Motor control of locomotor hindlimb posture in the American alligator (Alligator mississippiensis)

SUMMARY Crocodilians are unusual among quadrupedal tetrapods in their frequent use of a wide variety of hindlimb postures, ranging from sprawling to a more erect high walk. In this study, we use synchronized kinematic videos and electromyographic recordings to test how the activity patterns of hindlimb muscles in American alligators (Alligator mississippiensis Daudin) differ between sprawling and more upright postures. Previous force platform analyses suggested that upright posture in alligators would require greater activation by hindlimb extensors to counter increases in the flexor moments exerted about joints by the ground reaction force during upright stance. Consistent with these predictions, ankle extensors (gastrocnemius) and knee extensors (femorotibialis internus and iliotibialis 2) exhibit increases in signal intensity during the use of more upright stance. Bone loading data also predicted that activation patterns for hip adductors spanning the length of the femur would not differ between sprawling and more upright posture. Correspondingly, motor patterns of the adductor femoris were not altered as posture became more upright. However, the adductor puboischiofemoralis externus 3, which inserts far proximally on the femur, displays significant increases in burst intensity that could contribute to the greater femoral adduction that is integral to upright posture. In contrast to patterns in alligators, in mammals EMG burst intensity typically decreases during the use of upright posture. This difference in the motor control of limb posture between these taxa may be related to differences in the relative sizes of their feet. Alligator feet are large relative to the hindlimb and, as a result, the ground reaction force shifts farther from the limb joints during upright steps than in mammals, increasing flexor moments at joints and requiring alligator extensor muscles to exert greater forces to keep the limb in equilibrium. However, several alligator hindlimb muscles show no differences in motor pattern between sprawling and upright posture. The wide range of motor pattern modulations between different postures in alligators suggests considerable independence of neural control among the muscles of the alligator hindlimb.

[1]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[2]  S. Reilly Sprawling Locomotion in the Lizard Sceloporus clarkii: Speed Modulation of Motor Patterns in a Walking Trot , 1998, Brain, Behavior and Evolution.

[3]  F. Lacquaniti,et al.  Interactions between posture and locomotion: motor patterns in humans walking with bent posture versus erect posture. , 2000, Journal of neurophysiology.

[4]  J. Parrish The origin of crocodilian locomotion , 1987, Paleobiology.

[5]  B. Jayne,et al.  Comparative three-dimensional kinematics of the hindlimb for high-speed bipedal and quadrupedal locomotion of lizards , 1999, The Journal of experimental biology.

[6]  C. Pratt,et al.  Adaptive control for backward quadrupedal walking V. Mutable activation of bifunctional thigh muscles. , 1996, Journal of neurophysiology.

[7]  A. Romer Crocodilian pelvic muscles and their avian and reptilian homologues. Bulletin of the AMNH ; v. 48, article 15. , 1923 .

[8]  R. Blob Evolution of hindlimb posture in nonmammalian therapsids: biomechanical tests of paleontological hypotheses , 2001, Paleobiology.

[9]  S. Reilly,et al.  Locomotion in alligator mississippiensis: kinematic effects of speed and posture and their relevance to the sprawling-to-erect paradigm , 1998, The Journal of experimental biology.

[10]  J L Smith,et al.  Forms of forward quadrupedal locomotion. I. A comparison of posture, hindlimb kinematics, and motor patterns for normal and crouched walking. , 1996, Journal of neurophysiology.

[11]  A. Bekoff,et al.  Patterns of muscle activity during different behaviors in chicks: implications for neural control , 1996, Journal of Comparative Physiology A.

[12]  P. Thompson Electromyography for Experimentalists , 1987 .

[13]  S. Gatesy Neuromuscular diversity in archosaur deep dorsal thigh muscles. , 1994, Brain, behavior and evolution.

[14]  A. Biewener,et al.  Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). , 2001, The Journal of experimental biology.

[15]  A. Biewener Scaling body support in mammals: limb posture and muscle mechanics. , 1989, Science.

[16]  J. Altman,et al.  Swimming in the rat: Analysis of locomotor performance in comparison to stepping , 2004, Experimental Brain Research.

[17]  S. Reilly,et al.  Sprawling locomotion in the lizard Sceloporus clarkii: quantitative kinematics of a walking trot , 1997, The Journal of experimental biology.

[18]  P. Leyhausen,et al.  Cat behaviour. The predatory and social behaviour of domestic and wild cats. , 1979 .

[19]  J. Halbertsma,et al.  Changes in leg movements and muscle activity with speed of locomotion and mode of progression in humans. , 1985, Acta physiologica Scandinavica.

[20]  S. Reilly,et al.  Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking , 1997 .

[21]  D. Brinkman The hind limb step cycle of Caiman sclerops and the mechanics of the crocodile tarsus and metatarsus , 1980 .

[22]  G. Gillis,et al.  How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[23]  A. Biewener Biomechanics of mammalian terrestrial locomotion. , 1990, Science.

[24]  J. Coast Handbook of Physiology. Section 12. Exercise: Regulation and Integration of Multiple Systems , 1997 .

[25]  F. Seebacher,et al.  Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis) , 2003, Journal of Experimental Biology.

[26]  G. Loeb,et al.  Electromyography for Experimentalists , 1986 .

[27]  A. Biewener,et al.  In vivo locomotor strain in the hindlimb bones of alligator mississippiensis and iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture , 1999, The Journal of experimental biology.

[28]  J. Smith,et al.  Adaptive control for backward quadrupedal walking. II. Hindlimb muscle synergies. , 1990, Journal of neurophysiology.

[29]  S. Gatesy Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades , 1991 .

[30]  W. Rymer,et al.  Characteristics of synergic relations during isometric contractions of human elbow muscles. , 1986, Journal of neurophysiology.

[31]  Robert T. Barker DINOSAUR PHYSIOLOGY AND THE ORIGIN OF MAMMALS , 1971, Evolution; international journal of organic evolution.

[32]  William K. Gregory,et al.  NOTES ON THE PRINCIPLES OF QUADRUPEDAL LOCOMOTION AND ON THE MECHANISM OF HE LIMBS IN HOOFED ANIMALS , 1912 .

[33]  S. Gatesy,et al.  An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion , 1997, Journal of morphology.

[34]  R. Gregor,et al.  Adaptive control for backward quadrupedal walking. IV. Hindlimb kinetics during stance and swing. , 1993, Journal of neurophysiology.

[35]  S. Reilly Quantitative electromyography and muscle function of the hind limb during quadrupedal running in the lizard Sceloporus clarki , 2022 .