The Role of the Gluteus Maximus on Trunk Stability in Human Endurance Running

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2 The Role of the Gluteus Maximus on Trunk Stability in Human Endurance Running A thesis submitted to the Graduate School of the University of Cincinnati in partial fulfillment of the requirements for the degree of Master of Arts in the Department of Anthropology of the College of Arts and Sciences by Lauren Heitkamp B.S. University of Cincinnati, 2012 Committee Chair: Heather L. Norton, Ph.D. Committee Members: Katherine K. Whitcome, Ph.D. Brooke E. Crowley, Ph.D.

3 Abstract The human gluteus maximus is uniquely robust among primates (Stern, 1972; Lieberman et al., 2006). The large muscle s evolutionary role has long been debated and most recently explained in the Endurance Running (ER) Hypothesis as an adaptation for trunk balance in ER among early Homo (Bramble and Lieberman, 2004; Lieberman et al., 2006). Few studies have addressed trunk biomechanics in relation to barefoot running, the most likely foot condition of the hominin evolutionary past (Lieberman et al., 2010). Thus, this thesis further tests the ER Hypothesis by investigating the foot condition effect, barefoot and shod, on trunk kinematics and gluteus activity relative to trunk pitch. Kinematic and electromyographic data were collected from twenty-four adults: twelve males and twelve females. Subjects walked and ran on a treadmill at four speeds and three speeds, respectively, while shod and while barefoot. Sagittal plane trunk, thigh, and foot kinematics were calculated at heel strike and following. Gluteus maximus electromyographic data were calculated by average amplitude around foot contact. Joint angles of the trunk, thigh, and foot significantly differed between gaits within a single speed, between foot conditions within a single speed, and across speeds within a single gait. In contrast, muscle amplitude significantly differed across speeds within a single gait but not between gaits or between foot conditions at a single speed. Trunk forward pitch rate at foot strike increased with running speed, as did gluteus maximus activity. Although differences in magnitude of gluteus maximus contraction did not differ between shod and barefoot running, increased gait speed indepent of foot condition was associated with increased pitching of the trunk and greater gluteus maximus magnitude. i

4 Copyright 2016 by Lauren Heitkamp All Rights Reserved ii

5 Acknowledgements This thesis would not have been possible without the support of many other individuals. Firstly, I wish to thank my advisor Dr. Katherine Whitcome for your guidance and constant support through this process. I appreciate the long hours, constant rigor, and valuable feedback you offered while still providing an inspirational and energetic atmosphere. A special thanks to your adaptability and perseverance in sping a portion of this collaboration from a distance but still always being available for my calls and s. I wish to thank my thesis committee members; Dr. Heather Norton for your patience, unyielding encouragement and advice through this process and other related eavors; and Dr. Brooke Crowley for your flexibility, support, and insightful feedback. Thanks to Dr. Bruce Jayne for the support and willingness to l EMG equipment for this project. I cannot thank my subjects enough for their donated time and willingness to contribute to this research. I owe a great deal to everyone who helped teach me the invaluable skill of coding and spent their time helping me troubleshoot, especially Nicole Wallenhorst. Without your expertise and willingness to be a resource of mine I never would have been able to complete this project; my sincerest thanks. To all my fellow Anthropology Graduate Students, especially Dayna Reale and Kristen Tomko, for our coffee shop sessions, lively discussions, and your constant counsel, thank you for saving my sanity. To my fris and family for dealing with my continual existential crises, thesis babble, and requests for practice labs subjects, I appreciate everything. Thanks to my parents and sisters for being a constant and sometimes annoying source of motivation; I am eternally grateful for all you did. Funding was provided by the Charles Phelps Taft Research Center s Graduate Enrichment Award at the University of Cincinnati. iii

6 Table of Contents 1. Introduction Overview Research Goals Background Evolution of Human Endurance Running Walking and Running Foot Kinematics in Shod and Barefoot Running Shod versus Barefoot Kinetics in Running Shod versus Barefoot Trunk Kinematics in Running Gluteus Maximus Anatomy and Function Evolution of the Human Gluteus Maximus Summary Hypotheses Trunk Kinematics Differ in Shod versus Barefoot Running GMAX Force Production Differs in Walking versus Running at 2.0 ms GMAX Force Production Differs in Shod versus Barefoot Running Methods Subjects Equipment Kinematic Data Collection EMG Data Collection EMG Electrode Placement Validation: Human Cadaver Dissection...23 iv

7 4.5. Gait Speeds Kinematic Processing EMG Processing Analyses Results Foot Kinematics in Barefoot and Shod Conditions Kinematics in Shod and Barefoot Gaits Trunk Kinematics Differ in Shod versus Barefoot Conditions Thigh Kinematics in Shod and Barefoot Conditions GMAX Force Production Differs in Walking and Running at 2.0 ms GMAX Force Production Differs in Shod versus Barefoot Running Discussion Foot Strike Patterns Kinematics in Shod versus Barefoot Gaits Trunk Kinematics Differ in Shod versus Barefoot Conditions Thigh Kinematics in Shod and Barefoot Conditions GMAX Force Production Differs in Walking and Running at 2.0 ms GMAX Force Production Differs in Shod versus Barefoot Running Gait Patterns Implications for Homo Evolution Limitations and Future Research Summary and Conclusions.56 Glossary of Commonly Used Abbreviations.57 v

8 References Cited.58 Appix A...64 Appix B...66 Appix C...92 vi

9 List of Tables Table 4.1. Subject demographics...20 Table 4.2. List of variables 28 Table 5.1. Variable means and standard deviations...32 Table 5.2. Signed Rank Test between foot conditions...33 Table 5.3. Signed Rank Test between gaits at 2.0 ms Table 5.4. Friedman s speed test 37 Table 5.5. Friedman s walking speeds test 38 Table 5.6. Friedman s running speeds test.38 Table 5.7. Kall s tau_b correlations for 4.0 ms vii

10 List of Figures Figure 2.1. Ground reaction force duty factor differences...5 Figure 2.2. Ground reaction force speed differences...6 Figure 2.3. Walk versus run trunk depiction....8 Figure 2.4. Foot strike ground reaction force differences.. 10 Figure 2.5. Foot condition ground reaction force differences...10 Figure 2.6. Gluteus maximus differences human versus chimpanzee...12 Figure 2.7. Foot switches...16 Figure 4.1. Electrode placement and setup 22 Figure 4.2. Gluteus maximus dissection fascicle orientation 24 Figure 4.3. Gluteus maximus dissection craniocaudal length 24 Figure 4.4. Gluteus maximus dissection medial length. 25 Figure 4.5. Gluteus maximus dissection lateral depth Figure 4.6. Gluteus maximus dissection medial depth.. 26 Figure 4.7. Angle calculations...27 Figure 4.8. Foot strike identification..29 Figure 5.1. Foot angle at foot contact Figure 5.2. Trunk angle at foot contact..34 Figure 5.3. Overall trunk angular excursion..34 Figure 5.4. Trunk angular velocity at foot contact.35 Figure 5.5. Maximum stride trunk angular velocity..35 viii

11 Figure 5.6. Thigh angle at foot contact..36 Figure 5.7. Thigh angular excursion from foot contact to maximum 36 Figure 5.8. Thigh angular velocity excursion from foot contact to maximum..36 Figure 5.9. Superior gluteus maximus around foot contact...39 Figure Inferior gluteus maximus around foot contact Figure 6 a-h. Gait patterns for select variables at select speeds ix

12 1. Introduction 1.1 Overview Research addressing the evolutionary origin and function of the large human gluteus maximus (GMAX), the superficial muscle of the dorsal pelvis, is periodically revisited in the scientific literature (Karlsson and Jonsson, 1964; Fischer and Houtz, 1968; Lovejoy, 1988; Marzke et al., 1988; Lieberman et al., 2006). The Endurance Running (ER) Hypothesis proposes that the uniquely robust human GMAX plays a central role in stabilizing the upper body at ER speeds (Bramble and Lieberman, 2004; Lieberman et al., 2006). This ER Hypothesis, published nearly a decade ago, argues that early Homo evolved musculoskeletal adaptations for long distance running, including the robust GMAX. Because muscle tissue (i.e., GMAX) rarely preserves in the fossil record (Shaw, 2010), research testing the kinematic predictions of the ER Hypothesis is conducted on living human subjects. Furthermore, because fossil evidence supporting the ER Hypothesis is associated with the appearance of the genus Homo some two million years ago and footwear appears in the archaeological record no earlier than 40,000 years ago (Trinkaus and Shang, 2008), ER research has increasingly focused on barefoot biomechanics (eg., Lieberman et al., 2006; Squadrone and Gallozzi et al., 2009; Lieberman et al., 2010; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013; Shih et al., 2013). Although the kinematics and kinetics of the lower limb are now well described for both shod and barefoot running (eg., Lieberman et al., 2010; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013; Shih et al., 2013), less is known about trunk biomechanics in ER, most notably in barefoot running. Trunk kinematics are needed, for both shod and barefoot running, in order to test elements of the ER Hypothesis, particularly 1

13 to determine the role of GMAX in upper body stability because rapid trunk pitch is likely to occur at high speeds. 1.2 Research Goals The goal of this thesis is to determine if barefoot running and shod running at ER speeds produce significantly different trunk kinematics, and if so, whether the differences relate to patterns of force production in the GMAX. Magnitude of contraction as a relative measure of force production in a muscle can be quantified by an electromyogram (EMG), a recording of muscle electrical output that is representative of muscle force production (Moore et al., 2011). In particular, this thesis study aims to expand on previous work investigating the stabilizing role of the GMAX in counteracting trunk pitch, which is known to be rapid following foot contact (FC) in human running (Thorstensson et al., 1984; Lieberman et al., 2006). By exploring these phenomena not only in shod but also barefoot running, this thesis contributes to a growing literature that broadly explores the anatomical origin and functional role of ER in human evolution. 2

14 2. Background 2.1 Evolution of Human Endurance Running The evolutionary record, although not fully reconstructed, reveals two key shifts in hominin locomotor strategy (Lovejoy, 1988; Bramble and Lieberman, 2004; Harcourt-Smith and Aiello, 2004; Lieberman et al., 2006; Thorpe, 2009). The first occurred around six to seven million years ago (Harcourt-Smith, 2010) when hominins became habitual walking bipeds (Lovejoy, 1988; Schmitt, 2003; Harcourt-Smith and Aiello, 2004; Thorpe, 2009). Although the selection pressures underlying this transition are debated (Hunt, 1994; Schmitt, 2003; Foley, 2002; Watson et al., 2008; Thorpe, 2009; Pontzer et al., 2009), musculoskeletal adaptations of bipedalism are clearly evident from comparative study of fossils and living taxa (McHenry, 1986; Lovejoy, 1988; Schmitt, 2003). They include a valgus knee, an adducted hallux, and a broad and laterally flared illium that repositions the lesser gluteals (gluteus medius and gluteus minimus) as hip abductors (McHenry, 1986; Lovejoy, 1988; Aiello and Dean, 2002). The second locomotor transition occurred approximately two million years ago as members of the genus Homo are thought to have started active persistence hunting across expanding arid landscapes (Bramble and Lieberman, 2004, Lieberman et al., 2006). The pursuit of game made possible with long distance ER strategies allowed hominins to run prey to exhaustion (Bramble and Lieberman, 2004, Lieberman et al., 2006). Anatomical features that are biomechanically linked to long distance running include spring-like arches within the foot, short toes, long leg tons, a narrow thorax decoupled from a narrow pelvis, and an expanded attachment of an enlarged GMAX (Bramble and Lieberman, 2004). The presence of these traits in modern humans and early Homo along with persistence hunting practices among modern hunter gatherers (Bramble and Lieberman, 2004; Liebenberg, 2006; Liebenberg, 2008) provide 3

15 evidence that the robust human GMAX arose in association with long distance running. Furthermore, because the preferred speed for human urance running spans a wide range (2.2 meters per second, or ms -1, to 5.5 ms -1 ) and carries little or no additional energy cost as speed increases (Carrier, 1984), it may be argued that adaptations evolved to enhance locomotor efficiency at these ER speeds. Notably, a bipedal runner must stabilize an upright and freely mobile trunk against rapid angular displacement of the center of mass (COM) at foot contact (Biewener, 2003; Hamill and Knutzen, 2009). An anatomical mechanism to mitigate rapid trunk pitch and limit COM displacements would conserve locomotor energy and could be met by the large human GMAX (Bramble and Lieberman 2004, Lieberman et al., 2006). 2.2 Walking and Running A moving body exerts forces of varying direction and magnitude on the ground (Biewener, 2003; Hamill and Knutzen, 2009). In response, the ground applies equal and opposite reaction forces, called ground reaction forces (GRFs) on the body (Biewener, 2003; Hamill and Knutzen, 2009; Perry and Burnfield, 2010). The magnitude of a GRF is affected by the body s size and speed, the number of contacting limbs, the displacements of total body COM, and gait type (Figure 2.1; Figure 2.2; Biewener, 2003; Perry and Burnfield, 2010). Magnitude of GRFs are greater as speed and size increase and as duty factor decreases (Figure 2.1; 2.2; Hamill and Knutzen, 2009; Perry and Burnfield, 2010). Duty factor is a temporal stride component measured as the percentage of stride time that a limb is in contact with the ground (Biewener, 2003). Ground reaction forces, along with limb postures, segment weights, and inertial properties, influence external joint moments (Biewener, 2003; Perry and Burnfield, 2010). External moments are mitigated by internal moments produced by muscle force; greater external moments require greater opposing internal moments (Biewener, 2003; Hamill and Knutzen, 2009). 4

16 Although walking speeds carry relatively high duty factors and small displacements of the COM, running speeds produce lower duty factors with larger COM displacements and higher angular velocities (Hamill and Knutzen, 2009). Velocities are changes in angular positions over a period of time (Biewener, 2003). These pitching motions can be either forward (anterior pitch) or backward (posterior pitch) (Lieberman et al., 2006). In association with these differences, GRFs are often 1 to 1.2 times that of body weight at typical walking speeds (Hamill and Knutzen, 2009) and 2 to 5 times body weight at higher speeds (Biewener, 2003; Hamill and Knutzen, 2009). As the high-magnitude GRF in running increases joint torque, large body segments such as the trunk may experience destabilizing velocities and accelerations, particularly when obliquely oriented relative to the GRF vector (Biewener, 2003; Hamill and Knutzen, 2009; Perry and Burnfield, 2010). GRFv % of Limb Contact Time Figure 2.1. Bipeds experience a relatively higher GRFv than quadrupeds. Modified from Biewener (2003). 5

17 Figure 2.2. The ground reaction force increases with speed in both bipeds and quadrupeds (walk to trot/run to gallop). Modified from Biewener (2003). The position of the upright trunk in bipeds varies throughout the gait cycle (Saha et al., 2008). Its primary motion in both walking and running is flexion and extension within the sagittal plane (Thorstensson et al., 1984; Chung et al., 2010). At faster walking speeds (2.0 ms -1 to 2.5 ms -1 ) trunk flexion increases to 10 to 13 and is similar to that of modest running speeds (2.0 ms -1 to 6.0 ms -1 ) (Thorstensson et al., 1984). However, the preferred speed of individuals is typically 1.4 ms -1 to 1.6 ms -1, a speed that is notably slower than 2.0 ms -1 (Wagnild and Wall- Scheffler, 2013). Flexion-extension excursion defined as the difference between the initial and final positions of the rotating trunk (Pontzer, 2005) is greater in running than in walking 6

18 (Thorstensson et al., 1984; Schache et al., 1999). In walking gait, the trunk s maximum flexion angle increases from 6 at 1.0 ms -1 to 8 at 1.5 ms -1, and its overall stride excursion ranges from 2 to 2.5 (Thorstensson et al., 1984). Trunk angular excursion in running ranges from 2.3 to 23 at varying speeds between 2.0 ms -1 to 7 ms -1 (Schache et al., 1999). Thus, trunk flexion and COM displacement are greater in running gait than in walking gait (Figure 2.3; Thorstensson et al., 1984). Such displacements are energetically costly (Biewener, 2003), particularly because at increasing speed the obliquely orientated human trunk, which comprises 36% of body mass, experiences larger destabilizing GRF and higher velocities (Lieberman et al., 2006; Hamill and Knutsen, 2009; Teng, 2013). When flexed, the trunk s COM lies anterior to the biacetabular axis of the supporting hip joints (Winter, 1995). In this configuration, the vertical vector of gravitational force creates a pitching moment around the hips. Unchecked pitching would lead to rapid displacements of the COM, phenomena which carry increased locomotor cost and risk of injury from joint strain and sudden fall (Biewener, 2003; Hamill and Knutzen, 2009; Perry and Burnfield, 2010). In walking, the trunk pitches posteriorly following FC, while anterior trunk pitch does not occur until midstance (Lieberman et al., 2006). In running, the trunk pitches anteriorly during the first half of stance phase. It reaches its maximum forward pitch shortly after FC, followed by backward pitch in the second half of stance phase (Lieberman et al., 2006; Gazam and Hof, 2007). Because the trunk pitches forward at FC in running, a directional reversal from walking, the evolution of a running persistence strategy in Homo may have selected for enhanced forward pitch mitigation in the form of the enlarged gluteus maximus (Lieberman et al., 2006). 7

19 Walk Run Figure 2.3. The run depicts the aerial phase associated with the gait, which is lacking in the walk. The trunk depiction is representing the greater trunk flexion at foot contact and overall range of motion compared to walking, characteristic of the run gait. Modified from Bramble and Lieberman (2004). 2.3 Foot Kinematics in Shod and Barefoot Running When contacting the ground, runners in traditional thick-soled shoes habitually rear foot strike (RFS) and initiate stance phase with an exted knee and a dorsiflexed foot (Lieberman et al., 2010). In contrast, barefoot (BF) runners typically land with either a midfoot strike (MFS) or forefoot strike (FFS), with a slightly flexed knee and a plantarflexed foot (Squadrone and Gallozzi et al., 2009; Lieberman et al., 2010; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013; Shih et al., 2013). The joint positions common to MFS/FFS running are associated with greater limb compliance and lower GRF at impact than RFS running (Lieberman et al., 2010; Lohman et al., 2011; Altman and Davis, 2012; Giandolini et al., 2013; Kulmala et al., 2013). Magnitude of the GRF and joint loading rates at foot contact significantly differ in RFS and FFS, with MFS variable between RFS and FFS means (Lohman et al., 2011; Altman and Davis, 2012; Giandolini et al., 2013; Kulmala et al., 2013). Although RFS, MFS and FFS 8

20 occur in both barefoot running and shod running (Kulmala et al., 2013), RFS is far more common in shod running, and MFS and/or FFS typically characterize barefoot running (Lieberman et al., 2010; Hatala et al., 2013; Kulmala et al., 2013). Thus, foot strike pattern routinely differs between shod running and barefoot running, as does the GRF. 2.4 Shod versus Barefoot Kinetics in Running An increase in BF lower limb compliance reduces the ground reaction force impact (Lieberman et al., 2010; Lohman et al., 2011; Altman and Davis, 2012; Giandolini et al., 2013; Kulmala et al., 2013). The impact peak magnitude of the GRF vertical component (GRFv), and rate of magnitude increase (loading rates) significantly differ in RFS and FFS. However, MFS values are highly variable between RFS and FFS (Lohman et al., 2011; Altman and Davis, 2012; Giandolini et al., 2013; Kulmala et al., 2013). Running with a RFS, shod or barefoot, produces two peaks in the GRFv, an initial and rapid spike within the first 25% of stance followed by a second peak at midstance (Altman and Davis, 2012; Figure 2.4). The initial spike associated with RFS is absent in FFS (Lieberman et al., 2010; Lohman et al., 2011; Figure 2.4a). Barefoot RFS running exhibits high loading rates compared to MFS/RFS (Lieberman et al., 2010; Shih et al., 2013). A proposed biomechanical adaptation to reduce the otherwise high loading rate and associated heel stress of running with an RFS in the absence of thickly padded shoes is the adoption of a plantarflexed foot strike (FFS) (Divert et al., 2005; Lieberman et al., 2010). Indeed, the GRFv magnitude after impact is lower in BF running (Divert et al., 2005; Kulmala et al., 2013; Samaan et al., 2014; Figure 2.4b; Figure 2.5), and barefoot FFS has lower average loading rates (Kulmala et al., 2013). The differences in GRFv across foot conditions may impact trunk pitch, and therefore the GMAX force necessary to brake the trunk. 9

21 a b Figure 2.4. Vertical ground reaction force versus percent stance time in running. a. Vertical ground reaction force (GRFv) in shod running for rearfoot strike (RFS), midfoot strike (MFS) and forefoot strike (FFS). Two peaks occur in RFS running. Note the presence of an initial spike at 10% stance phase in RFS that is absent in MFS and FFS. b. Vertical ground reaction force for shod RFS and barefoot nonrfs (BF). Note the absence of an initial GRFv spike in BF. Modified from Altman and Davis (2012). BW is body weight. Figure 2.5. Vertical ground reaction force RFS in running. Bold line is shod, light line is barefoot. There is a higher magnitude of peak force in shod RFS running. Note both shod and barefoot produce initial spike after foot contact. Magnitude of initial peak is lower and the first peak is reached earlier in barefoot than in shod running. BW is body weight. Modified from Divert et al. (2005). 10

22 2.5 Shod versus Barefoot Trunk Kinematics in Running The trunk is clearly removed from direct contact with the ground in bipedal running, but its position within the body s kinetic chain may make it responsive not only to the transient ground reaction force but also to the rotations of other segments along the linked chain. Angular rotations of the ankle and knee joints are likely to impact the biomechanics of more cranial segments in the locomotor system (Ford et al., 2013). In a study performed on Tarahumara runners, in both minimalist huaraches sandals and modern conventional shoes, trunk angle at foot contact did not differ with foot strike type (Lieberman, 2014). It has been difficult to parse out any effects of foot strike pattern (RFS, MFS, FFS) from foot condition (shod, minimally shod, barefoot) because there is variation in foot strike pattern among both shod and BF runners (Lieberman, 2014). Yet, when limiting analyses to barefoot running only, Delgado et al. (2013) found that a FFS produced a statistically smaller range of flexion/extension motion in the lumbar spine than a RFS. However, comparing across studies can be difficult because methods of data collection vary. Whereas Lieberman (2014) calculated trunk position as the angle between the greater trochanter and neck center relative to horizontal, Delgado et al. (2013) measured trunk lordosis using a goniometer, capturing only the rotation of the lower back not the entire trunk segment. However, Delgado et al. (2013) also found that the smaller range of upper body motion in FFS barefoot running compared to RFS barefoot running accompanied a significant reduction in shock attenuation with the FFS pattern. Thus, while the hominin transition to ER clearly increased the magnitude of GRF affecting the trunk, the effect of ER on trunk stability remains unclear as does the role of the GMAX in ER. 11

23 2.6 Gluteus Maximus Anatomy and Function The GMAX of African apes is proportional in size to both gluteus medius and gluteus minimus and represents 12-13% of total hip musculature (Lieberman et al., 2006). It is remarkably robust relative to the lesser gluteals in humans, accounting for approximately 18% of hip muscle mass (Haughton, 1873; Zihlman and Brunker, 1979; Lieberman et al., 2006). The GMAX of apes has two heads that are configured with a cranial portion running from the sacroiliac ligament to the iliotibial tract (Figure 2.6a) that function to primarily abduct and laterally rotate the hip, and a smaller caudal head running from the ischial tuberosity to the gluteal tuberosity and lateral femoral epicondyle that exts the hip (Stern, 1972; Swindler and Wood, 1973; Lieberman et al., 2006, Morimoto et al., 2011; Kang et al., 2013). Despite its massive size, the human GMAX lacks two distinctive heads, and its attachment exts to the ilium and to the fascia overlying the multifidus muscle (Stern, 1972; Figure 2.6b). The muscle arises proximally on the ilium posterior to the gluteal line, the fascia of the multifidus, the dorsal surface of the sacrum and coccyx, and the sacrotuberous and sacroiliac ligaments. It inserts on the iliotibial tract, the gluteal tuberosity of the femur, and the lateral intermuscular septum (Stern, 1972; Agur et al., 2009). a b Figure 2.6. Comparison of gluteus maximus (GMAX) musculature chimpanzees (a) and modern humans (b). The GMAX in chimpanzees has two heads, poprius and ishiofemoralis, while the human GMAX has only one head. The human GMAX orientation is more horizontal compared to the chimpanzee s. The singular head of the human GMAX is more robust than either head of the chimpanzee GMAX. Modified from Lieberman et al. (2006). 12

24 Functions of the human GMAX are reported to be primarily hip extension and secondarily lateral rotation of the thigh (Stern, 1972; Agur et al., 2009; Moore et al., 2011). The large muscle may be subdivided into units, based on central nervous system motor tasks, anatomy, and fiber type (McAndrew et al., 2006). McAndrew et al. (2006) report that the GMAX has more Type 1 slow twitch muscle fibers superiorly with a greater proportion of Type 2 fast twitch fibers inferiorly. Although they are activated more slowly, Type 1 fibers have higher fatigue resistance, an important feature for urance activities (Moore et al., 2011). The proportional differences in fiber type within the GMAX suggest that there are functional differences in the superior and inferior regions of the GMAX. The mechanical advantage of a muscle is depent not only on its mass but also on its moment arm (Friederich and Brand, 1990; Lengsfeld et al., 1996), which is a dynamic linear dimension whose length changes during joint rotation (Hamill and Knutzen, 2009). In principle, long moment arms allow muscles to provide greater mechanical force with either less mass or less muscle effort (Lengsfeld et al., 1996; Payne et al., 2006; McArdle et al., 2010; Kang et al., 2013). The GMAX moment arm reaches its maximum length when the trunk is erect (0 flexion) and its minimum length when the trunk is fully flexed (130 flexion) (Lengsfeld et al., 1996). Although trunk rotations are relatively conservative in walking and running, the mechanical advantage of the GMAX in exting the trunk varies throughout the gait cycle as the trunk flexes and exts. Massive size and extensive muscle attachments confer high mechanical advantage to the GMAX in trunk extension, suggesting the GMAX has high mechanical advantage when it comes to braking trunk pitch in running (Lieberman et al., 2006). This is important because according to the ER Hypothesis, GMAX robusticity arose long after the origin of bipedal walking, with the transition to long distance running (Bramble and Lieberman, 2004). 13

25 2.7 Evolution of the Human Gluteus Maximus The ER Hypothesis focuses not only on the mass of the GMAX but also its biomechanically favorable position to brake trunk pitch (Bramble and Lieberman, 2004; Lieberman et al., 2006), which is important for decreasing locomotor energy cost (Biewener, 2003; Perry and Burnfield, 2010). While the GMAX primarily functions as a thigh/hip extensor (Agur et al., 2009; Moore et al., 2011), with the thigh in a fixed position, the muscle acts to ext the trunk (Lovejoy, 1988; Marzke et al., 1988; Kang et al., 2013). The latter function has long been recognized although until Bramble and Lieberman s ER Hypothesis (2004), it was not associated directly with urance running (Karlsson and Jonsson 1964; Fischer and Houtz, 1968; Marzke et al., 1988). Marzke et al. (1988) documented GMAX activation in various activities, throwing, clubbing, digging, and lifting, that were likely important for hominin success pre-homo. EMG data show that during fixed thigh activities, GMAX activation is timed to optimally position the trunk, limit its rotation and brake accelerations (Karlsson and Jonsson 1964; Fischer and Houtz, 1968; Marzke et al., 1988). Despite its focus on activities other than ER, Marzke and colleagues (1988) study demonstrates a functional role of the GMAX in trunk stability. While Marzke et al. (1988) examined GMAX function for dynamic movement, Karlsson and Jonsson (1964) tested GMAX activity for static positions in which trunk and thigh angles varied. Although the greatest GMAX amplitude was recorded with a neutral trunk and exted thigh, fixed thigh activities produced GMAX activity as well (Karlsson and Jonsson, 1964). Activities that fixed the thigh and allowed trunk rotation, scenarios similar to FC in running, generated more GMAX activity with increased trunk flexion, and GMAX activity increased relative to the increase in trunk flexion angle. (Karlsson and Jonsson, 1964). In combination the findings of Marzke et al. (1988) and Karlsson and Jonsson (1964) support an 14

26 argument for a functional role of the GMAX in trunk stability, but neither study addressed the notion or activities for the evolution of a robust GMAX so long after the origin of bipedalism, as the ER Hypothesis does. Lieberman et al. (2006) demonstrated that in running, but not walking, the peak magnitude of GMAX on the stance side occurred shortly after FC, just as the trunk approached its peak pitch velocity. Because GMAX can ext both the trunk and the thigh, researchers also had subjects run with a classic Groucho bent-hip and bent-knee gait, in order to keep the hip strongly flexed at foot strike (Lieberman et al., 2006). Comparison of normal and Groucho running revealed a lower peak magnitude of GMAX in the Groucho gait, indicating that thigh stabilization is not a major function of the GMAX in running. The researchers concluded that GMAX acts primarily to counter trunk pitch, and because rapid acceleration occurs at high speed, they argued a more prominent role of the human GMAX in running than in walking. EMG recordings demonstrate that GMAX produces strong bursts evident in two events of the running gait cycle: the first immediately before heel strike when muscle force is properly timed to brake trunk acceleration, and the second shorter contraction, just prior to mid-swing. By comparison, EMG traces in walking gait lack any true burst of GMAX activity. Early Homo, in running without footwear, would have likely used a variable MFS/FFS as do barefoot runners today (Lieberman et al., 2010; Hatala et al., 2013; Kulmala et al., 2013). Notably, while subjects in the study by Lieberman et al. (2006) ran unshod with the foot s plantar surface overlain by only a thin and flexible foot switch (Figure 2.7), the runners consistently used a rear foot strike (RFS), lacking the variation associated with barefoot running (Lieberman et al., 2010; Hatala et al., 2013; Kulmala et al., 2013). Because the research design did not include shod running, Lieberman et al. (2006) offered no comparison of shod and barefoot kinematics. 15

27 Figure 2.7. Example of thin and flexible foot switches used to signal ground contact. Circular pads are adhered to the plantar surface under the rearfoot and forefoot. Lieberman et al., (2006) employed two switches placing one under the heel and one under the head of the first metatarsal. Image from Bartlett et al. (2014) focused on activation timing and burst magnitude in the superior and inferior portions of the human GMAX (sgmax and igmax, respectively) across a wide range of locomotor activities. Applying an external load to the trunk, these researchers experimentally increased its moment of inertia some 70% during running. As a result, GMAX peak activity increased 23% but only within the igmax. Unlike urance running, both sgmax and igmax activity increased during climbing, jumping and sprinting. These authors (Bartlett et al., 2014) concluded that the ER Hypothesis fails to explain the evolutionary origin of the large human GMAX based on their finding that GMAX activity in both the superior and inferior portions of the muscle increased during non-er activity. However, it must be noted that while the Bartlett et al. (2014) findings do not support the ER Hypothesis, they also do not falsify it. Bramble and Lieberman (2004) describe numerous adaptations in early 16

28 Homo that are consistent with the high loading forces and gait biomechanics of long distance running. While Lieberman et al. s (2006) argument for the enhancement of the GMAX in Homo does not preclude climbing, jumping, walking, or throwing as GMAX related activities, the ER Hypothesis emphasizes a derived locomotor strategy with strong selection pressure for the enlargement of the ancestrally small GMAX. 2.8 Summary The ER Hypothesis for hypertrophy of the human GMAX is premised on the acquisition of a long distance urance running strategy (Bramble and Lieberman, 2004; Lieberman et al., 2006). Given that FFS/MFS running produces a lower GRFv than RFS, differences in joint accelerations and excursions are expected in barefoot and shod running with implications for the mechanical advantage and force production of GMAX. To date, the timing and magnitude of GMAX activity and trunk kinematics have not been thoroughly investigated in barefoot versus shod runners. To better understand the linkage between GMAX robusticity and ER, this thesis compares GMAX function and trunk kinematics during human walking and running, both shod and barefoot. 17

29 3. Hypotheses The hypotheses tested in this thesis research were based on the published kinematic, kinetic, and GMAX EMG studies presented above. There are few studies that address trunk kinematic differences between shod and barefoot gait, and those that do vary in methods and variables. Other known and published biomechanical differences introduced in the Chapter 2, along with biomechanical principles, were used to generate the following three hypotheses: Trunk kinematics differ between shod and barefoot running (section 3.1); sgmax and igmax amplitudes differ between walking and running at the same speed, 2.0 ms -1 (section 3.2); and sgmax and igmax amplitudes differ between shod and barefoot running (section 3.3). The hypotheses are outlined and discussed in detail below. 3.1 Hypothesis 1: Trunk Kinematics Differ in Shod versus Barefoot Running Because lower limb kinematics differ in shod and barefoot running (i.e., barefoot running characteristically involves a more flexed knee and a less dorsiflexed foot at contact; Squadrone and Gallozzi et al., 2009; Lieberman et al., 2010; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013; Shih et al., 2013), kinematics within the superior segment of the runner s kinetic chain are also likely to differ (Ford et al., 2013). Furthermore, it has been argued that the trunk generally maintains a more upright orientation in barefoot running than in shod running (Lieberman, 2014). Vertical alignment of the upper body COM and the hip joints reduces the torque applied by the ground reaction force at contact (Biewener, 2003). Reduced torque should result in less trunk angular momentum (Biewener, 2003). Therefore, I predict a reduction in trunk angular excursion and segment acceleration from shod to barefoot running. This is likely to be associated with a forefoot strike (FFS) and a midfoot strike (MFS), because 18

30 both strike patterns characterize barefoot running more often than shod running (Kulmala et al., 2013). 3.2 Hypothesis 2: GMAX Force Production Differs in Walking versus Running at 2.0 ms -1 The ER Hypothesis predicts that the robust human GMAX evolved in association with a long distance running strategy some two million years after habitual bipedal walking (Bramble and Lieberman, 2004). If this were the case, then activation and amplitude patterns of the GMAX should differ between walking and running gaits, not with speed difference alone. Therefore, I predict that the sgmax and igmax amplitude will differ at a given speed during running and walking, and amplitude of the igmax and sgmax, and the GRFv will be greater in running than in walking. 3.3 Hypothesis 3: GMAX Force Production Differs in Shod versus Barefoot Running The GRF is lower during FFS than RFS during the beginning of stance phase and lacks the initial impact peak (Lohman et al., 2011; Altman and Davis, 2012; Giandolini et al., 2013; Kulmala et al., 2013). Due to the predicted smaller flexion angle of the trunk, a greater GMAX lever arm is anticipated, which would expectedly increase mechanical advantage (Lengsfeld et al., 1996). High mechanical advantage is beneficial for runners because a less costly contraction is required of the GMAX in order to produce sufficient force to brake trunk pitch (McArdle et al., 2010). Thus, I predict that amplitude of the sgmax and igmax will be lower in barefoot running than in shod running. 19

31 4. Methods 4.1 Subjects Study participants included twenty-four physically active adults between the ages of 18 and 30 years (twelve males and twelve females) who were of normal body mass index (BMI) (Height: 171 cm ± 10.2; Weight: 65 kg ± 7.9; McArdle et al., 2010) and free of injury and pain participated (Table 4.1). Study protocol received approval by the University of Cincinnati (UC) Institutional Review Board ( ). Recruitment fliers and s were used to solicit subjects at the University as well as local running clubs (Appix A). Subjects gave their full informed and written consent upon enrollment and were able to withdraw at any time; zero withdrew. Table 4.1. Sex, age, height, and weight for each study participant. Subject Sex Age Height Weight (years) (cm) (kg) 1 F M F F M F F F M M M M M M F F M M M M F F F F

32 4.2 Equipment Kinematic, EMG, and kinetic data were collected in the Human Evolutionary and Locomotor Laboratory in the UC Department of Anthropology (Braunstein Hall 444). Kinematic data were recorded at 200 Hz with a Vicon MX eight-camera 3D motion caption system (MX 3D Vicon Motion Systems, Centennial, CO, USA). EMG was captured at 4,000 Hz with portable Powerlab hardware and Chart 7 software supplied on loan from the UC Department of Biological Sciences. The Powerlab equipment consisted of a 16sp AD converter, two double channel amps, and one single channel amp. The EMG equipment and Vicon system were synced via an external trigger system; the Vicon data collection start initialized EMG data collection. 4.3 Kinematic Data Collection Participants wore taught spandex shorts customized with open ports for placement of GMAX electrodes. Females additionally wore spandex sports bras. Because footwear influences strike patterns and joint angles (Kong et al., 2009), all subjects were provided with new Asics, Gel-Cont 2 shoes to control for the effects of shoe variation. This thickly-soled footwear was expected to elicit a uniform RFS (Squadrone and Gallozzi et al., 2009; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013) and was worn by all participants during shod trials. Subjects were allowed time to walk on the treadmill for a self-determined period of acclimation to the provisioned footwear and the sensation of barefoot contact on the moving deck. After completing all walking trials, subjects were allowed self-determined periods of warm-up running. After reporting they were comfortable with gait, speed, and foot condition, relevant trials began. In order to track movement of body segments, small 14 mm reflective markers traceable by Vicon 3D were adhered to subjects by double-sided tape at bony landmarks. The markers were placed over the bony processes of glabella, seventh cervical 21

33 vertebra (C7), xiphoid, and bilaterally for the following; mastoid process, acromion process, olecranon process, distal radius, anterior superior iliac spine, posterior superior iliac spine, greater trochanter, lateral condyle, lateral malleolus, heel, and 5th metatarsal head. Additionally, segment markers were positioned over the right and left midthigh and right and left midshank. Kinematic data were used to calculate sagittal angles of the trunk, thigh, and foot, and velocity of the trunk. 4.4 EMG Data Collection EMG data were collected only from the left side of the body. To remove any surface oil or grit that might limit signal impedance, the skin was wiped with rubbing alcohol and lightly brushed with an abrasive pad prior to electrode placement. Foam electrodes (Kall, Medi- Trace Mini EG 100) were placed in pairs at a 2 cm inter-electrode distance overlying the sgmax and igmax with a 14.5 cm distance between the muscles in order to record the contraction activity of each muscle (Figure 4.1). The reference electrode was placed on the right spine of the scapula. EMG leads were secured to the body with a Stress Belt (Danlee Medical) and leads were merged in the belt pocket along the subject s back at mid-level between the xyphoid and pelvic markers, not shown in Figure 4.1. Figure 4.1. EMG electrode placement and setup of the semg and iemg. 22

34 4.4.1 EMG Electrode Placement Validation: Human Cadaver Dissection Dissection was performed to validate the EMG electrode placement and muscle fascicle orientation on an adult male GMAX in the Senior Elective Anatomical Lab at the UC College of Medicine. The donor was anonymous, and no medical record, age, height, or weight were available. The left arm had been amputated mid length along the humeral shaft and soft tissues appeared fully healed. There were no indications of asymmetrical effect on size and shape of other body segments. Pelvic musculature lacked any noticeable irregularities. Only the most superficial layer of pelvic musculature was dissected. The first incision began at the sagittal midline of the body superior to the iliac crest and proceeded laterally to the greater trochanter. The second incision was made medial and inferior to the gluteal fold along the hamstrings of the right leg from the medial to lateral. A third incision connected the two transverse cuts vertically along the midline of the body. The skin overlaying the GMAX was reflected medio-laterally exposing the superficial fat tissue. Fat deposits were removed exposing the superior, medial, and inferior border of the GMAX muscle. Fascicles were aligned mediolaterally in the superior region (sgmax) and transitioned inferiorly to an oblique orientation (Figure 4.2). Once the dissection of the superficial layer was completed, a cut was made along the sacral line to detach the muscle. The GMAX was then reflected laterally. Measurements were taken of the muscle superioinferior length, depth, and mediolateral breadth. Muscle depth varied; the lateral portion was thicker than the medial, and the thickness decreased superioinferiorly (Figures 4.3; 4.4; 4.5; 4.6). 23

35 Figure 4.2. The most superficial view of the gluteus maximus after the dermis was removed. Muscle fascicle orientation is more horizontal in the superior region and becomes more oblique inferiorly. Change in fascicle orientation is shown with orientation of arrows. Figure 4.3. Superficial craniocaudal length of lateral portion of the gluteus maximus (22.8 cm). 24

36 Figure 4.4. Length of medial portion of the gluteus maximus at the attachment site to the sacrum (10.5 cm). Figure 4.6. Depth of medial gluteus maximus around sacral attachment site (1.2 cm). Figure 4.5. Depth of superior, lateral gluteus maximus (3.3 cm). 25

37 Figure 4.6. Depth of medial gluteus maximus around sacral attachment site (1.2 cm). The orientation of the GMAX fascicles, and the size and shape of the muscle influenced the overlying soft tissue placement of the GMAX electrodes. As a result of the dissection, the superior electrodes were placed more horizontally while the inferior more obliquely to follow the muscle fascicle orientation (Figure 4.1). 4.5 Gait Speeds Each subject performed a total of fifty-nine trials, five of which were static and fifty-four dynamic. Static trials consisted of force plate quiet stance, treadmill quiet stance shod and barefoot, and treadmill t-stance (arms held out parallel to the floor in the shape of a T), shod and barefoot. The force plate static trials provided the subjects body weight. In order to standardize angles across subjects, baseline angles were calculated for each subject from static trials that were recorded on the treadmill in both shod and barefoot conditions. Varied speeds were needed to determine if change in speed affect GMAX force production as well as trunk position at foot 26

38 contact. Every subject performed three ten-second treadmill trials at each speed described below, both shod and barefoot. Walking speeds were 1.25 ms -1, 1.5 ms -1, 1.75 ms -1, 2.0 ms -1, and running speeds consisted of 2.0 ms -1, 3.0 ms -1 and 4.0 ms -1. Walking trials were required to confirm that the GMAX activates differently during walking and running gaits based on the predictions of the ER Hypothesis (Lieberman et al., 2006, Bartlett et al., 2014). Speeds were categorized numerically from 1 to 7 in increasing order for data processing and analyses. 4.6 Kinematic Processing Captured trials were reconstructed in Vicon and raw.csv files were input into Matlab (Math Works, Inc., Natick, MA, USA). Custom scripts (Appix B) first filtered the data through a Butterworth 4 th order low pass filter with a 10Hz cutoff, and then calculated joint angles, velocities, and excursions. Trunk and thigh angles were calculated against the global horizontal (Figure 4.7). Values at FC, as well as maxima and minima of trunk and thigh variables were produced for the entire trial. Global Horizontal 0º Trunk Thigh θ θ Foot θ Figure 4.7. Foot, trunk, and thigh angles calculated against the horizontal from the trochanter marker. Foot angle is depicted as 0 in this figure, negative is dorsiflexion (toe above horizontal reference line) and positive is plantarflexion (heel above horizontal reference line). For the thigh and trunk absolute vertical is

39 Table 4.2. Variable definitions and abbreviations. Variable Definition- FCfootAng Foot)angle)at)foot)contact FCtrunkAng Trunk)angle)at)foot)contact FCtrunkVel Trunk)velocity)at)foot)contact FCthighAng Thigh)angle)at)foot)contact FCthighVel Thigh)velocity)at)foot)contact MaxTrunkVel Maximum)trunk)pitch TrunkExcu Overall)stride)trunk)angle)excursion FCtrunkExcu Thigh)angle)displacement)from)foot)contact)to)maximum)extension FCtrunkVelExcu Thigh)velocity)difference)from)foot)contact)to)maximum)posterior)velocity semg EMG)amplitude)average)25)milliseconds)pre)and)post)foot)contact)for)the)superior)GMAX iemg EMG)amplitude)average)25)milliseconds)pre)and)post)foot)contact)for)the)inferior)GMAX LHEL Left)heel)reflective)marker LMT5 Left)fifth)metatarsal)head)reflective)marker Velocity of the left fifth metatarsal head (LMT5) and left heel (LHEL) markers were determined in Matlab. FC was identified by the marker, either LHEL or LMT5, in the stride that first reached zero vertical velocity from the negative direction (Appix B). The vertical Z plane coordinates were traced in Vicon to check the Matlab FC pattern (Figure 4.8). The marker that reached its vertical nadir first determined FC. Variables calculated and analyzed to assess kinematics at foot contact included foot angle (FCfootAng), trunk angle (FCtrunkAng), trunk velocity (FCtrunkVel), thigh angle (FCthighAng), thigh velocity (FCthighVel). The FCfootAng is positive when the LMT5 maker has greater vertical height than the LHEL (dorsiflexion) and negative when the LHEL marker has greater height than the LMT5(plantarflexion). Other variables of interest calculated and analyzed include the maximum trunk velocity (MaxTrunkVel), overall trunk angle excursion (TrunkExcu), foot contact to maximum angle trunk (FCtrunkExcu), and thigh (FCthighExcu) excursions, and foot contact to maximum velocity trunk (FCtrunkVelExcu), and thigh (FCthighVelExcu) excursions. Excursions are differences in angles or velocities between two events in the stride pattern. FC variable excursions were calculated using FC values minus the extrema following FC that correspond 28

40 with the variables GMAX segment function (Appix C). Flexion angles and forward velocity were used for the trunk, while extension angles and backward velocity were used for the thigh to correspond with the GMAX known functions. Figure 4.8. Graph of heel (red) and fifth metatarsal (green) markers position in the vertical z plane during trials. The marker that reached the z nadir first determined which marker to use for foot contact to get an accurate frame for stride FC calculations. The vertical blue bar depicts a FC event with the heel reaching its vertical minimum first. 4.7 EMG Processing EMG files were opened in LabChart7 (Mac) and saved as MATLAB files. Raw EMG data were bandwidth filtered using 20Hz, 400Hz cut-offs. The data were then full wave rectified and low pass filtered at a 50 Hz cutoff frequency. In order to compare across subjects, EMG were normalized to each subject to account for individual variation. Walking amplitude differences were expected to be minimal compared to those in running, so signals were normalized to each subject s maximum peak during shod walking at 1.25 ms -1. EMG data were 29

41 averaged from 5 frames (25 milliseconds) before and after FC to determine GMAX activity prior to and following contact with the ground (semg and iemg, respectively). 4.8 Analyses Kinematic and muscle amplitude data were truncated to a uniform number of strides per condition per subject, based on the first five good quality FC events in the first two trials of each speed (n =10). They were then transferred to SPSS (IBM Corp, Armonk, NY, USA) for statistical analysis. Data were tested for normal distribution using Shapiro-Wilk Tests and for homoscedasticity using Levene s Tests of Equality of Error Variances as bases for parametric or non-parametric testing. The majority of variables lacked normal distribution and equal variance. Therefore, non-parametric tests were used. Grand means of the 10 strides, for each subject at each condition were calculated and used for all statistical tests. In order to test for between-gait differences, a Sign Rank t-test was performed for each variable at 2 ms -1 paired for running and walking. The sign test was executed instead of a non-parametric Wilcoxon signed-rank test because the majority of variables related group differences were not symmetrically distributed (Laerd Statistics, 2016). Since the study design involved repeated measures, Friedman s tests were run to determine if there were any significant differences between speed and foot condition for all variables of interest. Significant correlations between subjects were considered to be weak (±) , fair (±) , moderate (±) , and strong (±) (Bacchieri and Cioppa, 2007). The level of statistical significance was set at P < 0.05, and significant results within multi-test comparisons were P adjusted using a modified Bonferroni Stepwise Correction calculation (Rice, 1989). 30

42 5. Results 5.1 Foot Kinematics in Barefoot and Shod Conditions For all subjects, walking gaits were performed with a dorsiflexed foot and a clear heel strike (RFS) regardless whether the foot was shod or unshod (Figure 5.1; Table 5.1). At all walking speeds, the unshod foot at heel-ground contact was less dorsiflexed than the shod foot (all P-values = 0.0; Table 5.2). With speed held constant at 2.0 ms -1, foot position statistically differed between walking and running in both shod and barefoot conditions (all P-values = 0.0; Table 5.3). Mean foot angle at contact was less dorsiflexed (more positive) in running gait (run shod ±6.61, run BF 0.05 ±10.68 ; mean ± SD) than in walking gait (walk shod ±3.3, walk BF ±4.86 ; Figure 5.1). The mean differences in FCfootAng between barefoot and shod conditions were statistically significant for all running speeds (all P-values = 0.0; Table 5.2). Runners used a RFS when shod and more often used a MFS/FFS (plantarflexion) or a near MFS when barefoot (run shod ±6.61, run BF 0.05 ±10.68 ; Table 5.1). Mean foot angle at contact in barefoot running approximated 0 (MFS) across running speeds (Figure 5.1). Dispersion around the foot angle was greater in running gait than in walking gait (walk shod ±3.3, walk BF ±4.86, run shod ±6.61, run BF 0.05 ±10.68 ; Table 5.1; Figure 5.1). Among the twenty-four subjects, eight dorsiflexed and four plantarflexed in both foot conditions (Table 5.1). Additionally, five who dorsiflexed when running shod, plantarflexed when barefoot. Finally, seven dorsiflexed when shod but used variable foot angles when running barefoot. Out of the seven subjects who varied in strike pattern when running barefoot, five plantarflexed at 4.0 ms -1 and dorsiflexed at the slower speeds. The remaining subjects dorsiflexed at the 2.0 ms -1 run and plantarflexed at the higher running speeds. Overall, 31

43 these patterns show high variability in foot angle at contact (foot strike pattern) among study subjects while running. Figure 5.1. Normalized mean foot angle and standard deviation for shod and barefoot conditions at foot contact. Negative angles indicate dorsiflexion (RFS), neutral angle flatfoot (MFS) and positive angles plantarflexion (FFS). Table 5.1. Mean and standard deviation for variables of interest at all speeds in both foot conditions (shod and barefoot). 32

44 Table 5.2. P-values of Sign Rank Test between foot conditions (shod and barefoot) at each speed. Significant variables are shaded. Table 5.3. P-values of Sign Rank Test between walking and running gaits at 2.0 ms -1. Significant variables are shaded. 5.2 Kinematics in Shod and Barefoot Gaits Trunk Kinematics Differ in Shod versus Barefoot Conditions (Hypothesis 1) Whether shod or barefoot, trunk position at foot contact was significantly more flexed in running gait than in walking gait (walk shod ±3.33, walk BF ±3.87, run shod ±3.0, run BF ±3.54 ; all P-values < ; Figure 5.2; Tables 5.3; 5.4). Mean trunk position at contact also differed between barefoot and shod conditions (Figure 5.4) The trunk was significantly less flexed at foot contact in barefoot walking at speeds greater than 1.25 ms -1 and in barefoot running at 3.0 ms -1 (all P-values < 0.023; Table 5.2). The trunk s overall range of motion throughout the stride significantly increased as speed increased within gait type (all P- values < 0.023; Figure 5.3; Table 5.4). However, the range of motion was smaller in running 33

45 than in walking (walk shod 9.02 ±0.08, walk BF 8.98 ±2.11, run shod 4.15 ±1.37, run BF 5.05 ±2.93 ; all P-values = 0.0; Table 5.3). There were no significant differences in range of motion between shod and barefoot conditions at walking speeds (Table 5.2). In contrast, at running speeds of 2.0 ms -1 and 3.0 ms -1 mean trunk excursion differed significantly between barefoot and shod conditions, with a greater range of motion in barefoot running (all P-values < 0.007). The trunk pitched backward at foot contact in walking (Figure 5.4), with slightly greater pitching as walking speed increased. However, in running, as expected, the trunk pitched forward at impact (Figure 5.4). Pitch rate increased with speed more sharply in running than in walking. Rates were greater in running than in walking for both shod and barefoot conditions (Tables 5.1; 5.4). Overall, the rate of trunk pitch did not differ between barefoot and shod gaits for a given speed, except at the highest running speed of 4.0 ms -1 in which the trunk pitched more rapidly with barefoot running (shod 30.0 ±17.56 s -1, BF ±18.03 s -1 ; P = 0.002; Table 5.2). However, the maximum rate of forward trunk pitch significantly differed between foot conditions running at 3.0 ms -1 and 4.0 ms -1 with barefoot running having higher forward peak pitch rates (all P-values < 0.007; Figure 5.5; Tables 5.1; 5.2). Walk Run Shod Barefoot 15 Walk Run Shod Barefoot Trunk Angle at Foot Contact [ o ] Total Trunk Angle Excursion [Δ o ] Speed [ms -1 ] Speed [ms -1 ] Fig Normalized mean trunk angle and standard deviation for shod and barefoot conditions at foot contact by speed. 90 is absolute vertical. Flexion < 90. Extension > 90. Figure 5.3. Normalized mean trunk angle excursion and standard deviation for shod and barefoot conditions. Maximum trunk extension to maximum trunk flexion within the stride. 34

46 60 50 Walk Run Shod Barefoot Walk Run Shod Barefoot Trunk Velocity at Foot Contact [ o /s] Max Trunk Velocity [ o /s] Speed [ms -1 ] Figure 5.4. Trunk mean angular velocity (pitch rate) and standard deviation for shod and barefoot conditions at foot contact Speed [ms -1 ] Figure 5.5. Maximum trunk angle velocity means and standard deviations for shod and barefoot conditions Thigh Kinematics in Shod and Barefoot Conditions Whether shod or barefoot, thigh position at foot contact was significantly more exted in running gait than in walking gait (walk shod ±2.95, walk BF ±5.41, run shod ±3.31, run BF ±5.38 ; all P-values = 0.0; Figure 5.6; Tables 5.3; 5.4). Although mean thigh position was more exted at FC in BF conditions, the means difference between barefoot and shod thigh position was nonsignificant (Figure 5.4). The thigh s range of motion from FC to maximum extension significantly increased as speed increased within gait type (all P-values < 0.034; Figure 5.7; Table 5.4). The range of motion was greater in running than in walking (walk shod ±3.84, walk BF ±3.94, run shod ±5.04, run BF ±4.47 ; all P-values = 0.0; Table 5.3). There were significant differences in range of motion between shod and barefoot conditions at all walking speeds and at 4.0 ms -1 running (all P-values < 0.023; Table 5.2). The thigh velocity was approximately 0 s -1 as the limb decelerated at FC and began to pitch backward in stance phase (Figure 5.8). Thigh velocity at FC differed significantly only at 35

47 4.0 ms -1 between foot conditions (shod ±36.59 s -1, BF ±36.39 s -1 ; P = 0.002; Table 5.2). Further, thigh velocity differed for shod but not BF (walk shod ±18.15 s -1, run shod 7.34 ±37.67 s -1 ; P = 0.007; Table 5.3). Thigh Angle at Foot Contact [ o ] Walk Run Shod Barefoot Foot Contact Thigh Angle Excursion [Δ o ] Walk Run Shod Barefoot Speed [ms -1 ] Figure 5.6. Normalized thigh angle means and standard deviations for shod and barefoot conditions at foot contact Speed [ms -1 ] Figure 5.7. Normalized thigh angle excursion means and standard deviations for shod and barefoot conditions at foot contact. Foot contact (FC) to maximum thigh extension after FC Walk Run Shod Barefoot Foot Contact Thigh Velocity Excursion [Δ o /s] Speed [ms -1 ] Figure 5.8. Thigh angle velocity excursion means and standard deviations for shod and barefoot conditions. Foot contact (FC) to maximum posterior velocity after FC. 36

48 Table 5.4. P-values of Friedman s non-parametric repeated measures test between all seven speeds for variables shod and BF. Cells shaded gray Bonferonni Stepwise significant values. w is a walking gait and r is a running gait ms - 1, 1.5 ms ms - 1, 1.25 ms - 1, 1.75 ms ms - 1 walk 1.5 ms - 1, 1.5 ms - 1, 1.75 ms ms - 1 walk 1.75 ms - 1, 2.0 ms - 1 walk 1.25 ms - 1, 2.0 ms - 1 run 1.25 ms - 1, 3.0 ms ms - 1, 1.5 ms - 1, 3.0 ms ms - 1 run 1.5 ms - 1, 3.0 ms ms - 1, 1.75 ms - 1, 4.0 ms ms - 1 run 1.75 ms - 1, 3.0 ms ms - 1, 2.0 ms ms - 1 walk, 2.0 ms - 1 run w,w w,w w,w w,w w,w w,w w,r w,r w,r w,r w,r w,r w,r w,r w,r w,r w,r w,r r,r r,r r,r FCfootAng FCtrunkAng FCtrunkVel FCthighAng FCthighVel MaxTrunkVel TrunkExcu FCtrunkExcu FCtrunkVelExcu FCthighExcu FCthighVelExcu semg iemg FCfootAng FCtrunkAng FCtrunkVel FCthighAng FCthighVel MaxTrunkVel TrunkExcu FCtrunkExcu FCtrunkVelExcu FCthighExcu FCthighVelExcu semg iemg ms - 1 walk, 3.0 ms ms - 1 walk, 4.0 ms ms - 1 run, 3.0 ms ms - 1 run, 4.0 ms ms - 1, 4.0 ms - 1 Barefoot Shod 37

49 Table 5.5. P-values for all pairwise comparisons from the Freidman s test between walking (w) speeds only. Gray cells are significant after Bonferroni corrections (p <0.05). Shod Barefoot 1.25 ms - 1, 1.25 ms, ms - 1 ms ms - 1, 2.0 ms - 1 walk 1.5 ms - 1, 1.75 ms ms - 1, 2.0 ms - 1 walk 1.75 ms - 1, 2.0 ms - 1 walk w,w w,w w,w w,w w,w w,w FCfootAng FCtrunkAng FCtrunkVel FCthighAng FCthighVel MaxTrunkVel TrunkExcu FCtrunkExcu FCtrunkVelExcu FCthighExcu FCthighVelExcu semg iemg FCfootAng FCtrunkAng FCtrunkVel FCthighAng FCthighVel None Sig, No Pairwise MaxTrunkVel TrunkExcu FCtrunkExcu FCtrunkVelExcu FCthighExcu FCthighVelExcu semg iemg Table 5.6. P-values for all pairwise comparisons from the Freidman s test between running (r) speeds only. Gray cells are significant after Bonferroni corrections (p <0.05). Shod Barefoot 2.0 ms - 1 run, 3.0 ms ms - 1 run, 4.0 ms ms - 1, 4.0 ms - 1 r,r r,r r,r FCfootAng FCtrunkAng FCtrunkVel FCthighAng FCthighVel MaxTrunkVel TrunkExcu FCtrunkExcu FCtrunkVelExcu FCthighExcu FCthighVelExcu semg iemg FCfootAng FCtrunkAng None Sig, No Pairwise FCtrunkVel FCthighAng FCthighVel MaxTrunkVel TrunkExcu FCtrunkExcu None Sig, No Pairwise FCtrunkVelExcu FCthighExcu FCthighVelExcu semg iemg

50 5.3 GMAX Force Production Differs in Walking versus Running at 2.0 ms -1 (Hypothesis 2) Despite the kinematic differences in walking and running at 2.0 ms -1, the average EMG amplitude produced by the sgmax and igmax did not differ significantly with gait based on a pairwise Rank Signed Test of mean magnitudes and a Friedman s One Way ANOVA for repeated measures (all P-values > 0.05; Figures 5.9; 5.10; Table 5.3; 5.4). Thus, gait type alone does not appear to be a factor in GMAX force production, at least at a speed of 2.0 ms -1. However, when comparisons are made between walking and running at varying gait speeds, significant differences in muscle EMG amplitude result (Table 5.4). For example, both iemg and semg significantly differ between walking at 1.25 ms -1 and all running speeds Walk Run Shod Barefoot 10 8 Walk Run Shod Barefoot semg 2 iemg Speed [ms -1 ] Speed [ms -1 ] Figure 5.9. Normalized superior gluteus maximus amplitudes around foot contact for shod and barefoot conditions. Figure Normalized inferior gluteus maximus amplitudes around foot contact for shod and barefoot conditions. 39

51 Table 5.7. Kall's tau_b correlation coefficients and p-values for 4.0 ms -1 shod and barefoot. Correlations shaded in light gray are fair correlations (± ). Values shaded in dark gray are moderate correlations (± ). 40

52 5.4 GMAX Force Production Differs in Shod versus Barefoot Running (Hypothesis 3) While the mean amplitude of both sgmax and igmax overall increased with speed (Figures 5.9; 5.10; Tables 5.4; 5.5; 5.6), and the speed differences were greater in running than in walking, there were no significant differences in sgmax or igmax between shod and barefoot conditions at any running speed, counter to Hypothesis 3 (Table 5.2). Positive Kall s correlations between the GMAX muscles and the kinematic variables are weak overall (Table 5.7). Other than the correlation between the muscles (shod: igmax, sgmax, 0.335), no other fair, moderate, or strong correlations occur between the GMAX and kinematic variables. Trunk pitch at foot contact positively correlates more strongly with GMAX when shod (semg, 0.295; iemg, 0.225) than barefoot (semg, 0.160; iemg, ). 41

53 6. Discussion My primary goal in this research was to investigate trunk kinematics in shod and barefoot running. Further, if differences were identified, I aimed to explore what evolutionary implications they had for the role of the gluteus maximus (GMAX) in trunk biomechanics. In order to test Bramble and Lieberman s (2004) Endurance Running (ER) Hypothesis, I tested kinematic and EMG variables not only between foot conditions (shod and barefoot) but also between gaits (walking and running) and gait speeds (1.25 ms ms -1 ). I discuss results from the three comparisons and their relevance to the ER Hypothesis in the following sections. 6.1 Foot Strike Patterns The strike angle of the stance foot in walking was in agreement with results previously reported in the literature (De Clercq et al., 1994; De Wit et al., 2000; Roberts et al., 2011). Dorsiflexion at foot contact produced a definitive rearfoot strike (RFS) characteristic of walking gait. Foot strike patterns in running gait varied. Some runners used a less dorsiflexed foot and retained a slight heel strike while others repositioned the foot more dramatically using either a midfoot strike (MFS) or a forefoot strike (FFS). The MFS and FFS patterns predominantly occurred in barefoot running consistent with other reports (Squadrone and Gallozzi et al., 2009; Lieberman et al., 2010; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013; Shih et al., 2013). Also in agreement with previous studies, barefoot running, unlike shod running, involved a less dorsiflexed foot, or a fully plantarflexed foot (Lieberman et al., 2010; Hatala et al., 2013; Kulmala et al., 2013). Barefoot walkers also used a less dorsiflexed foot at heel strike than shod walkers. While a more neutral strike angle increases heel pad deformation and therefore increases capacity of the foot to dampen ground reaction forces (De Clercq et al., 1994; De Wit et al., 2000), impact force 42

54 during walking gait is considerably lower than during running gait (Keller et al., 1996; Biewener, 2003). Soames (1985) reported pressure differences between shod and barefoot walking. While shod walking produced a more uniform pressure under the rearfoot calcaneus, barefoot walking resulted in greater pressure under the forefoot metatarsals. Because foot strike angle was not quantified in Soames study, it remains uncertain if the barefoot walkers used a rearfoot strike, neutral strike, or forefoot strike. Furthermore, while pressure may be a causal factor of foot placement in running barefoot, reduced heel pressure in walking barefoot may merely be a consequence of reduced dorsiflexion. That is, an alternative explanation for strike angle in barefoot walking may have more to do with foot kinematics than with foot strike kinetics. Walking without a thick-soled shoe shortens foot height. Without the added sole thickness, the ankle of the unshod foot rotates farther toward plantarflexion (toe-down) before striking (Roberts et al., 2011). 6.2 Kinematics in Shod versus Barefoot Gaits Trunk Kinematics Differ in Shod versus Barefoot Conditions (Hypothesis 1) At ER speeds I expected barefoot runners to maintain a more upright trunk with less forward pitch than shod runners (Hypothesis 1). As predicted, the trunk at foot strike was less flexed in barefoot running, indicating support for trunk position at foot contact in Hypothesis 1. This characteristic was also reported by Lieberman (2014), who found that minimally shod runners have a more upright trunk at impact compared to runners wearing thickly soled shoes. Moreover, trunk motion differs between barefoot and shod running, with excursions being greater in barefoot running, contrary to the prediction of trunk pitch in Hypothesis 1. Not only is the barefoot trunk less flexed at foot contact it also rotates more following contact than shod running (Figure 6c-d; 6g-h). This greater range of motion could be attributed to trunk pitch 43

55 differences. Forward pitch defined as the trunk s maximum angular velocity and its angular velocity at foot strike is greater in barefoot running than in shod running. Saha et al. (2008) conducted research on normal gait and two flexed trunk gaits (25 and 50 ). Saha and colleagues (2008) found higher step frequencies and shorter step lengths, and greater stance knee flexion in flexed trunk gait compared to normal gait. The researchers argued that compensatory kinematics, caused by a flexed trunk, alter the COM alignment and trajectory. This is inferred based on a phase shift that results in the trunk accelerating downward in a flexed trunk gait directly before foot contact, which is in contrast to its deceleration downward in normal gait directly before foot contact (Saha et al., 2008). Because the lower limb kinematics found in Saha et al. (2008) are similar to barefoot running kinematics (Lieberman et al., 2010; Lohman et al., 2011; Altman and Davis, 2012; Giandolini et al., 2013; Kulmala et al., 2013), a similar COM phase shift may occur in barefoot running. Thus, despite the less flexed position of the trunk at foot contact in barefoot running, the lower limb kinematics associated with barefoot running may alter the COM. In this thesis the trunk pitched backward prior to shod foot contact and then pitched forward after foot contact (Figure 6c-d). However, in barefoot running the trunk continues to pitch forward before and after foot contact (Figure 6g-h). This sustained forward pitch may explain the greater maximum pitch and range of motion identified in barefoot running Thigh Kinematics in Shod and Barefoot Conditions Thigh angle and angular velocity did not differ between foot conditions at most speeds (Table 5.2). This is somewhat surprising given differences reported for lower limb joints (Squadrone and Gallozzi et al., 2009; Lieberman et al., 2010; Lussiana et al., 2013; Rooney and Derrick, 2013; Schutte et al., 2013; Shih et al., 2013). Angular excursion of the thigh at walking 44

56 speeds ts to be greater in barefoot walking than in shod walking, a difference consistent with the larger trunk excursions of barefoot walking. This again may be attributable to inexperience with barefoot gait on a treadmill. In barefoot running, strides t to be shorter and the contact foot lands more centrally under the body (De Wit et al., 2000; Divert et al., 2005; Kerrigan et al., 2009; Squadrone and Gallozzi, 2009; Lieberman et al., 2010), resulting in a less flexed thigh at foot contact as documented in this thesis (Figure 5.3). However, despite a less flexed thigh at foot contact, the maximum thigh extension angle is greater in barefoot running than in shod running. Maximum extension in running occurs after toe off and in walking around toe off. The late-stance and swing phases of the stride, where maximum extension occurs, are not addressed in this thesis research. Future research should test other lower limb muscles in association with kinematics to better understand the increased range of motion in barefoot gait. The significant difference between foot conditions at high running speeds could be an exaggerated outcome of speed increase effects, such as elevating segmental (thigh) velocities or range of motions (Mann and Hagy, 1980; Nilsson et al., 1985; Novacheck, 1998). More research is needed to better understand the influence of foot condition differences on speed effects of segment kinematics. 6.3 GMAX Force Production Differs in Walking versus Running at 2.0 ms -1 (Hypothesis 2) I predicted greater EMG amplitudes for superior and inferior GMAX in running than walking. The findings do not support Hypothesis 2. Mean EMG amplitude of GMAX at foot contact is indistinguishable for walking and running at 2.0 ms -1, which is surprising given the difference reported by Lieberman et al. (2006). However, the forward pitch rate of the trunk following foot contact at 2 ms -1 was also lower in my results. Thus, mitigating force produced by the GMAX in order to stabilize the trunk in running at this speed would be lower here than in Lieberman et al. (2006). The lack of a significant difference in GMAX force production in this thesis suggests no functional difference between gaits for the GMAX when running at a 45

57 speed slower than is typical for urance runners (Carrier, 1984). Because urance running speeds are typically greater than 2.0 ms -1 (Carrier, 1984), the comparisons between GMAX activity in walking and running gaits are additionally meaningful when testing the ER Hypothesis at running speeds of 3.0 ms -1 and 4.0 ms -1. My thesis shows that mean amplitude of both igmax and sgmax are significantly lower in walking than in running at faster speeds. The significant kinematic differences associated with increasing speeds that were identified correspond with findings from previous research (Mann and Hagy, 1980; Nilsson et al., 1985; Novacheck, 1998; Kawabata et al., 2013; Bartlett et al., 2014). Total range of motion in lower limb joints increases as gait speed increases (Mann and Hagy, 1980). Thus, at lower duty factors, segment velocities increase (Biewener, 2003). Accordingly, speed effect differences are also apparent in EMG data. As speed increases so does stride frequency, while limb-substrate contact times decrease (Biewener, 2003; Nicola and Jewison, 2012). Forces are necessary to keep the body in motion. To compensate for the shorter contact times associated with greater speed, locomotor muscles must increase force amplitude (Biewener, 2003). This supports the conclusion of Bartlett et al. (2014) and other recent studies suggesting a main effect of speed over gait type (Gazom and Hof, 2007; Wall- Scheffler et al., 2010). While both walking and running gaits include a swing phase and a stance phase (Biewener, 2003; Farris and Sawicki, 2011; Nicola and Jewison, 2012), there are fundamental kinematic differences between walking and running (Novacheck, 1998; Biewener, 2003; Nicola and Jewison, 2012). Running gait lacks the double support phase of walking gait. In running, no more than one limb contacts the ground at any time. Also, running gait includes an aerial phase in which neither limb contacts the ground (Biewener, 2003; Nicola and Jewison, 2012). Thus, running gait carries low duty factors, large center of mass displacements, and 46

58 high angular velocities (Hamill and Knutzen, 2009). Furthermore, walking exploits pular energetics while running exploits elastic spring energetics (Biewener, 2003). Limb kinematics are sure to differ between a walking gait in which one or both limbs support the body against ground reaction forces and a running gait in which the center of mass falls abruptly from a flight phase to single limb support. The significant differences found between gait for all kinematic variables other than barefoot thigh velocity at foot contact and the difference between thigh velocity excursion can be attributed to range of motion differences that result from the presence or absence of an aerial phase. Timing of segment movement and range of motion often differ between walking and running (Novacheck, 1998; Lieberman et al., 2006). The observation that thigh velocity at barefoot contact does not statistically differ between walking and running at 2.0 ms -1, but does at shod contact may be attributed to the highly variable barefoot foot strike angle in the 2.0 ms -1 run. Barefoot strike at the slow running speed of 2.0 ms -1 was nearly bimodal; thirteen runners dorsiflexed (RFS) and eleven plantarflexed (FFS). In contrast, shod foot strike for slow running at 2.0 ms -1 was more uniform in that twenty subjects dorsiflexed (RFS) and just four plantarflexed (FFS). The current study design compared barefoot and shod because early Homo lacked footwear (Trinkaus and Shang, 2008). However, in barefoot running the strike pattern is highly variable in modern populations and most likely was variable during our distant evolutionary past. Investigation subdividing foot conditions by strike pattern would be beneficial to further test gait EMG differences and to deepen the understanding of trunk kinematic differences. Although the trunk is more flexed at foot contact in running than in walking, its overall angular excursion or range of motion is smaller. Despite the greater speed and higher impact force associated with running, the trunk swings less, and thus appears to be more stable in 47

59 running. In addition, the trunk motions vary between gaits yet there is no significant GMAX EMG difference. Thus, results do not support Hypothesis 2, and instead suggest that gait transition is not the primary factor influencing GMAX activity. This thesis research shows that GMAX force production increases with an increase in gait speed, and this occurs within walking and running gaits. Nonetheless, the higher EMG magnitude and greater trunk pitch demonstrated at ER speeds that exceed typical walking speeds does not falsify the evolutionary argument for robusticity in GMAX as introduced in the ER Hypothesis (Bramble and Lieberman, 2004). 6.4 GMAX Force Production Differs in Shod versus Barefoot Running (Hypothesis 3) I predicted that the amplitude of the EMG signal from the gluteus maximus muscle would be lower in barefoot running than in shod running (Hypothesis 3). Although running kinematics differed significantly, muscle force production did not. Collectively, the kinematic results depict a more upright orientation of the trunk at foot contact (3.0 ms -1 ), a larger range of overall motion in the trunk segment (all running speeds), and a greater pitch rate of the trunk at the ER speed of 4.0 ms -1 when runners are barefoot. From the latter finding, one might expect a significantly greater amplitude in GMAX activity as a means to mitigate angular displacement of the trunk. While it is clear from previous research that the GMAX can brake trunk pitch in running (Lieberman et al., 2006), the relatively low pitch rate recorded in this thesis for both shod and barefoot running (30-35 s -1 at 4.0 ms -1 ) may not have had a destabilizing effect on the trunk. For example, even at the slow running speed of 2.0 ms -1, Lieberman et al. (2006) recorded a mean trunk pitch rate of s -1, which is considerably higher than that observed in this thesis research. Also, given that the moment arm of GMAX is greatest at 0 flexion and least at 130 flexion (Lengsfeld et al., 1996), the upright trunk position at barefoot strike may confer greater mechanical advantage to the muscle than the 48

60 more flexed position at shod strike. If so, the muscle can deliver adequate counter force to brake forward trunk pitch without increasing the magnitude of contraction, which is higher at foot contact in barefoot running. This may explain why I found no difference in GMAX EMG despite the higher pitch rate of the trunk in barefoot running. An additional factor in trunk pitch is the resultant ground reaction force. Although the research laboratory was equipped with a force plate, its short track-way length did not accommodate the number of strides necessary to establish natural running form (e.g., pace and speed), Therefore, the GRFs captured during force plate running trials were not analyzed. Further questions regarding the role of the GMAX in ER running will require ground reaction force data of the kind that can be captured on an instrumented treadmill. Force data would allow for evaluation of external and internal moments used to determine type of muscle contraction occurring, providing insight into whether the GMAX is acting on the trunk or thigh. Such data would provide data evidence either supporting or rejecting the ER Hypothesis. 6.5 Gait Patterns One of the major contributions this thesis makes to our understanding of the role of the large human gluteus maximus in urance running is its novel profile of trunk segment kinematics in barefoot running. Given the evolutionary context of the ER Hypothesis (Bramble and Lieberman, 2004), studies conducted on barefoot runners are key. Furthermore, knowing how barefoot running kinematics differ from shod running kinematics allows for new interpretation of earlier shod running studies. Graphical visualization trunk kinematics in different gaits reveals fundamental patterns (Figure 6a-h). During walking, foot contact occurs before maximum trunk extension followed by maximum trunk flexion. Foot strike in walking occurs during the trunk s maximum posterior pitch. The thigh velocity is nearly zero at foot 49

61 contact in walking and the thigh angle has already reached maximum flexion increasing towards maximum extension. EMG amplitude for both the superior and inferior regions of the GMAX are at their maximum and midburst at this event (Figure 6a-b; 6e-f). This pattern is similar for shod walking and barefoot walking. The walking pattern is similar to 2.0 ms -1 running. Notably, running at 3.0 ms -1 and 4.0 ms -1 differs. At ER speeds, foot contact the trunk is already pitching forward and collapsing downward. The trunk continues in this direction with maximum pitch and flexion shortly after foot contact in running (Figure 6.c-d; 6.g-h). The timing of foot contact appears to occur around the same time in the gait cycle for thigh angle, thigh velocity and EMG bursts. It is important to note that the trunk angle has not only high intra-subject variability but also intra-trial variability (Figure 6.c-e; 6.g-h). The thigh angle appears to be more uniform in pattern, suggesting the trunk is less stable than the thigh segment in running gait. 50

62 51

63 52 h. BF 4.00 ms -1

64 6.6 Implications for Homo Evolution Among the many adaptations addressed in the ER Hypothesis is the evolution of the large human GMAX as a force mechanism to resolve the stability problem of rapid trunk pitch in long distance running (Bramble and Lieberman, 2004; Lieberman et al., 2006). By examining trunk kinematics and GMAX EMG in shod and barefoot running, my research informs earlier inferences made between modern human running and early Homo running. My results show that the human trunk in barefoot running is more upright, as was predicted in Hypothesis 1, compared to shod running. While it is reasonable to conclude that early Homo ran with a similarly upright trunk, my findings also demonstrate greater trunk pitching in barefoot running than in shod running, counter to the prediction of Hypothesis 1. The surprising statistical similarity between GMAX EMG in barefoot and shod running identified here may be explained by the modest pitch differences, and by the greater mechanical advantage of the more vertical trunk at foot contact in barefoot running (Lengsfeld et al., 1996). High mechanical advantage reduces muscle energy expiture and therefore may have further benefited early Homo when traveling at running speeds across long distances in the persistent hunt (Biewener, 2003). Gait speed is the primary determinant of GMAX force production in my study and was similarly important in the work of Gazam and Hof (2007), Wall-Scheffler et al. (2010), and Bartlett et al. (2014). Increase in trunk pitch and increase in EMG amplitude were greatest with increase in gait speed for both barefoot and shod conditions. Muscle fiber length and muscle cross-sectional area are factors in the economy of muscle lever force (Biewener, 2003). The cross-sectional area of the human GMAX is larger that that of living apes (Payne et al., 2006). Humans therefore reduce energy cost using GMAX muscles with larger cross-sectional areas and shorter fibers in generating higher forces (Biewener, 2003; 53

65 Payne et al., 2006). Although my findings suggest that speed is the main factor in GMAX EMG amplitude (not gait or foot condition), the proposed transition to long distance running in early Homo as argued by Bramble and Lieberman s ER Hypothesis (2004) remains a plausible selection pressure for the evolution of the robust GMAX. Muscle fibers of the superior portion of the human GMAX are predominantly Type I slow twitch fibers with high fatigue resistance and are well suited for urance tasks (McAndrew, 2006). Additionally, the greater muscle mechanical advantage of the slightly less flexed trunk noted here in barefoot running improves energetic economy by increasing force output with less contractile effort (Biewener, 2003). Modern hunter gathers have marginally higher daily energy expiture than expected for body mass (Leonard and Robertson, 1997) and routinely travel greater foraging distances than living apes (Marlowe, 2005; Pontzer and Wrangham, 2006). Thus, a robust GMAX muscle with a large moment arm and high percentage of slow twitch muscle fibers would be evolutionarily beneficial when traveling long distances at increased speeds. 6.7 Limitations and Future Research My goal in this thesis was to examine natural gait among varying foot conditions and to study possible evolutionary implications of barefoot urance running. However, a recent influx of research and minimal shoe marketing may have prompted a change in gait pattern among my subjects that was not entirely natural. The subject pool consisted of practiced runners who often join running groups or seek running advice; any coaching or advice could have possibly altered their normal running kinematics (Robbins and Hanna, 1987; Sache et al., 1999). The novelty of running without shoes on a mechanically driven substrate may have further affected subject gait patterns in unexpected ways even though subjects were given a warm up period. Greater trunk excursion may be due in part to the unfamiliar sensation of barefoot contact 54

66 on the treadmill deck, as this was a new experience for study subjects. Additionally, foot strike under barefoot conditions was audibly louder than under shod conditions. Such high noise level may have caused subjects to alter their foot strike angle and other segment angles to lessen the abrupt contact volume. A longitudinal study design allowing subjects an exted period in which to acclimate to barefoot running on a treadmill may shed more light on this effect. A larger sample size and more robust numbers could provide more insight and stronger statistical testing to determine whether differences and patterns hold for the multiple variables tested. Another limitation of this thesis research is its inability to determine onset of the EMG or any timing variables of the EMG. This was due to the high movement artifacts in the EMG signals. Statistically evaluating the timing of the GMAX EMGs would provide better insight into any differences between speed and gait. Due to the trunk s large mass, future work may benefit from redefining the trunk as a single solid segment to two segments allowing for upper and lower trunk rotations. The mean differences in trunk pitch between foot conditions in this thesis are modest, at most 8 s -1, which is consistent with Delgado et al. (2013) s lumbar range of motion differences. Lieberman et al. (2006) found a 75 s -1 increase in anterior trunk pitch rate with running compared to walking, along with a proportional increase in GMAX amplitude. Lieberman et al. (2014) placed a rate gyro on the superior trunk between the left and right scapulae. By capturing trunk movement data from the cranial margin of the trunk, the trunk pitch amplitude of Lieberman et al (2014) may not be fully comparable to the trunk pitch reported in this study. The craniocaudal position of an accelerometer placed on a lengthy segment such as the trunk is likely to affect the magnitude and pattern of acceleration data recorded (Cavagna et al., 1964), suggesting height can effect velocities as well. 55

67 7. Summary and Conclusions Overall differences between foot conditions (barefoot and shod, rearfoot and forefoot strike) differed as expected. However, the only universally significant difference between foot conditions was the foot angle at initial contact. Although the other variables held no consistency in their differences, their means suggest possible trs. The trunk was often less flexed in barefoot running than in shod running, supporting Hypothesis 1. Yet, the trunk in barefoot running had a greater forward pitch and range of motion following foot contact than in shod running, which was not expected. No significant difference in gluteus maximus muscle magnitude was detected between barefoot and shod running, providing no support for Hypothesis 3. Further research is needed to test the energetic costs of greater trunk pitch and greater trunk range of motion without increase in GMAX EMG. The lack of difference in EMG amplitude between walking and running at a single speed does not support Hypothesis 2, which was based on earlier work by Lieberman et al. (2006). However, the strong statistical difference in EMG amplitude with increase in gait speed is consistent with Bartlett et al. s (2014) conclusion that gait speed rather than gait type is the primary factor in GMAX trunk pitch mitigation. Future work including kinetic variables and joint moments is needed to determine the role of GMAX in running as it relates to motions of both the trunk and the thigh. Resolving which segment or segments the GMAX acts on during habitual locomotion and how the functional demands on the muscle change according to speed, gait, and foot condition will provide a more holistic understanding of the evolutionary origins of the unique human gluteus maximus. 56

68 Glossary of Commonly Used Abbreviations GMAX = gluteus maximus; sgmax = superior; igmax = inferior BF = barefoot FC = foot contact ER = urance running EMG = electromyography COM = center of mass GRFs = ground reaction forces; GRFv = vertical component of ground reaction force RFS = rearfoot strike MFS = midfoot strike FFS = forefoot strike 57

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75 Appix A. Recruitment flier 1 and screening questionnaire 2 Subject Recruitment Flier 1 64