varying inversely with the contact angle which water makes with a substratum. This can be explained in terms of thermodynamics. Surface roughness also affects tenacity and this is explained in the same manner. Different angles of detachment were tested and it was clearly shown that when a strong peeling component was introduced, a much reduced force was needed to detach a limpet. Contrary to a normal pull, when a shear pull is exerted the force is not proportional to the surface area of the foot. It has also been shown that the speed of separation affects the measured tenacity; there is a speed at which tenacity will be maximum. The effect of water temperature on tenacity has been tested, tenacity increasing with rising temperature (7, 13, 20 °C). At the higher temperatures limpets are able to contract the foot muscles more powerfully, indicating that increased foot rigidity increases tenacity. By measuring the tenacity of limpets left out of water for different periods of time it has been shown that desiccation has no effect on tenacity, but a change from aquatic to aerial respiration increases tenacity. Tenacity has also been measured when the limpets have been subjected to a reduction in metabolic rate. The effect of both anoxia and narcotization shows that reduced muscle tonus, especially in the foot, results in decreased tenacity. These results further demonstrate that foot rigidity is essential for efficient adhesion. Eimpets from different habitats (exposed and sheltered) and vertical distribution (high and low level on shore) exhibited no differences in tenacity. During locomotion limpets leave a mucous trail, most of the mucus being confined to the edge of the trail. Water is incorporated anteriorly under each new locomotory wave and these pockets of water are used to release the mucus from the substratum during locomotion. It is concluded from this study that limpet adhesion can be explained solely by the tackiness of the pedal mucus, tack being due to the stored elastic energy within the mucous layer itself.     

Mechanics of locomotion of dogs (Canis familiaris) and sheep (Ovis aries)

Records have been made of the forces exerted on the ground by dogs and a sheep, in walking, trotting, cantering and slow galloping. Film has been taken simultaneously. The difference between walking and trotting was much less marked for the sheep than for the dogs.
Step length and stride length increase as speed increases. They are expressed as functions of the Froude number.
The vertical component of the force exerted by a foot on the ground shows two main maxima in walking, except in the case of the fore feet of sheep. In this case and in other gaits there is only one main maximum. The vertical movements of the fore and hind quarters which occurred in examples of each gait have been calculated from the force records.
The force exerted by a foot on the ground changes direction in the course of a step so as to remain more or less in line with a point fixed relative to the animal, but dorsal to its back.
The force records show impact disturbances in the first 003 sec of contact of each foot with the ground.
The point of application of the force on the sole of a foot tends to move posteriorly as the force increases.
The results are discussed in relation to a theoretical account of the mechanics of locomotion on legs.     

The architecture of the shoulder in some mammals

A series of nine features of the shoulder girdle, chosen as having functional significance in relation to the movements of the shoulder in arboreal locomotion, have been studied in 1188 specimens of 194 genera of mammals. The features were defined metrically and examined by means of a multivariate statistical technique: viz. canonical analysis. The study has shown that those mammals which are nonarboreal differ considerably among themselves and form the arboreal forms. But the myriad shapes of the shoulder girdle in a wide range of mammals (e.g. some marsupials, edentates, rodents, carnivores and primates) which climb or forage in trees, can be summarized mathematically by a very small number of similar canonical variates. This information correlates well with that of a previous series of studies carried out on the primates alone. The biological information that was postulated as being reflected by the individual canonical variates for the primates is also apparent for the arboreal mammals. The different variates separate the forms in ways which are consonant with what is known about the function of the shoulder in locomotion. Aspects of the shape of the shoulder defined by the analysis appear to be discernible from an examination of the contribution of the original variables to each individual canonical variate. This seems to confirm that the shape of the shoulder girdle within a very wide range of mammals is limited by a very small number of underlying factors of biological significance. One interpretation of the results suggests that the genetic model of the mammalian shoulder may have been sufficiently fixed at an early stage in the evolution of the class as to place considerable constraints upon the subsequent evolution of the shoulder in the different Orders.     

Peristaltic waves of tubicolous worms and the problem of irrigation in Sabella pavonina

A simple scheme is presented to illustrate four possible kinds of locomotory peristalsis in worm-like animals. The application of this scheme to real animals is discussed. Peristaltic waves may be of constriction or dilatation. A continuous body cavity enables the worm to regulate both speed and direction of travel by controlling the relative tonus of its body wall muscles. Thus peristaltic waves can be used to pump water without causing locomotion.
Sabella irrigates its tube by peristaltic swellings but the coelom and intestine are sub-divided by entire septa. Anatomical and morphological features which allow the shortest, widest segments forming a "piston" to slide down the tube and the narrower elongated segments to grip its walls are considered. In this way the construction of the typical body segment is given a functional explanation.
The functions of septa in annelids are discussed.     

Laryngotracheal morphology of Afro-Madagascan geckos: a comparative survey

The structural variation of the gekkonid larynx and trachea is examined within a representative subset of 17 species of Afro-Madagascan gekkonines to determine if there are underlying morphological correlates of vocalization. The documented morphology is compared to that of the tokay (Gekko gecko), which has previously been described. Data were obtained from gross anatomical observations, scanning electron microscopy, histological examinations and computer-generated, three-dimensional, skeletal reconstructions. Although there is limited variation among most Afro-Malagasy gekkonids, the larynges of Ptenopus garrulus and Uroplatus fimbriatus exhibit marked degrees of differentiation, suggesting that laryngeal and tracheal morphology may account for the documented vocal variability of gekkonid lizards. Cladistic analyses indicated that parallel adaptive trends characterize the laryngeal morphology of the examined taxa. Alternate designs and refinements to a model of gekkonid phonation are presented, and the evolution of acoustic communication in the Gekkonidae is considered.     

Serotonin modulates locomotory behavior and coordinates egg-laying and movement in Caenorhabditis elegans.

Biogenic amines have been implicated in the modulation of neural circuits involved in diverse behaviors in a wide variety of organisms. In the nematode C. elegans, serotonin has been shown to modulate the temporal pattern of egg-laying behavior. Here we show that serotonergic neurotransmission is also required for modulation of the timing of behavioral events associated with locomotion and for coordinating locomotive behavior with egg-laying. Using an automated tracking system to record locomotory behavior over long time periods, we determined that both the direction and velocity of movement fluctuate in a stochastic pattern in wild-type worms. During periods of active egg-laying, the patterns of reversals and velocity were altered: velocity increased transiently before egg-laying events, while reversals increased in frequency following egg-laying events. The temporal coordination between egg-laying and locomotion was dependent on the serotonergic HSN egg-laying motorneurons as well as the decision-making AVF interneurons, which receive synaptic input from the HSNs. Serotonin-deficient mutants also failed to coordinate egg-laying and locomotion and exhibited an abnormally low overall reversal frequency. Thus, serotonin appears to function specifically to facilitate increased locomotion during periods of active egg-laying, and to function generally to modulate decision-making neurons that promote forward movement.     

Chimpanzee bipedal locomotion in the Gombe National Park,East Africa

An adult male chimpanzee in the natural habitat has been observed to walk predominantly bipedally after a total forelimb paralysis in 1966. The major differences from previously described bipedal chimpanzee gait are (1) one third of the femoral extension is posterior to the hip joint in propulsion, (2) excursion of the swinging foot is close to midline, due to adduction of the lower hindlimb in swing and propulsive phases, (3) depressed pelvic tilt is on the side of the swinging limb, (4) thoracic vertebrae rotate and are vertical and erect, and (5) there is only a moderate lateral sway of the midline. This locomotory complex is interpreted as individual variability and suggests an evolutionary model for the origin of hominid bipedal locomotion.     

L'Organisation Ultrastructurale Corticale de la Gregarine Lecudina pellucida; ses Rapports avec l'Alimentation et la Locomotion

SYNOPSIS. The structure of the cortical region (epicyte and ectoplasm) of the gregarine Lecudina pellucida , an intestinal parasite of the polychete worm Perinereis cultrifera was studied by electron microscopy.
The epicitary folds have 3 unit type membranes. Between the 1st and 2nd is a layer probably composed of fine longitudinal fibrils which has an arch-like or gutter-like structure at the crest of the folds. Inside these folds is cytoplasm without any noticeable differentiation or inclusion except for a granular (or finely fibrillar) layer under the limiting inner membrane and close to it.
The ectoplasmic zone of the entocyte is separated from the epicitary region by a lengthwise discontinuous cylindrical opaque layer, inwardly tangential to the folds. The ectoplasm lacks paraglycogen granules but has various organelles: apparently pinocytic vesicles against the wall between the folds, vesicles with myelinic membranes, opaque granules, a few mitochondria with blistered internal vesicles, and a few circular tubular fibers.
The superficial zone of the gregarine is supposed to contribute to nutrition, thru the extensive surface furnished by its folds and thru the pinocytic vesicles; but this alimentary intake is incomplete compared with that of the previously studied anterior region.
Insufficient mucus is discharged to account for locomotion. There are some circular ectoplasmic fibers, but locomotory myonemes are completely absent. However, there are deformations of the folds and corresponding waves that could account for locomotion by creeping or swimming. These movements of the folds might be due to the action of the contractile proteins and correspond with some of the layers seen in the wall.     

Pre-adaptive plasticity in atherinids and the estuarine seat of teleost evolution

With the aid of models and selected examples, an analysis of speciation within the family Atherinidae is presented. This is a large family of pelagic fish, many members of which look strikingly similar. They are primarily a marine coastal group, favouring sheltered estuaries and lagoons, although in some regions they have invaded fresh waters.
Many atherinids show a high degree of intraspecific morphological variability which can be linked to their estuarine habitat. It is argued that estuarine and lagoonal environments are physically highly variable and this has acted to select for generalist genotypes able to adjust their morphology, physiology and behaviour to a wide range of conditions. Such plasticity pre-adapts atherinids to invade and rapidly speciate in fresh waters containing vacant niches. Examples of such invasions and speciation are presented, and the rate of evolution discussed.
The selective forces acting on atherinids should be common to other fish groups, suggesting that many freshwater fish may have estuarine ancestors. The influence of estuaries in evolution may be out of all proportion to their size.     

Evaluation of a patient-specific cost function to predict the influence of foot path on the knee adduction torque during gait

A large external knee adduction torque during gait has been correlated with the progression of knee osteoarthritis (OA). Though foot path changes (e.g. toeing out) can reduce the adduction torque, no method currently exists to predict whether an optimal foot path exists for a specific patient. This study evaluates a patient-specific optimization cost function to predict how foot path changes influence both adduction torque peaks. Video motion and ground reaction data were collected from a patient with knee OA performing normal, toe out, and wide stance gait. Joint and inertial parameters in a dynamic, 27 degree-of-freedom, full-body gait model were calibrated to the patient's normal gait data. The model was then used in gait optimizations that predicted how the patient's adduction torque peaks would change due to changes in foot path. The cost function tracked the patient's normal gait data using weight factors calibrated to toe out gait and tested using wide stance gait. For both gait motions, the same cost function weights predicted the change in both adduction torque peaks to within 7% error. With further development, this approach may eventually permit the design of patient-specific rehabilitation procedures such as an optimal foot path for patients with knee OA.     

F-actin assembly in Dictyostelium cell locomotion and shape oscillations propagates as a self-organized reaction-diffusion wave.

The crawling locomotion and shape of eukaryotic cells have been associated with the stochastic molecular dynamics of actin and its protein regulators, chiefly Arp2/3 and Rho family GTPases, in making a cytoskeleton meshwork within cell extensions. However, the cell's actin-dependent oscillatory shape and extension dynamics may also yield insights into locomotory mechanisms. Confocal observations of live Dictyostelium cells, expressing a green fluorescent protein-actin fusion protein, demonstrate oscillating supramolecular patterns of filamentous actin throughout the cell, which generate pseudopodia at the cell edge. The distinctively dissipative spatio-temporal behavior of these structures provides strong evidence that reversible actin filament assembly propagates as a self-organized, chemical reaction-diffusion wave.     

Development and morphological variation of the axial and appendicular skeleton in hylidae (Lissamphibia,Anura)

The axial and appendicular skeleton, the associated musculature and tendons form a functional system related to specific modes of locomotion in anurans. Many transformations in the structures linked with the locomotor function of the adult occur during larval stages and metamorphosis. In this study, we present the larval ontogeny and adult morphology of the axial and appendicular skeletons of 14 species of frogs in the family Hylidae with different locomotor modes and habitat uses. Among Hylidae, a diversity of shapes, locomotory types occurs (e.g., walker, swimmer, jumper, hopper) and different habitat types occupied (shrubby, terrestrial, aquatic, arboreal). Many elements complete differentiation at the end of metamorphosis; others, such as sesamoids, still show an incomplete development at that stage. Sixty seven characters were scored and optimized in an available phylogeny. Nine characters of developmental timing and adult osteology are optimized as synapomorphies of specific groups. Some characters appear to be related to the locomotor type (e.g., the sacro‐urostyle region configuration is highly linked with the jumping mode; nonexpanded diapophyses would related to aquatic habitat use). Nevertheless, the functional interpretations are quite particular to this family. Monophyletic clades are also groups with shared locomotory modes or habitat uses. Hence, the hypothesis of common ancestry or adaptation can be evaluated, taking into account the analysis level of the phylogenetic context, so that, when a character is inherited via common ancestry, it necessarily means that functional constraints could also be inherited. Here, we outline the basis for further work on: postmetamorphic development as a fundamental period for the complete differentiation of structures related to a full locomotor functionality; the biomechanical performance in relationship to the variation in ligaments and sesamoids; the importance of analyzing these topics within the frame of heterochrony. J. Morphol. 277:786–813, 2016. © 2016 Wiley Periodicals, Inc.     

Serotonin modulates locomotory behavior and coordinates egg‐laying and movement in Caenorhabditis elegans

Biogenic amines have been implicated in the modulation of neural circuits involved in diverse behaviors in a wide variety of organisms. In the nematode C. elegans, serotonin has been shown to modulate the temporal pattern of egg‐laying behavior. Here we show that serotonergic neurotransmission is also required for modulation of the timing of behavioral events associated with locomotion and for coordinating locomotive behavior with egg‐laying. Using an automated tracking system to record locomotory behavior over long time periods, we determined that both the direction and velocity of movement fluctuate in a stochastic pattern in wild‐type worms. During periods of active egg‐laying, the patterns of reversals and velocity were altered: velocity increased transiently before egg‐laying events, while reversals increased in frequency following egg‐laying events. The temporal coordination between egg‐laying and locomotion was dependent on the serotonergic HSN egg‐laying motorneurons as well as the decision‐making AVF interneurons, which receive synaptic input from the HSNs. Serotonin‐deficient mutants also failed to coordinate egg‐laying and locomotion and exhibited an abnormally low overall reversal frequency. Thus, serotonin appears to function specifically to facilitate increased locomotion during periods of active egg‐laying, and to function generally to modulate decision‐making neurons that promote forward movement. © 2001 John Wiley & Sons, Inc. J Neurobiol 49: 303–313, 2001     

The functional anatomy of the hindlimb of some African Viverridae (Carnivora).

The functional anatomy of the hindlimb of 12 species of viverrids was studied with relation to locomotion. The animals were allocated to primary locomotor categories on the basis of their anatomy and locomotion. The climbing, arboreal walking category (Nandinia binotata) is characterized by a small sacroiliac articulation, the iliopsoas inserts onto a medially located lesser trochanter and the femoral condyles are not posteriorly placed. The hindfoot is plantigrade and its structure permits considerable movement. The pads are soft and the claws retractile. Representatives of the arboreal and terrestrial walking and jumping category (Genetta genetta, G. servalina, G. tigrina) have a plantigrade forefoot and digitigrade hindfoot. The lesser trochanter is more posteriorly placed than in the climbing category. A previously undescribed muscle, the caudofemoralis profundus extends from several anterior caudal vertebrae to the femur. The tibio-astragular joint restricts supination of the foot. There is little mediolateral movement in the digitidgrade foot. The claws are retractile. In the general terrestrial walking and scrambling group (Helogale parvula, Mungos mungo, Atilax paludinosus, Bdeogale crassicauda, Herpestes ichneumon, H. sanguineus) the animals have essentially similar hindlimbs except for size differences and modifications to the feet. Helogale and Mungos have large medial epicondyles on the humerus and large terminal phalanges. Bdeogale has a vestigial first metatarsal, while Atilax can splay its digits. In all species the distal phalanges are non-retractile. The trotting category (Civettictis civetta, Ichneumia albicauda) is characterized by longer epipodials and metapodials and a more proximal position of muscle bellies. Most of the adaptations minimize rotation, adduction and abduction of the leg and supination of the foot. The metatarsals are closely adjoined and the distal phalanx is stout and non-retractile. There appear to be two levels of locomotory adaptation. Major adaptations affect the whole appendicular skeleton and are used to assign animals to primary locomotor categories. Minor adaptations occur mainly in the foot and indicate the more specific habits of the animal.     

Mutually exclusive muscle designs: the power output of the locomotory and sonic muscles of the oyster toadfish (Opsanus tau)

Animals perform a vast array of motor activities. Although it has generally been accepted that muscles are well suited to the function that they must perform, specialization for performing one function may compromise their ability for carrying out another. We examined this principle in the toadfish muscular system: slow-twitch red and fast-twitch white myotomal muscles are used for powering swimming at relatively low frequencies, while the superfast swimbladder muscle powers mating calls by contracting at 100 Hz. We measured muscle power output over a wide range of frequencies. The red and white locomotory muscles could not generate power over ca. 2.2 and 12 Hz, respectively and, hence, could not power sound production. In contrast, the swimbladder muscle has many specializations that permit it to generate power at frequencies in excess of 100 Hz. However, these specializations drastically reduce its power output at low frequencies: the swimbladder muscle generated only one-twentieth of the power of the red muscle and one-seventh of the power of the white muscle at the frequencies used during swimming. To generate the same total power needed for swimming would require unfeasibly large amounts of swimbladder muscle that could not fit into the fish. Hence, the designs of the swimbladder and locomotory muscles are mutually exclusive.     

High PKC α and Low E-Cadherin Expression Contribute to High Migratory Activity of Colon Carcinoma Cells

The protein kinase C (PKC) is a family of serine/threonine kinases that are key regulatory enzymes involved in growth, differentiation, cytoskeletal reorganization, tumor promotion, and migration. We investigated the functional involvement of PKC isotypes and of E-cadherin in the regulation of the locomotion of six human colon-adenocarcinoma cell lines. The different levels of the PKC alpha and the E-cadherin expression have predictable implications in the spontaneous locomotory activity. With the use of PKC alpha--specific inhibitors (safingol, Go6976) as well as the PKC delta--specific inhibitor rottlerin, we showed that only PKC alpha plays a major role in the regulation of tumor cell migration. The results were verified by knocking out the translation of PKC isozymes with the use of an antisense oligonucleotide strategy. After stimulation with phorbol ester we observed a translocation and a colocalization of the activated PKC alpha at the plasma membrane to the surrounding extracellular matrix. Furthermore, we investigated the functional involvement of E-cadherin in the locomotion with the use of a blocking antibody. A high level of PKC alpha expression together with a low E-cadherin expression was strongly related to a high migratory activity of the colon carcinoma cells. This correlation was independent of the differentiation grade of the tumor cell lines.     

Xenopus laevis: an ideal experimental model for studying the developmental dynamics of neural network assembly and sensory-motor computations

The amphibian Xenopus laevis represents a highly amenable model system for exploring the ontogeny of central neural networks, the functional establishment of sensory-motor transformations, and the generation of effective motor commands for complex behaviors. Specifically, the ability to employ a range of semi-intact and isolated preparations for in vitro morphophysiological experimentation has provided new insights into the developmental and integrative processes associated with the generation of locomotory behavior during changing life styles. In vitro electrophysiological studies have begun to explore the functional assembly, disassembly and dynamic plasticity of spinal pattern generating circuits as Xenopus undergoes the developmental switch from larval tail-based swimming to adult limb-based locomotion. Major advances have also been made in understanding the developmental onset of multisensory signal processing for reactive gaze and posture stabilizing reflexes during self-motion. Additionally, recent evidence from semi-intact animal and isolated CNS experiments has provided compelling evidence that in Xenopus tadpoles, predictive feed-forward signaling from the spinal locomotor pattern generator are engaged in minimizing visual disturbances during tail-based swimming. This new concept questions the traditional view of retinal image stabilization that in vertebrates has been exclusively attributed to sensory-motor transformations of body/head motion-detecting signals. Moreover, changes in visuomotor demands associated with the developmental transition in propulsive strategy from tail- to limb-based locomotion during metamorphosis presumably necessitates corresponding adaptive alterations in the intrinsic spinoextraocular coupling mechanism. Consequently, Xenopus provides a unique opportunity to address basic questions on the developmental dynamics of neural network assembly and sensory-motor computations for vertebrate motor behavior in general.     

Involvement of pedal peptide in locomotion in Aplysia: modulation of foot muscle contractions

Pedal peptide (Pep) is a 15-amino-acid neuropeptide that is localized within the Aplysia central nervous system (CNS) predominantly to a broad band of neurons in each pedal ganglion. Pep-neurons were identified by intracellular staining and immunocytology or by radioimmunoassay (RIA) of extracts from identified neurons. RIA reveals that 97% of all Pep-like immunoreactivity (IR-Pep) in pedal nerves is found in the three nerves that innervate the foot. Nearly every Pep-neuron sends an axon out at least one of these three nerves. Application of Pep to foot muscle causes an increase in the amplitude and relaxation rate of contractions driven by nerve stimulation or intracellular stimulation of pedal motor neurons. The increase in relaxation rate was the predominant effect. Intracellular recording in "split-foot" preparations reveals that Pep-neurons increase their overall firing rates and fire in bursts with each step during locomotion. Recovery of IR-Pep from foot perfusate following pedal nerve stimulation increases in a frequency-dependent fashion. Thus it appears that one function of Pep-neurons is to modulate foot muscle contractility during locomotion in Aplysia.