Kinematic and EMG determinants in quadrupedal locomotion of a non-human primate (Rhesus).

We hypothesized that the activation patterns of flexor and extensor muscles and the resulting kinematics of the forelimbs and hindlimbs during locomotion in the Rhesus would have unique characteristics relative to other quadrupedal mammals. Adaptations of limb movements and in motor pool recruitment patterns in accommodating a range of treadmill speeds similar to other terrestrial animals in both the hindlimb and forelimb were observed. Flexor and extensor motor neurons from motor pools in the lumbar segments, however, were more highly coordinated than in the cervical segments. Unlike the lateral sequence characterizing subprimate quadrupedal locomotion, non-human primates use diagonal coordination between the hindlimbs and forelimbs, similar to that observed in humans between the legs and arms. Although there was a high level of coordination between hind- and forelimb locomotion kinematics, limb-specific neural control strategies were evident in the intersegmental coordination patterns and limb endpoint trajectories. Based on limb kinematics and muscle recruitment patterns, it appears that the hindlimbs, and notably the distal extremities, contribute more to body propulsion than the forelimbs. Furthermore, we found adaptive changes in the recruitment patterns of distal muscles in the hind- and forelimb with increased treadmill speed that likely correlate with the anatomical and functional evolution of hand and foot digits in monkeys. Changes in the properties of both the spinal and supraspinal circuitry related to stepping, probably account for the peculiarities in the kinematic and EMG properties during non-human primate locomotion. We suggest that such adaptive changes may have facilitated evolution toward bipedal locomotion.

[1]  F. Lacquaniti,et al.  Kinematic control of walking. , 2002, Archives italiennes de biologie.

[2]  J W Fanton,et al.  Effects of spaceflight on rhesus quadrupedal locomotion after return to 1G. , 1999, Journal of neurophysiology.

[3]  P. Aerts,et al.  Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus). , 2002, American journal of physical anthropology.

[4]  S Mori,et al.  Quadrupedal locomotor movements in monkeys (M. Fuscata) on a treadmill: kinematic analyses. , 1996, Neuroreport.

[5]  P. Viviani,et al.  The law relating the kinematic and figural aspects of drawing movements. , 1983, Acta psychologica.

[6]  S. Rossignol,et al.  Determinants of locomotor recovery after spinal injury in the cat. , 2004, Progress in brain research.

[7]  F. Lacquaniti,et al.  Two-thirds power law in human locomotion: role of ground contact forces , 2002, Neuroreport.

[8]  M. Tuszynski,et al.  Spontaneous and augmented growth of axons in the primate spinal cord: Effects of local injury and nerve growth factor‐secreting cell grafts , 2002, The Journal of comparative neurology.

[9]  J. Vilensky Locomotor behavior and control in human and non-human primates: Comparisons with cats and dogs , 1987, Neuroscience & Biobehavioral Reviews.

[10]  V. Dietz,et al.  Arm to leg coordination in humans during walking, creeping and swimming activities , 2001, Experimental Brain Research.

[11]  J. Vilensky,et al.  Stepping in Nonhuman Primates with a Complete Spinal Cord Transection: Old and New Data, and Implications for Humans , 1998, Annals of the New York Academy of Sciences.

[12]  V. Reggie Edgerton,et al.  Electromyographic activity of cat hindlimb flexors and extensors during locomotion at varying speeds and inclines , 1989, Brain Research.

[13]  J. Vilensky Primate quadrupedalism: how and why does it differ from that of typical quadrupeds? , 1989, Brain, behavior and evolution.

[14]  R. Poppele,et al.  Kinematic analysis of cat hindlimb stepping. , 1995, Journal of neurophysiology.

[15]  Van de Crommert HW,et al.  Neural control of locomotion; The central pattern generator from cats to humans. , 1998, Gait & posture.

[16]  E. Eidelberg,et al.  Recovery of Locomotion in Monkeys With Spinal Cord Lesions. , 1992, Journal of motor behavior.

[17]  J. Nielsen How we Walk: Central Control of Muscle Activity during Human Walking , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[18]  E. Zehr,et al.  Regulation of Arm and Leg Movement during Human Locomotion , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[19]  Trevor Drew,et al.  A kinematic and kinetic analysis of locomotion during voluntary gait modification in the cat , 2004, Experimental Brain Research.

[20]  M. Tuszynski,et al.  Neurotrophic factors, cellular bridges and gene therapy for spinal cord injury , 2001, The Journal of physiology.

[21]  D. Dunbar,et al.  Development of Posture and Locomotion in Free-ranging Primates , 1998, Neuroscience & Biobehavioral Reviews.

[22]  A. English,et al.  An electromyographic analysis of compartments in cat lateral gastrocnemius muscle during unrestrained locomotion. , 1984, Journal of neurophysiology.

[23]  S. Larson,et al.  Compliant walking in primates: elbow and knee yield in primates compared to other mammals. , 2004, American journal of physical anthropology.

[24]  S. Harkema,et al.  Retraining the injured spinal cord , 2001, The Journal of physiology.

[25]  J. Manter The Dynamics Of Quadrupedal Walking , 1938 .

[26]  G. Courtine,et al.  Human walking along a curved path. II. Gait features and EMG patterns , 2003, The European journal of neuroscience.

[27]  F. Lacquaniti,et al.  Motor Patterns in Walking. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[28]  S. Mori,et al.  Bipedal locomotion by the normally quadrupedal Japanese monkey, M. Fuscata: strategies for obstacle clearance and recovery from stumbling. , 2001, Acta physiologica et pharmacologica Bulgarica.

[29]  M. Hildebrand Symmetrical gaits of primates , 1967 .

[30]  F. Lacquaniti,et al.  Development of pendulum mechanism and kinematic coordination from the first unsupported steps in toddlers , 2004, Journal of Experimental Biology.

[31]  T. Drew Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. , 1993, Journal of neurophysiology.

[32]  V. Edgerton,et al.  Plasticity of the spinal neural circuitry after injury. , 2004, Annual review of neuroscience.

[33]  S. Rossignol,et al.  On the initiation of the swing phase of locomotion in chronic spinal cats , 1978, Brain Research.

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

[35]  C. M. Bastiaanse,et al.  Neuronal coordination of arm and leg movements during human locomotion , 2001, The European journal of neuroscience.

[36]  N. Ogihara,et al.  Do highly trained monkeys walk like humans? A kinematic study of bipedal locomotion in bipedally trained Japanese macaques. , 2004, Journal of human evolution.

[37]  R. E. Burke,et al.  Peripheral and central control of flexor digitorum longus and flexor hallucis longus motoneurons: The synaptic basis of functional diversity , 2004, Experimental Brain Research.

[38]  Shik Ml,et al.  Control of walking and running by means of electric stimulation of the midbrain , 1966 .

[39]  V R Edgerton,et al.  EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming. , 1991, Journal of applied physiology.

[40]  S. Miller,et al.  Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats , 1975, Brain Research.

[41]  V. Edgerton,et al.  Paralysis recovery in humans and model systems , 2002, Current Opinion in Neurobiology.

[42]  P. Cheney,et al.  Properties of primary motor cortex output to forelimb muscles in rhesus macaques. , 2004, Journal of neurophysiology.

[43]  M. Taussig The Nervous System , 1991 .

[44]  K. Pearson,et al.  Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats , 1980, Brain Research.

[45]  T. Drew,et al.  Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat , 2002, Brain Research Reviews.

[46]  Daniel Schmitt,et al.  Insights into the evolution of human bipedalism from experimental studies of humans and other primates , 2003, Journal of Experimental Biology.

[47]  Douglas G. Stuart,et al.  Neural Control of Locomotion , 1976, Advances in Behavioral Biology.

[48]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.

[49]  J W Fanton,et al.  Circadian force and EMG activity in hindlimb muscles of rhesus monkeys. , 2001, Journal of neurophysiology.

[50]  Richard R Neptune,et al.  Biomechanics and muscle coordination of human walking. Part I: introduction to concepts, power transfer, dynamics and simulations. , 2002, Gait & posture.

[51]  Daniel M. Wolpert,et al.  Making smooth moves , 2022 .

[52]  P. Nathan,et al.  Vestibulospinal, reticulospinal and descending propriospinal nerve fibres in man. , 1996, Brain : a journal of neurology.

[53]  T. Drew,et al.  Effects of red nucleus microstimulation on the locomotor pattern and timing in the intact cat: a comparison with the motor cortex. , 1999, Journal of neurophysiology.

[54]  John G. Fleagle,et al.  Primate locomotion : recent advances , 1998 .

[55]  J. Nielsen,et al.  Pharmacologically evoked fictive motor patterns in the acutely spinalized marmoset monkey (Callithrix jacchus) , 1998, Experimental Brain Research.

[56]  G Schöner,et al.  A synergetic theory of quadrupedal gaits and gait transitions. , 1990, Journal of theoretical biology.

[57]  S. M. Morton,et al.  Cerebellar Control of Balance and Locomotion , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[58]  M. Cartmill,et al.  Support polygons and symmetrical gaits in mammals , 2002 .

[59]  Stepping in Humans with Complete Spinal Cord Transection: A Phylogenetic Evaluation , 1997 .

[60]  T. Kimura Bipedal and quadrupedal walking of primates : Comparative dynamics , 1985 .

[61]  Elzbieta Jankowska,et al.  Neuronal Basis of Crossed Actions from the Reticular Formation on Feline Hindlimb Motoneurons , 2003, The Journal of Neuroscience.

[62]  Jens Bo Nielsen,et al.  Motoneuronal drive during human walking , 2002, Brain Research Reviews.

[63]  S. Larson Unique Aspects of Quadrupedal Locomotion in Nonhuman Primates , 1998 .

[64]  M. E. Morbeck Primate morphophysiology, locomotor analyses and human bipedalism , 1986, International Journal of Primatology.

[65]  J. Duysens,et al.  Neural control of locomotion; Part 1: The central pattern generator from cats to humans , 1998 .

[66]  Masahiro Mori,et al.  Reactive and anticipatory control of posture and bipedal locomotion in a nonhuman primate. , 2004, Progress in brain research.

[67]  C. Capaday The special nature of human walking and its neural control , 2002, Trends in Neurosciences.

[68]  F. Lacquaniti,et al.  Kinematic coordination in human gait: relation to mechanical energy cost. , 1998, Journal of neurophysiology.

[69]  H. Kuypers,et al.  Cells of origin of propriospinal fibers and of fibers ascending to supraspinal levels. A HRP study in cat and rhesus monkey , 1978, Brain Research.

[70]  S. Grillner,et al.  Visuomotor coordination in reaching and locomotion. , 1989, Science.

[71]  J. Halbertsma,et al.  Basic Programs for the Phasing of Flexion and Extension Movements of the Limbs during Locomotion , 1976 .

[72]  V. Reggie Edgerton,et al.  Extensor- and flexor-like modulation within motor pools of the rat hindlimb during treadmill locomotion and swimming , 1994, Brain Research.

[73]  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.

[74]  Kuypers Hg The motor system and the capacity to execute highly fractionated distal extremity movements. , 1978 .

[75]  Keir G Pearson,et al.  Generating the walking gait: role of sensory feedback. , 2004, Progress in brain research.

[76]  T. Drew,et al.  Cortical and brainstem control of locomotion. , 2004, Progress in brain research.

[77]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999, Journal of neurophysiology.

[78]  N. A. Borghese,et al.  Kinematic determinants of human locomotion. , 1996, The Journal of physiology.

[79]  P. Aerts,et al.  Locomotion in bonobos (Pan paniscus): differences and similarities between bipedal and quadrupedal terrestrial walking, and a comparison with other locomotor modes , 2004, Journal of anatomy.

[80]  Ole Kiehn,et al.  Firing Properties of Identified Interneuron Populations in the Mammalian Hindlimb Central Pattern Generator , 2002, The Journal of Neuroscience.

[81]  A. English,et al.  An electromyographic analysis of forelimb muscles during overground stepping in the cat. , 1978, The Journal of experimental biology.

[82]  Marco Schieppati,et al.  Tuning of a basic coordination pattern constructs straight-ahead and curved walking in humans. , 2004, Journal of neurophysiology.

[83]  E. Taskinen Transmission of substituent effects through the unsaturated system in ring-substituted α-methoxystyrenes and related compounds , 1978 .

[84]  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.

[85]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. , 1968, Brain : a journal of neurology.

[86]  S. Larson,et al.  Uniqueness of primate forelimb posture during quadrupedal locomotion. , 2000, American journal of physical anthropology.

[87]  Richard R Neptune,et al.  Biomechanics and muscle coordination of human walking: part II: lessons from dynamical simulations and clinical implications. , 2003, Gait & posture.

[88]  Daniel Schmitt,et al.  Compliant walking in primates , 1999 .

[89]  V R Edgerton,et al.  Architectural and fiber type distribution properties of selected rhesus leg muscles: feasibility of multiple independent biopsies. , 1991, Acta anatomica.

[90]  J. Vilensky Gait characteristics of two macaques, with emphasis on relationships with speed. , 1983, American journal of physical anthropology.

[91]  Michael J. O'Donovan,et al.  Actions of FDL and FHL muscles in intact cats: functional dissociation between anatomical synergists. , 1982, Journal of neurophysiology.

[92]  F E Zajac,et al.  Contralateral movement and extensor force generation alter flexion phase muscle coordination in pedaling. , 2000, Journal of neurophysiology.

[93]  E. Eidelberg,et al.  Locomotor control in macaque monkeys. , 1981, Brain : a journal of neurology.

[94]  D. Armstrong The supraspinal control of mammalian locomotion. , 1988, The Journal of physiology.

[95]  G E Goslow,et al.  The cat step cycle: Electromyographic patterns for hindlimb muscles during posture and unrestrained locomotion , 1978, Journal of morphology.

[96]  L. Rowell,et al.  Exercise : regulation and integration of multiple systems , 1996 .

[97]  O. Kiehn,et al.  Functional Identification of Interneurons Responsible for Left-Right Coordination of Hindlimbs in Mammals , 2003, Neuron.

[98]  T. Drew,et al.  Effects of bilateral lesions of the dorsolateral funiculi and dorsal columns at the level of the low thoracic spinal cord on the control of locomotion in the adult cat. I. Treadmill walking. , 1996, Journal of neurophysiology.