Journal of Human Evolution 59 (2010) 608e619
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Journal of Human Evolution
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Comparative in vivo forefoot kinematics of Homo sapiens and Pan paniscus
Nicole L. Griffin a,*, Kristiaan D’Août b,c, Brian Richmond d,e, Adam Gordon f, Peter Aerts b,g a Department of Evolutionary Anthropology, Duke University, P.O. Box 90383 Science Drive Durham, NC, 27708-0383, USA b Department of Biology, University of Antwerp, Belgium c Centre for Research and Conservation, Royal Zoological Society of Antwerp, Belgium d Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, USA e Human Origins Program, National Museum of Natural History, Smithsonian Institution, USA f Department of Anthropology, University at Albany e SUNY, USA g Department of Movement and Sports Sciences, University of Ghent, Belgium article info abstract
Article history: The human metatarsophalangeal joints play a key role in weight transmission and propulsion during Received 10 September 2009 bipedal gait, but at present, the identification of when a habitual, human-like metatarsi-fulcrimating Accepted 10 July 2010 mechanism first appeared in the fossil record is debated. Part of this debate can be attributed to the absence of certain detailed quantitative data distinguishing human and great ape forefoot form and Keywords: function. Great ape The aim of this study is to quantitatively test previous observations that human metatarsophalangeal Hallux joints exhibit greater amounts of dorsal excursion (i.e., dorsiflexion) than those of Pan at the terminal Human Joint excursion stance phase of terrestrial locomotion. Video recordings were made in order to measure sagittal Metatarsophalangeal joint excursions of the medial metatarsophalangeal joints in habitually shod/unshod adult humans and adult Terrestrial locomotion bonobos (Pan paniscus). Results indicate that the human first and second metatarsophalangeal joints usually dorsiflex more than those of bonobos. When timing of maximum excursion of the first meta- tarsophalangeal joint is coupled with existing plantar pressure data, the unique role of the human forefoot as a key site of leverage and weight transmission is highlighted. These results support hypotheses that significant joint functional differences between great apes and humans during gait underlie taxonomic distinctions in trabecular bone architecture of the forefoot. Ó 2010 Elsevier Ltd. All rights reserved.
Introduction distal articular regions of the MTs that are oriented in a way to allow greater metatarsophalangeal joint excursion in the dorso- Modern human bipedal gait is unique in many ways, including plantar plane, and relatively short pedal phalanges (Morton, 1964; a long stride with an extended hip that contributes to walking Susman, 1983; Rolian et al., 2009). In addition, the modern human efficiency (Alexander, 2004; Sockol et al., 2007; Crompton et al., foot is characterized by a thick plantar aponeurosis, a ligamentous 2008). Part of this unique gait complex involves a forefoot form band that originates from the calcaneus and through a complex and function that differs from the closest living relatives of modern network, attaches to each proximal phalanx (PP) (Hicks, 1954; humans, the great apes (Elftman and Manter, 1935; Morton, 1964; Bojsen-Møller and Lamoreux, 1979; Erdemir et al., 2004). The Bojsen-Møller, 1979; Wunderlich, 1999; Vereecke et al., 2003). plantar aponeurosis maintains the longitudinal arch of the foot Comparisons between great ape and modern human hard and soft during gait (Hicks, 1954; Caravaggi et al., 2009), transmits forces tissue characteristics of the foot clearly highlight the specialization between the hindfoot and the forefoot during the stance phase of the modern human metatarsophalangeal joints for habitual (Erdemir et al., 2004), cushions against the high ground reaction bipedality. forces that occur at the ball of the foot during the latter part of the Bipedal adaptations that distinguish the modern human fore- stance phase (Bojsen-Møller and Lamoreux, 1979), and acts as an foot from that of the great ape forefoot include an adducted 1st energy saving mechanism (Ker et al., 1987). Many researchers have metatarsal (MT) that is substantially larger than the lateral MTs, noted that great apes lack a well-developed plantar aponeurosis compared to modern humans (Morton, 1964; Susman, 1983; Susman et al., 1984; Vereecke et al., 2005). The great apes also * Corresponding author. lack a longitudinal arch (Weidenreich, 1923; Elftman and Manter, E-mail address: nicole.griffi[email protected] (N.L. Griffin). 1935; Morton, 1964; Tuttle, 1970; Vereecke et al., 2003, 2005).
0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.07.017 N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 609
Both hard and soft tissue differences between modern humans toeing-off (i.e., during the last part of stance phase when the toes and the great apes reflect the demands of different positional leave the ground) occurs at the second and third digits of behaviors, and these differences become most recognizable Pan troglodytes (chimpanzees) while Wunderlich (1999) noted that through a comparison of terrestrial gaits of modern humans and it occurs most often between the first and second digits and less great apes (particularly for Pan, for which most nonhuman data are frequently at the first or third digit. Vereecke et al. (2003) docu- available). During human walking, the heel is the first part of the mented that Pan paniscus (bonobos) can toe-off at the second, third foot to contact with the ground. The lateral midfoot touches down, or first digit when the foot is not fully pronated (i.e., the hallux is followed by the lateral MT heads and then medial MT heads; this abducted and the lateral toes are curled medially). In sum, the typical pathway of touchdown is referred to as the medial weight modern human foot contrasts with the foot of Pan by exhibiting transfer. As the heel rises, the imposing weight forces the meta- a more consistent pattern of leverage during gait e one which is tarsophalangeal joints (MTPJ) into dorsiflexion and the plantar characterized by a more stable midfoot, a stereotypical medial aponeurosis is tightened e an event termed the windlass mecha- weight transfer, a large, adducted MT 1, and MTPJs that form nism (Hicks, 1954; Caravaggi et al., 2009). Each phalanx (i.e., the a stable lever at the terminal stage of the stance phase. handle of the windlass) moves onto the dorsum of the respective Though several researchers have observed that the meta- MT head (i.e., the drum of the windlass) and pulls the plantar tarsophalangeal joint dorsiflexion prior to toeing-off in modern aponeurosis along with the plantar pad (i.e., cable). When MTPJ humans is more pronounced than in great apes (e.g., Elftman and dorsiflexion increases, the plantar aponeurosis tightens, the Manter, 1935; Susman, 1983), the hypothesis that there are statis- longitudinal arch becomes more pronounced, and the foot becomes tically significant differences between taxa regarding in vivo fore- a rigid lever (Hicks, 1954; Bojsen-Møller and Lamoreux, 1979; foot kinematics has not been tested. Tuttle (1970) and Tuttle et al. Erdemir et al., 2004; Caravaggi et al., 2009). As noted in studies of (1998) measured African ape passive MTPJ (rays 2-5) hyper-dorsi- MT 1, joint compression occurs at the MTPJ during dorsiflexion flexion and noted that if it were not for the long toe length, these (Hetherington et al., 1989; Muehleman et al., 1999) and when the joints could have a human-like function during gait. Tuttle et al. MTPJs become extensively dorsiflexed, the collateral ligaments (1998) further explain that long toes, like those in the great apes, around the MTPJ tighten to provide stability, a position known as may not be able to support the loading on the forefoot consistently close-packing (Susman and Brain, 1988; Susman and de Ruiter, during the terminal stance phase when the MTPJs are highly dor- 2004). The MTPJs can now serve as a stable fulcrum for pro- siflexed. Furthermore, it has been observed that chimpanzees and pulsion; thus, the human foot can be described as ‘metatarsi-ful- bonobos can walk with flat, extended toes (Elftman and Manter, crimating’ (Meldrum, 1991). As suggested by Bojsen-Møller (1978; 1935; Vereecke et al., 2003), but the amount of MTPJ dorsal Bojsen-Møller and Lamoreux, 1979), because the MT 2 is often the excursion coupled with the weight borne on the forefoot at longest of the MTs, forefoot push-off can occur about two axes: the maximum dorsiflexion has not been quantified. The addition of this transverse axis which includes the MT 1 and MT 2 and the oblique information will more clearly define how a modern human weight- axis which includes the MT 2 through MT 5. Bojsen-Møller (1978) bearing, metatarsi-fulcrimating foot differs from the great ape foot indicated that the transverse axis is most useful during fast, level that lacks this type of forefoot propulsion. walking. In addition, the oblique axis is often recruited during Though there have been previous in vivo studies of human uphill walking, when carrying heavy loads, or at the start of a sprint. forefoot kinematics (Bojsen-Møller and Lamoreux, 1979; Kidder The first or second toe is usually the last to break contact with the et al., 1996; Leardini et al., 1999, 2007; Nawoczenski et al., 1999; ground at the end of stance phase (Vereecke et al., 2003). MacWilliams et al., 2003; Halstead et al., 2005; Caravaggi et al., During terrestrial locomotion, foot kinematics of Pan shows 2009), the specific aim of this study is to compare human and more variation than those of modern humans. The heel and lateral bonobo forefoot kinematics. Bonobo forefoot function is of special midfoot of Pan are usually the first parts of the foot to contact the interest because Pan is the closest living relative of humans and substrate, sometimes simultaneously, and these parts are followed serve as an important comparative outgroup for understanding the by the medial side (Elftman and Manter, 1935; Schmitt and Larson, descendents of the HomoePan common ancestor (McHenry, 1984; 1995; Wunderlich,1999; Vereecke et al., 2003). However, the hallux Richmond and Strait, 2000; Vereecke et al., 2003; but see Lovejoy sometimes strikes the substrate pointed in the medial direction, et al., 2009). With the addition of these data, researchers will be and the lateral toes follow in contact (Wunderlich, 1999; Vereecke in a better position to determine quantitative approaches that are et al., 2003). During midstance, the foot can also present with an suitable for interpreting early hominin forefoot function from fossil adducted or abducted first ray, and lateral rays can be either foot bones (e.g., Latimer et al., 1982; Lovejoy et al., 2009) and plantigrade or curled (Elftman and Manter, 1935; Susman, 1983). footprints (e.g., Leakey and Hay, 1979; Bennett et al., 2009). As the heel rises, the midfoot does not always break contact with Specifically, this study tests the hypothesis that the great ape the ground immediately. This occurrence is called the ‘midtarsal forefoot does not dorsiflex in the same manner prior to toe-off as break’ or ‘midfoot break’ (DeSilva, 2010), and at this moment, the the human forefoot (Elftman and Manter, 1935; Susman, 1983). midfoot serves as a fulcrum (Elftman and Manter, 1935; Susman, Although such a hypothesis has been used as a basis for studies of 1983; Meldrum, 1991; D’Août et al., 2002; Vereecke et al., 2003; fossil hominin foot function (e.g., Latimer and Lovejoy, 1990; DeSilva, 2010)1. As weight is transferred anteriomedially, MTPJs of Duncan et al., 1994; Griffin and Richmond, 2010), in vivo forefoot Pan can extend, but these joints do not experience the close- kinematics during terrestrial gait need to be empirically tested to packing that occurs in the modern human forefoot (Susman et al., determine whether or not the differences between humans and 1984; Susman and de Ruiter, 2004). Susman (1983) observed that great apes are significant. In addition, new kinematic results will be combined with existing plantar pressure measures in order to further highlight what appears to be a unique human metatarsi- 1 Originally, the “midtarsal break” was thought to occur when only the transverse fulcrimating mechanism. It was not possible to collect plantar tarsal joint served as a fulcrum and transmitted weight onto the anterior region of pressure or force plate data in this study, therefore existing the foot (Elftman and Manter, 1935; Nowak et al., 2010), but recent research shows bonobo- and human-averaged pressure data profiles were used. that more dorsiflexion actually occurs at the cuboid-metatarsal joint (D’Août et al., The measurement of MTPJ excursion is only one aspect of forefoot 2002; Vereecke et al., 2003; DeSilva and MacLatchy, 2008; DeSilva, 2009, 2010) than the calcaneocuboid joint during this event. As a result, DeSilva (2010) has function, and therefore, the combination of angular excursion with proposed that the “midtarsal break” be renamed the “midfoot break”. plantar pressure of the forefoot will be valuable to studies aiming to 610 N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 use skeletal morphology (e.g., trabecular bone architecture) to Humans: India predict function in fossil hominids. In order to establish the degree of difference between bonobo This sample consists of habitually shod and habitually unshod and human forefoot mechanics, two predictions were tested. The people native to India. Details regarding the sample and method- first prediction is that human first, second, and third meta- ology can be found in D’Août et al. (2009). All subjects walked tarsophalangeal joints will each show greater amounts of dorsi- barefoot across the viewing area (i.e., lateral to the camera view) flexion prior to toe-off than the corresponding joints of bonobos and were encouraged to walk with a comfortable velocity. For most (whether during terrestrial quadrupedalism or bipedalism). subjects, three trials were collected per foot. Kinematic data were Secondly, because the human forefoot serves as a weight-bearing only measured from the right foot when its view was unobstructed lever at the terminal stance phase, we predict that the greater (i.e., as individuals moved from right to left across the runway). The average MTPJ 1 dorsal excursions are associated with relatively MTPJ angle (defined as the angle formed by the angle of the heel higher average hallux plantar pressures during push-off on the [i.e., the most posterior-plantar point on the heel], the center of the human foot, while smaller average MTPJ 1 excursions will be MT head on the medial side, and the distal end of the hallucal associated with relatively lower average hallux plantar pressures proximal phalanx) was digitized in ImageJ software (http://rsbweb. on the bonobo foot. nih.gov/ij/). This angle was measured at midstance and prior to toe- off at maximum dorsiflexion. The midstance frame was chosen as Sample overview the moment when the swing leg was almost next to the foot in stance, but did not block its view (Fig. 1a). Several frames were The human sample comprises two geographic subdivisions and digitized to identify the video frame in which the maximum angle fl the bonobo sample is represented by one captive group. The first of dorsi exion occurred prior to toe-off (Fig. 1b). The measurement human sample comes from a previous study (D’Août et al., 2009) of MTPJ dorsal excursion is the angle measured at midstance sub- and consists of adult male (n ¼ 26) and female (n ¼ 24) inhabitants tracted by the angle measured at maximum dorsiflexion. NG digi- of Bangalore, India and nearby areas. This sample can also be tized one trial 10 times (each on separate day) to determine divided into habitually unshod (n ¼ 25) and habitually shod precision error and standard deviation (SOM Table 1). (n ¼ 25) groups (Table 1). The second human sample consists of habitually shod adult male (n ¼ 8) and female (n ¼ 8) subjects Humans and bonobos: Animal Park Planckendael residing in Belgium at the time of the study (Table 1). Permission to sample human subjects was approved by the Ethical Committee of Filming of the bonobo sample (n ¼ 6) and part of the Belgian ¼ the University of Antwerp (#A0401) and the George Washington human sample (n 8) took place in the Bonobo Playhall at the University (IRB #100644). Animal Park Planckendael in Muizen, Belgium. Four synchronized The Pan paniscus sample comes from a colony housed at the video cameras (JVC PAL cameras with Sony Digital-8 recorders, Animal Park Planckendael in Muizen, Belgium. Only adults were 50 Hz) were set up in the playhall in order to collect MTPJ angles in 2 fi included as subjects (n ¼ 6) (Table 1). The group lives on a 3000 m 3D (for more details see Grif n, 2009). Trials with a clear view of island surrounded by a moat. The island is full of bushes and the foot in at least two camera views were saved for digitization climbing structures that mimic a natural habitat and include using the program Motus 7.2.10 (Peak Performance Technologies, supports varying in diameter and inclination (Van Elsacker et al., Englewood, Colorado). For each trial, locomotor behavior and foot 1993). Permission to collect bonobo video at the Animal Park posture were recorded (Table 2). MTPJ angle landmark points were Planckendael was approved by both the Royal Zoological Society of similar to those chosen for the Bangalore trials, but slightly Antwerp and the George Washington University (IACUC # 27-11,6). different due to the use of multiple camera views. In other words, due to the different camera positions in the playhall, the distal end of the proximal phalanx and MT head were digitized at the center Methods of the joint, not the medial side. In two cases, the foot posture at midstance was not typical of what would be expected (e.g., the heel We collected three types of video footage. Data capture and was not in contact with the ground at midstance), and in these processing of each type are described below. A description of the cases another frame exhibiting a more neutral position of the foot statistical analyses then follows. was chosen for digitization. Also, it should be noted that in most trials (Table 2), the lateral toes exhibit varying degrees of plantar Table 1 flexion and inversion and are not completely flat or extended on the Sample. ground. For the bonobo subjects, the “midfoot break” was identified Taxon N Age Mass Height during each cycle. (yrs) * (kg) * (m)* Homo sapiens Angle computation (Bangalore, Índia) Habitually Unshod 25 (16F, 9 M) 46.6 ( 13.6) 58.1 ( 14.5) 1.59 ( 0.09) Over the course of this study, three methods of measuring MTPJ Habitually Shod 25 (8F, 17 M) 36.9 ( 13.6) 59.6 ( 7.07) 1.63 ( 0.09) angles for the bonobo trials were explored: (1) raw angles gener- Homo sapiens 16 (8F, 8 M) 30.6 ( 8.9) 66.2 ( 10.0) 1.74 ( 0.11) ated by the Peak Motus program (Griffin et al., 2008; Griffin, 2009), (Belgium) (2) angles projected onto a reference plane using the Peak Motus Pan paniscus Subject Age (yrs) Sex program (Griffin, 2009) and (3) angles generated using code (Belgium) DJ 12 F written for the free R Project for Statistical Computing software HO e29 F (“R,” http://www.r-project.org/). As a result of the problems HE e29 F inherent in the first two measures, the third became the method of KI e29 M ZM 12 M choice (Griffin, 2009). Essentially, the R program was used to take RD 17 M coordinate values of landmarks generated in Peak Motus and F, female; M, male. measure the selected angle projected onto a reference plane * Mean (Standard Deviation). established by the position of the foot. Using the R program, the N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 611
Figure 1. The MTPJ 1 angles of habitually shod and unshod individuals from India were digitized in ImageJ. Dorsal joint excursion was defined as the difference of the MTPJ angle at (A) midstance and (B) prior to toe-off when the MTPJ is maximally dorsiflexed. As illustrated in (B), the MTPJ angle is formed by the most posterior-plantar point on the calcaneus, the central point on the medial side of the first metatarsal head, and the distal end of the hallucal proximal phalanx on the medial side. The last two points were marked in black on each subject prior to filming. Both pictures have been flipped horizontally. reference plane was established by digitized points of two MT MT head visibility in the camera. These vectors were, effectively, heads and the calcaneus (Fig. 2). The line connecting the MT head the axis of rotation of the projected angles because the vertex of landmarks was identified as the normal vector (Fig. 2a), perpen- each angle is always one of the projected MT head landmarks, and dicular to the plane of interest (i.e., sagittal plane). This sagittal thus falls perpendicular to the vector. For one trial, DJ_1, the plane was calculated to pass through the landmark of the calcaneus excursions of MTPJ 1e3 were measured (Fig. 2). For MTPJ 1, the axis (Fig. 2a). MTPJ angles were calculated with this reference plane was defined as the line formed by points representing the MT 1 and (i.e., landmark points were projected onto this sagittal plane) MT 2 heads. For most trials (including all 8 human trials recorded in (Fig. 2b,c,d). For example, in most cases, the MTPJ 2 angle consisted the Playhall), the MT 1 and MT 2 segments were used, but for some of the angle formed by the calcaneus, MT head segment (MT 1 and bonobo trials, other MT head segments were used (SOM Table 2). MT 2 heads) and the head of second proximal phalanx as projected Regarding the angle measurements of the MTPJ 2 and MTPJ 3 as onto the reference plane. Different MT head segments were used to shown in Fig. 2, the MT 2 and MT 5 head segments were selected. In form the normal vector (Fig. 2a), depending on forefoot posture and this case, MT 2 and MT 5 were chosen because this particular
Table 2 Bonobo trial descriptions.
Subject_Trial # Locomotion Midstance Foot Posture DJ_1 knuckle-walking MT 1 is abducted and lateral digits are slightly flexed; overall, forefoot is tending towards plantigrady DJ_2 quadrupedal walk with knuckle-walking hand carrying branches MT 1 is abducted and lateral digits are slightly flexed; overall, forefoot is tending towards plantigrady DJ_3 knuckle-walking MT 1 is abducted and lateral digits are slightly flexed; overall, forefoot is tending towards plantigrady DJ_4 tripedal gallop with baby clinging, and also carrying wood log MT 1 is adducted and plantigrade, lateral digits are flexed DJ_5 knuckle-walking with baby clinging MT 1 is abducted and lateral digits are slightly flexed; overall, forefoot is tending towards plantigrady DJ_6 tripedal walk with baby clinging MT 1 is abducted and lateral digits are slightly flexed; overall, forefoot is tending towards plantigrady DJ_7 knuckle-walking, holding branches in one hand MT 1 is abducted and lateral digits are slightly flexed; overall, forefoot is tending towards plantigrady HE_1 knuckle-walking with baby clinging MT 1 is abducted and plantigrade, lateral digits are flexed HO_1 knuckle-walking MT 1 is abducted and plantigrade, lateral digits are flexed HO_2 knuckle-walking with baby clinging MT 1 is abducted and plantigrade, lateral digits are flexed KI_1 quadrupedal gallop MT 1 is abducted and plantigrade; lateral digits show some flexion KI_2 tripedal gallop, carrying hay in right hand MT 1 is abducted and plantigrade, lateral digits are flexed KI_3 quadrupedal gallop MT 1 is abducted and plantigrade; lateral digits show some flexion RD_1 knuckle-walking MT 1 is abducted and plantigrade; lateral digits show a small degree of flexion RD_2 knuckle-walking MT 1 is abducted and plantigrade; lateral digits show some flexion RD_3 bipedal-walking MT 1 is abducted and plantigrade; lateral digits show small degree of flexion RD_4 knuckle-walking MT 1 is abducted and plantigrade; lateral digits show small degree of flexion RD_5 knuckle-walking MT 1 is slightly abducted and is plantigrade, lateral digits are flexed ZM_1 tripedal walk (carrying branches in one hand) MT 1 is abducted and plantigrade; lateral digits show some flexion ZM_2 tripedal (pushing cardboard box along floor with one hand) MT 1 is abducted and plantigrade, lateral digits are flexed ZM_3 tripedal galloping MT 1 is abducted and plantigrade, lateral digits show some flexion ZM_4 pushing a cardboard box with one hand, no touchdown of MT 1 is abducted and plantigrade, lateral digits show some flexion other hand viewed ZM_5 knuckle-walking MT 1 is abducted and plantigrade; lateral digits show some flexion ZM_6 knuckle-walking MT 1 is abducted and plantigrade; lateral digits show a small degree of flexion ZM_7 sliding a cardboard box across the floor with both hands MT 1 is abducted and plantigrade, lateral digits are flexed 612 N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619
Figure 2. Direction of locomotion and foot posture of bonobo subjects presented a challenge for measuring MTPJ dorsal excursion. Code was written in the program R to provide a reference plane that is based on foot posture and ensures that only excursion along the sagittal plane of the forefoot is measured. (A) The plane onto which an MTPJ angle is projected was formed by two metatarsal head landmarks and the calcaneus landmark. The segment formed by the two metatarsal heads defines the normal vector (MT 1 and MT 2 on the left and MT 2 ad MT 5 on the right). The plane of projection is represented by the line formed by the calcaneus and the MT head segment in (A). For this particular trial (DJ_1), raw angles were generated for the MTP1 using the MT 1 and MT 2 head segment (left) while MTPJ 2 and 3 raw angles were generated using the MT 2 and MT 5 head segment (right) (see text for justification). This means that different planes were established for generating the MTPJ 1 and MTPJ 2 excursion values for trial, DJ_1. (B) The code is written to adjust the forefoot landmarks forming the MTPJ angle to values reflecting a projection along the reference plane (MT 2 and its proximal phalanx are shown only for illustrative purposes when the MT 1 and MT 2 head segments are used to generate MTPJ 2 angles for other trials; see SOM Table 3). (C) As shown here for the first ray, after landmarks are projected onto the plane, the angle is generated. Angles are calculated for all the frames from midstance to toe-off. (D) Here, the MTPJ 1 angle shown represents maximum dorsiflexion prior to toeing-off. N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 613 segment appears to be in line with the locations of the MTPJ 2 and subject when subjects participated in more than one trial. For the MTPJ 3 joints better than the MT 1 and MT 5 segments (see Fig. 2A). VICON video, subjects participated in both walking and jogging The MT 5 head was chosen because it was visible in more than two trials and therefore, walking and jogging trials were averaged cameras and was easier to distinguish the MTPJ 5 joint than the separately. As a result of the small sample size available, bonobo MTPJ 3. NG digitized one bonobo trial (ZM_1, listed in Table 2)10 trials were not averaged per subject. The human and bonobo times (each on a separate day) to determine precision error and excursions were compared using the nonparametric Watson’sU2 standard deviation (SOM Table 3). test for angular data (Zar, 1999). The angle representing maximum dorsiflexion was identified as Finally, the timing of both maximum MTPJ 1 dorsiflexion and the smallest angle in the set. Dorsal excursions were calculated the the “midfoot break” during the stance phase were expressed as same way as the Bangalore trials. Of the 25 digitized bonobo trials, percentages of contact time (i.e., when during stance phase, the six could not be run in the R program to generate the MTPJ 1 “midfoot break” and MTPJ excursion occur). This permitted inclu- excursion because an additional MT head was either not easily sion with Vereecke et al.’s (2003: Fig. 4) averaged plantar pressure distinguished or not visible in two or more camera views. MTPJ 2 profiles. Here, plantar pressure is assumed to be an indication of excursions could be measured for eight trials. In the other cases, the loading. Timings of maximum MTPJ 1 dorsiflexion (i.e., percentages second ray was substantially flexed or not visible in more than of the stance phase) were averaged for the quadrupedal walking one camera view. Only one trial was suitable for digitization of the trials of bonobos and separately for the bipedal walking trials of the MTPJ 3. humans. The occurrence of the “midfoot break” was also averaged Velocity could not be directly calculated for the trials collected at for bonobo quadrupedal walking and bipedal walking trials. For Planckendael because of restrictions to camera views. Contact time each locomotion type, event timings were first averaged by subject was measured for the purpose of determining the timing of before the taxonomic average of either MTPJ 1 maximum dorsi- maximum dorsiflexion during the stance phase. Previous studies flexion or “midfoot break” was calculated. For the human sample, have shown an inverse correlation between contact time and only the Bangalore and Planckendael videos were used because velocity for humans (Vilensky and Gehlsen, 1984) and great apes contact time could be estimated with greater accuracy than VICON (Demes et al., 1994; Vereecke et al., 2004). video. Only one bonobo bipedal trial was available, so its values were used. Timings of either MTPJ 2 or MTPJ 3 maximum dorsi- Humans: Brussels flexion relative to plantar pressure were not considered because the pressure data were not available for each of these individual Human data were also collected using a VICON 612 system rays. (http://www.vicon.com/spots/ESMAC2009.html) at the University of Brussels Biomechanics Lab (for more details see Hagman et al., Results 2008; Griffin, 2009). The sample consisted of 10 subjects, with two of the subjects having also been subjects for the video collected As predicted, human metatarsophalangeal joints dorsiflex more at Planckendael. Subjects were asked to walk and jog at than those of bonobos, and coupled with the plantar pressure, the a comfortable pace (for more details, see Griffin, 2009). Fourteen timing of maximum dorsiflexion of the first metatarsophalangeal millimeter infrared markers were attached to the right side of the joint highlights the key role of the human forefoot in propulsion. body (Fig. 3). One marker was placed on the medial side of the head Summary statistics for human and bonobo samples are reported in of the first MT and another on the lateral side of the head of the fifth Tables 3e5. Although the habitually shod human group has both MT to create a segment. Then, a marker was placed on the dorsal higher mean MTPJ excursion and velocity values than the habitu- aspects of each of the distal ends of first three proximal phalanges. ally unshod group (Table 3), the comparison of the regressions This setup allowed for the measurement of the MTPJ 1, 2, and 3 generated for each group showed neither slope differences angles using the MT 1 and MT 5 segment as the vertex in each case. (p ¼ 0.47) nor y-intercept differences (p ¼ 0.12) (Fig. 4). This result For one subject with exceptionally short digits and overall foot size, justified combining the habitually shod and habitually unshod data two trials were necessary to record kinematics and a slightly for the interspecific comparisons. different marker system was used (see Griffin, 2009). Like the The ranges of the human forefoot excursions are: MTPJ 1, Planckendael trials, MTPJ angles of all the VICON trials were 24 e53 ; MTPJ 2, 25 e47 and MTPJ 3,16 e42 . The bonobo MTPJ 1 generated using the R program and using the calcaneus and the two values range from 10 e38 and the MTPJ 2 values range from MT head coordinates to form the reference plane. Summary 14 e34 . The one bonobo MTPJ 3 dorsal excursion was measured as statistics for each sample’s raw angles (i.e., midstance angle and 25 degrees, and is well within the excursion range for the human angle at greatest MTPJ dorsiflexion) can be found in SOM Table 4. MTPJ 3. Though there is overlap between the taxa regarding ranges of excursions, as expected, human MTPJ 1 and MTPJ 2 excursions Analyses are significantly larger than those of bonobo MTPJ 1 and 2 (p < 0.001 in both cases) (Fig. 5). Statistical summaries for joint excursion values were generated The timing of forefoot kinematics and existing plantar pressure in Statistica 7 (Statsoft, Tulsa, OK). A comparison of MTPJ 1 excur- data also distinguish the two taxa (Fig. 6). For example, the timing sions was first made between the two Bangalore groups in order to of maximum MTPJ 1 dorsiflexion occurs at an average of 87% test whether a lifetime of wearing shoes may have had an effect on ( 2.1%) of contact time for a quadrupedal bonobo, 93% of contact joint range of motion during barefoot walking. Velocity and time for the one bipedal bonobo, and an average of 96% ( 2.5) of excursion ranges were averaged when two or three trials had been contact time for the pooled human trials. Timing of maximum recorded for a subject. To test for a difference in the habitually shod dorsiflexion in the human sample takes place just before peak and habitually unshod groups, values of MTPJ excursion were pressure underneath the first ray, which occurs at 98% of contact regressed against values of velocity. Least squares regression lines time. For the quadrupedal bonobo, peak pressure under the first ray were generated for each group and compared using an ANCOVA. occurs at 84% of contact time, which is also around the time of Before interspecific differences in metatarsophalangeal joint maximum MTPJ 1 dorsiflexion. In contrast to the human trials, both excursion were explored, first metatarsophalangeal joint excursion quadrupedal (Fig. 6A) and bipedal trials (Fig. 6B) indicate that values and contact time values were each averaged per human maximum dorsiflexion is not associated with a substantial increase 614 N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619
Figure 3. Ten human subjects were recruited at the University of Brussels Biomechanics Lab in order to measure MTPJ kinematics during walking and jogging. (A) Fourteen millimeter infrared markers were attached to the right side of the body on the greater trochanter, the lateral and medial femoral condyles, the lateral and medial malleoli, the calcaneal tuberosity, the navicular tuberosity, the heads of the first and fifth metatarsals and the heads of the first, second and third proximal phalanges. (B) Close-up of the foot markers (marker for calcaneus is not in view).
Table 3 MTPJ 1 summary statistics.
Sample N Dorsal Excursion Velocity (m/s) Contact time (s)
Mean & SD Range Mean & SD Mean & SD Range Homo sapiens Habitually Unshod (India) 25 37 6.2 24e51 0.96 0.25 0.87 0.17 0.61e1.3 Habitually Shod India 25 41 5.8 34e53 1.1 0.23 0.77 0.13 0.61e1.3 Planckendael 8 40 6.2 29e47 n/a 0.73 0.059 0.62e0.78 VICON Walking 10 43 4.9 35e48 n/a 0.70 0.095 0.63e0.93 Jogging 10 36 4.8 30e43 n/a 0.29 0.051 0.21e0.38
Pan paniscus Quadrupedalism 5 19 5.5 10e24 n/a 0.86 0.064 0.77e0.94 Tripedalism 1 13 n/a n/a 0.89 n/a Quadrupedal/Tripedal Gallop 3 26 10 18e38 n/a 0.34 0.020 0.32e0.36 Bipedalism 1 18 n/a n/a 0.88 n/a
SD ¼ Standard Deviation. n/a ¼ not available. Two human individuals participated as subjects in both the Animal Park Planckendael and VICON setups. For the statistical analysis, the excursions of the walking trials from each setup were averaged together. They are not averaged together in the table above. N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 615
Table 4 MTPJ 2 Summary Statistics.
Sample N Dorsal Excursion Contact time(s)
Mean & SD Range Mean & SD Range Homo sapiens Planckendael 8 39 6.4 30e47 0.73 0.059 0.62e0.78 VICON Walking 10 34 4.3 25e38 0.66 0.14 0.41e0.93 Jogging 10 33 4.2 25e41 0.29 0.050 0.21e0.38
Pan paniscus Quadrupedalism 3 24 10 14e34 0.77 0.095 0.66e0.83 Tripedalism 1 19 n/a 0.97 0.21 0.82e1.1 Quadrupedal Gallop 1 22 n/a 0.28 n/a
SD ¼ Standard Deviation. n/a ¼ not available. Two human individuals participated as subjects in both the Animal Park Planck- endael and VICON setups. For the statistical analysis, the excursions of the walking trials from each setup were averaged together. They are not averaged together in the table above. Figure 4. A comparison of the slope generated by the habitually unshod Indian group (stippled line, y ¼ 32.7 þ 4.6x) and the slope of the habitually shod Indian group (solid in pressure under the first ray (relative to the lateral rays) leading to line, y ¼ 30.1 þ 9.7x) indicates that relative to velocity, the two groups do not differ in a spike as shown in the human trial profile. Therefore, the spike of MTPJ 1 dorsal excursion prior to toe-off. Habitually unshod human values are repre- fi sented by open circles; habitually shod human values are represented by black pressure distinguishes the human rst ray from the rest of the foot diamonds. and clearly shows its primary role in weight-bearing just prior to toeing-off (Fig. 6C). MTPJ 1 maximum dorsiflexion in the bipedal bonobo occurs when pressure in the first ray is already declining hominins. This obstacle is further compounded by the lack of data and the pressure increases in the lateral rays and lateral midfoot. on forefoot function and structure in living great apes and humans. While the quadrupedal bonobo profile shows a human-like pattern In light of these problems, the main goal of this study was to test with maximum dorsiflexion taking place when the first digit bears whether or not human MTPJs show greater dorsal excursions prior more pressure than any other region of the foot, there is not to toe-off than the MTPJs of bonobos during terrestrial gait. Keeping a substantial difference between the pressure of the first ray and such limitations as the small and variable (in terms of gait type and the lateral rays present in the human profile. foot posture; see Table 2) bonobo sample in mind, the observations The “midfoot break” was observed at around 64% ( 11.7%) of for the MTPJ 1 and 2 support the conclusion that, during gait, dorsal contact time for the quadrupedal bonobo trials and 70% of contact excursion of human forefoot generally exceeds that of the bonobo time for the bipedal bonobo (Fig. 6A,B). At the “midfoot break” during the stance phase, pressure is present under the lateral C tno ca t iT me v .s M TPJ 1 D o sr al xE c noisru midfoot, and as more clearly shown in the quadrupedal bonobo 60 profile, this corresponds with the role of the midfoot as a weight- bearing site during stance phase of Pan. Neither human subjects in 50 the current study sample nor those in Vereecke et al.’s (2003) study exhibited a “midfoot break.” In the latter study the lack of a “mid- 40 foot break” was reflected in the minimal amount of weight support 4_JD ZM 5_ by the lateral midfoot during stance phase. lasroD 30 Ex noisruc IK 1_ 1_JD 6_MZ Discussion (d )seerge 3_MZ HO_1 2_JD 20 IK 2_ 4_MZ H 1_E DR _ D3 3_J Habitual bipedalism is a key hominin adaptation. Traditionally, 7_MZ Z 1_M the external morphology of the lower limb has been at the center of 10 KI 3_ 2_MZ _DR 2 debates over whether or not early hominin gait was modern RD 1_ human-like and whether or not climbing was an important part of 0 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 locomotor behavior. However, relying on morphological differences alone has proven to be inconclusive so far, especially regarding the tcatnoC emiT )s( functional implications of forefoot morphology among early muH na s naB( ag lo er , I n )aid :
Table 5 snamuH ,leadnekcnalP( :)muigleB MTPJ 3 summary statistics. aH b ti ua ll y S hod muH na s ( rB ssu e ,sl eB l :)muig +
Sample N Dorsal Excursion Contact time (s) ,leadnekcnalP(sobonoB :)muigleB
Mean & SD Range Mean & SD Range Figure 5. The human sample is composed of the Indian habitually unshod and shod Homo sapiens (VICON) sample (open circles), the Planckendael human sample (closed squares), the Brussels Walking 10 31 7.5 16e42 0.70 0.095 0.63e0.93 sample (crosses), and the average values of the individuals that participated in both the Jogging 10 30 6.2 17e39 0.29 0.051 0.21e0.38 Planckendael and Brussels walking trials (closed circles). Each bonobo value is repre- sented by a closed triangle followed by a code indicating the individual (see Tables 1 Pan paniscus and 2), trial number (see Table 2). Note the values from the Brussels sample form Quadrupedalism 1 25 n/a 0.80 n/a two distinct clusters because walking and jogging trials of each subject are repre- SD ¼ Standard Deviation. sented. It should also be noted that some bonobos achieve values of excursion n/a ¼ not available. comparable to those of humans. 616 N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619
Figure 6. The timing of maximum MTPJ 1 dorsiflexion (solid arrow) during the stance phase of the (A) averaged quadrupedal bonobo trials, (B) bipedal bonobo trial, and (C) averaged walking human trials were matched with the corresponding averaged plantar pressure profiles (of the hallux [first metatarsal and first digit]), courtesy of Vereecke et al. (2003). Maximum dorsiflexion (solid arrows) occurs at 87% ( 2.1%) of stance phase for the averaged quadrupedal bonobo, 93% for the one bipedal bonobo, and 96% ( 2.5) contact time for the averaged human walking trials. Note that maximum MTPJ 1 dorsiflexion in humans occurs just before the first ray experiences peak pressure (at 98% contact time). The average occurrence of the ‘midfoot break’ (broken arrow) is 64% ( 11.7%) of contact time for the quadrupedal bonobos and 70% of contact time for the one bipedal bonobo. On a separate note, the plantar pressure profile of the bipedal bonobo indicates that plantar pressure of the heel is present throughout the stance phase. As indicated in the plantar pressure profile, weight is not only transferred to the anterior part of the foot, but plantar pressure in the hindfoot region also shows a slight increase as well. This suggests that this averaged plantar pressure profile includes individual bonobos who did not exhibit a ‘midfoot break’. When a midtarsal break occurs, pressure under the heel region should be absent. Between 64% and 70% contact time, the human lateral midfoot exhibits minimal plantar pressure. H, heel; V1, medial midfoot; V2, lateral midfoot; M, metatarsal heads 2e5; T, lateral toes 2e5; Hallux, first metatarsal head and first digit. N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 617 forefoot. Additional bonobo trials need to be collected before habitually different locomotor behaviors (Fajardo and Müller, 2001; taxonomic differences in MTPJ 3 excursions can be tested. MacLatchy and Müller, 2002; Ryan and Ketcham, 2002a,b, 2005). The results support previous observations that the forefoot of The kinematic data presented in this study support results from the Pan does not dorsiflex in the same manner as the human forefoot analysis of trabecular architecture in the extant hominid MTPJ 1 and (Elftman and Manter, 1935; Susman, 1983). The results also show 2(Griffin et al., 2010). Quantification of the trabecular bone of either some previously unrecognized levels of overlap between the taxa in the MT 1 or MT 2 head shows that humans can be distinguished ranges of excursion for both MTPJ 1 and 2, and in future studies, this from the great apes based on a more organized trabecular strutting overlap may become accentuated with the addition of more bonobo pattern, especially in the dorsal region. The more stereotypical subjects and trials. Also, the excursion of the one bonobo MTPJ 3 falls pattern of strutting and reinforcement of bone in the dorsal area of within the observed human range. These areas of overlap may be the human joint correspond with its role as a primary lever prior influenced by some methodological limitations. For example, it is to toe-off. The less organized pattern of the great ape trabeculae possible that the greater joint mobility in the bonobo midfoot emphasizes that the MTPJs need to accommodate stresses in (i.e., dorsiflexion as the heel rises during the stance phase) may have several directions as a result arboreal foot use for grasping and in contributed to a larger value of MTPJ dorsal excursion than would be variable postures during terrestrial gait (Table 2). Combining the measured if the base of the MT was used as a marker instead. current experimental results with morphological observations Because markers could not be placed on the bonobo subjects, the suggests that trabecular bone structure in hominin forefoot fossils calcaneus was chosen as a proxy for the MT base in all of the may provide a means of testing hypotheses about the origin and subjects. The calcaneus has been used in other studies to reconstruct evolution of the human metatarsi-fulcrimating mechanism. MTPJ excursion (e.g., Nawoczenski et al., 1999), but may introduce Together, the results of the kinematic study and more recent errors in comparisons between taxa with very different foot struc- studies such as the measurement of dorsal canting in proximal tures. Another limitation is the use of the MT head segment as the phalanges (Griffin and Richmond, 2010) show that human MTPJs vertex, which further prevents the direct measurement of MTPJ usually exhibit more excursion, which is reflected in the previous motion, especially in the case of the bonobos when the hallux is and current findings that human proximal phalanges have more divergent from the second ray. Ideally, both taxonomic samples dorsally canted basal joints than those of Pan. However, it is would be measured with a VICON system and markers would important to note that there is overlap in ranges of the two taxa be placed at the locations defining the metatarsophalangeal joint regarding results in both kinematic and morphological analyses. (i.e., head of the proximal phalanx, MT head, and MT base). These results affirm Tuttle’s (1970) and Tuttle et al.’s (1998) finding Though it is important to acknowledge the overlap in MTPJ that passive dorsiflexion of the African ape MTPJs is comparable to excursion values between the two taxa, this study supports and that of humans. As noted in the current and previous studies, this adds to previous research. Coupling the present study’s kinematic MTPJ dorsiflexion is not habitual because bonobo and chimpanzee data with Vereecke et al.’s (2003) pressure data clearly distin- subjects often walk with curled toes (i.e., flexed phalanges) and this guishes human forefoot function from that of the bonobo. Not only posture is most likely used to avoid high bending stresses associ- is human maximum dorsiflexion on average greater than that of ated resulting from having long toes (Tuttle, 1970; Preuschoft, the bonobo, the pressure at this occurrence is relatively greater 1970). Both the overlap in dorsal canting, as well as the in vivo (i.e., hallux vs. lateral forefoot pressure) than under the bonobo first and in vitro kinematic data, suggest that humans are not unique in ray during bipedal or quadrupedal walking (Fig. 6). Thus, the medial the ability to dorsiflex their MTPJs quite substantially. Also, side of the human forefoot contrasts with the bonobo medial according to Rein and Harrison (2007), some species of Papio are forefoot by showing a larger contribution to propulsion during gait. indistinguishable from humans in the degree of dorsal canting. When the occurrence of the “midfoot break” in the current Thus, simply observing or quantifying dorsal canting of a single study’s trials is included with Vereecke et al.’s (2003) pressure data, phalanx should not be used as the only diagnostic character of the role of the lateral midfoot during weight-bearing in bonobos is human-like forefoot function. However, it can be used in combi- highlighted (Fig. 6)(Elftman and Manter, 1935). However, the nation with other traits, specifically those that will provide clues to fulcrum action of the lateral midfoot is not as clear. For example, whether or not the forefoot was being used as a primary weight- regarding the single bipedal bonobo trial, the occurrence of the bearing lever. This includes a specific pattern of trabecular bone “midfoot break” does not match the plantar pressure profile orientation in the dorsal region of the MT head (Griffin et al., 2010). reported by Vereecke et al. (2003). In the average plantar pressure profile, the pressure under the heel is present through most of Conclusions the stance phase, indicating that in this profile that at least some of fi the subjects did not exhibit a “midfoot break.” Also, when the This study is the rst to provide quantitative measurements of occurrence of the “midfoot break” is matched on the quadrupedal both human and bonobo forefoot kinematics during locomotion. plantar pressure profile, it shows that plantar pressure in the lateral The results support previous qualitative observations that great ape fl midfoot is decreasing as weight is being transferred to the anterior MTPJs do not usually dorsi ex in the same manner as humans prior “ ” regions of the foot. This is not comparable to the human pattern in to toe-off. In addition, relating the occurrence of a midfoot break fi the forefoot, in which maximum MTPJ 1 dorsiflexion occurs when to the pressure pro le of the lateral midfoot of Pan emphasizes the pressure underneath the first ray is increasing. use of this region for weight transmission. However, the foot of Pan An overarching goal of this study is to increase our current does not exhibit a notable push-off mechanism like the human knowledge about forefoot functional differences in extant hominids foot; the end of stance phase in Pan might be better described as “ ” “ ” for the purpose of making inferences about early hominin postural lift-off than push-off. The results here show that the role of the and locomotor behavior. Several in vivo studies have shown that human forefoot as a key site of leverage and weight transmission is trabecular struts and plates can respond to the direction and unique compared to our closest living relatives. magnitude of local loading by aligning themselves in the direction of stress and increasing in density (Lanyon,1974; Goldstein et al.,1991; Acknowledgments Pontzer et al., 2006; van der Meulen et al., 2006). In addition, high- resolution X-ray computed tomography has shown significant We wish to thank the Royal Zoological Society of Antwerp and differences in trabecular bone properties between primates that use the Animal Park Planckendael staff for permitting KD and NG to 618 N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 608e619 videotape the bonobos. We are grateful for the zookeepers’ coop- Fajardo, R.J., Müller, R., 2001. Three-dimensional analysis of nonhuman primate eration and patience, and thankful to all of our subjects. Special trabecular architecture using micro-computed tomography. Am. J. Phys. Anthropol. 115, 327e336. thanks is given to Jan Scholliers for constructing the calibration Goldstein, S.A., Matthews, L.S., Kuhn, J.L., Hollister, S.J., 1991. Trabecular bone cube, Dave Frans for deinterlacing the Bangalore video, and Dr. Bart remodeling: an experimental model. J. Biomech. 24 (Suppl. 1), 135e150. fi Van Gheluwe for allowing KD and NG to use the VICON system in Grif n, N.L., 2009. Comparative Forefoot Kinematics and Bone Architecture in Extant Hominids. Ph.D dissertation, George Washington University. his Biomechanics Lab. NG is grateful to Adrienne and Jan Van Den Griffin, N.L., D’Août, K., Aerts, P., Richmond, B.G., 2008. Comparative in vivo forefoot Baere for their exceptional hospitality during her stay in Muizen, kinematics in extant hominids. Am. J. Phys. Anthropol. 46, 108. Gabriel Mallozzi for his assistance with Peak Motus, Can Kirmizi- Griffin, N.L., D’Aout, K., Ryan, T.M., Richmond, B.G., Ketcham, R.A., Postnov, A., 2010. Comparative forefoot trabecular bone architecture in extant hominids. bayrak and Erin Marie Williams for their help with the VICON J. Hum. Evol. program, J. Tyler Faith for his statistical help and Pascal W. Prinz for Griffin, N.L., Richmond, B.G., 2010. Joint orientation and function in great ape and modeling his own hindlimb. We greatly appreciate Dr. Evie Ver- human proximal pedal phalanges. Am. J. Phys. Anthropol. 141, 116e123. Hagman, F., van de Ven, F., Van Gheluwe, B., van Eijndhoven, S., 2008. Setting up eecke for making the bonobo and human plantar pressure data gait analysis measurement devices for simultaneously measuring force, pres- available. We are grateful to Daniel Schmitt, Masato Nakatsukasa, sure, and motion. In: D’Août, K., Lescrenier, B., Van Gheluwe, B., De Clercq, D. Bernard Wood, and Tim Ryan for their comments on drafts of this (Eds.), Advances in Plantar Pressure Measurements in Clinical and Scientific e manuscript. We are grateful to Steven Leigh, and the anonymous Research. Shaker Publishing BV, pp. 26 43. Halstead, J., Turner, D.E., Redmond, A.C., 2005. The relationship between hallux Associate Editor and reviewers for their editorial suggestions. dorsiflexion and ankle joint complex frontal plane kinematics: a preliminary This study has been supported by the L.S.B. Leakey Foundation, study. Clin. Biomech. 20, 526e531 (Bristol, Avon). fi NSF BCS-0726124, Sigma Xi Grant-in-Aid of Research, Lewis Cotlow Hetherington, V.J., Carnett, J., Patterson, B.A., 1989. Motion of the rst meta- tarsophalangeal joint. J. Foot Surg. 28, 13e19. Research Fund, and through PA and KD, the FWO-Flanders Grant Hicks, J.H., 1954. The mechanics of the foot. II. The plantar aponeurosis and the arch. G.0125.05, and BOF-UA. NG would also like to acknowledge J. 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