Interlimb Coordination

Neural, Dynamical, and Cognitive Constraints

Stephan P. Swinnen, Jean Massion, Herbert Heuer, P. Casaer

• Publisher: Academic Press
• Year: 2013
• Print ISBN: 9780126792706
• eBook ISBN: 9781483289243
• Topic: Psychology
• Subtopic: Cognitive Psychology & Cognition
• Index: Psychology

This comprehensive edited treatise discusses the neurological, physiological, and cognitive aspects of interlimb coordination. It is unique in promoting a multidisciplinary perspective through introductory chapter contributions from experts in the neurosciences, experimental and developmental psychology, and kinesiology. Beginning with chapters defining the neural basis of interlimb coordination in animals, the book progresses toward an understanding of human locomotor control and coordination and the underlying brain structures and nerves that make such control possible. Section two focuses on the dynamics of interlimb coordination and the physics of movement. The final section presents information on how practice and experience affect coordination, including general skill acquisition, learning to walk, and the process involved in rhythmic tapping.

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Topics on Interlimb Coordination

Stephan P. Swinnen, Laboratorium Motorische Controle, Departement Kinantropologie, Katholieke Universiteit Leuven, Leuven, Belgium

Jean Massion, Laboratoire de Neurosciences Fonctionelles, Centre National de la Recherche Scientifique, Marseille, France

H. Heuer, Institut für Arbeitsphysiologie, Universität Dortmund, Dortmund, Germany

Publisher Summary

This chapter provides an overview of an elementary framework of the field of interlimb coordination. Humans are capable of coordinating various limbs and body parts with each other—for example, the left and right hands or thumbs, the hand and foot, and the head and arm. One of the most intensively studied examples of interlimb coordination in the field of neuroscience is animal and human locomotion. The neural substrate underlying limb coordination is structured in such a way that flexibility and differentiated activity is possible whenever required. Afferent information plays a crucial role in interlimb coordination, and it is at the basis of the phase-dependent modulation of patterns of muscle activity.

I Introduction

II Exploring the Neural Basis of Interlimb Coordination

A The Neural Control of Locomotion

B The Neural Control of Posture

C Coordination of Head, Body, and Limbs

D The Neural Control of Goal-Directed Arm Movements

E Bimanual Coupling and Decoupling: Central and Peripheral Contributions

III In Search of the Equations of Motion Underlying Interlimb Coordination: Interlimb Dynamics

IV Modulation of Coordination Patterns through Practice and Experience

A Development of Coordination Patterns

B Acquisition of Coordination Patterns

V Conclusion

References

I Introduction

Humans are capable of coordinating various limbs and body parts with each other, for example, the left and right hands or thumbs, the hand and foot, and the head and arm. A remarkable spatiotemporal coordination is evident in spite of the large differences in inertial characteristics of the effectors involved. This observation suggests the existence of some basic coordination principles that apply across widely different cooperative ensembles. Underlying this well-organized global behavior is the coordination of subcomponents at various levels of the movement apparatus: intrajoint, intralimb, and interlimb. At the level of the individual joint, coordination between muscles acting on a common joint is required, such as the interplay between agonists and antagonists. Within a limb, the various joints and muscles, acting on one or more of these joints, must be properly organized to function efficiently. Finally, interlimb coordination is necessary to perform the most essential animal functions like walking, swimming, and feeding.

Whereas particular expressions of interlimb coordination such as locomotion have been investigated intensively in the neurosciences during the past 30 years, the interest in coordination within the behavioral sciences is relatively recent. Due to the development of new movement registration technologies, increased computational power, and the search for new links with the neurosciences and biophysics, the way has been made free for the study of more complex motor behaviors. This is an important development, since the capability to coordinate our limbs is at the heart of everyday life.

Two scientists, who were already actively involved in interlimb coordination research more than half a century ago, can be considered pioneers in this field. First, we owe a great deal to the Russian physiologist and movement specialist Bernstein (1967) who was particularly interested in studying complex motor acts. He was mainly struck by the observation that the movement apparatus, with such a tremendous degree of multilayered complexity, can accomplish goal-directed behavior so effortlessly. This came to be known as the degrees-of-freedom problem. Second, the German behavioral physiologist Von Hoist collected miles of data on the coordination of fin movements in decapitated fish (Labrus). He divided the observed coordination patterns into two major categories: absolute and relative coordination. Absolute coordination is characterized by the maintenance of a fixed-phase relation and by frequency synchronization of the fin movements. Relative coordination refers to a larger group of coordination patterns characterized by less stringent coupling modes, that is, the component activities are neither completely independent of one another nor linked in a fixed mutual relationship. Whereas this distinction is theoretically relevant, Von Hoist remarked that both types are often observed intermittently in fish preparations. In addition, he derived two basic principles that pertained to these coordination modes. On the one hand, he observed a tendency for each fin pattern to maintain its own frequency, referred to as the maintenance tendency (Beharrungstendenz). On the other hand, a tendency for one fin pattern to impose its inherent frequency on the other fin was often evident. This form of cooperation or (mutual) attraction of the fin movements was referred to as the magnet effect (Magnet-effect). The latter effect was often associated with the superposition effect that pertains to attraction between rhythmic units in the amplitude domain.

Von Hoist argued that the magnet effect and the maintenance tendency are in mutual opposition: “If the former predominates, then there is continuous agreement in frequency under absolute coordination; if the latter predominates, there is relative coordination—the frequencies of the rhythms differ, and the dependent rhythm, under the magnet effect of the dominant rhythm, exhibits periodicity whose form is determined by the reciprocal frequency relationship and whose extent is governed by the intensity of the magnet effect” (Von Hoist, 1973, p. 63).

Even though these principles were extracted from research on fin movements, they currently form a major source of inspiration for the study of human coordination (Kelso, Chapter 15, this volume; Turvey & Schmidt, Chapter 14, this volume). Today, many research laboratories across the world investigate these phenomena in a variety of different contexts. Others are more concerned with the study of discrete bimanual tasks in which the limbs assume differentiated roles to accomplish goal-directed behavior (Fagard, Chapter 21, this volume; Peters, Chapter 27, this volume; Walter & Swinnen, Chapter 23, this volume).

The present book consists of a series of introductory chapters, representing various levels of research and subdivisions of science that currently address interlimb coordination, for example, the neurosciences, the behavioral sciences, kinesiology, biomechanics, and dynamics. Even though each of these fields of science is characterized by a unique approach to the study of interlimb coordination, using its own techniques to acquire knowledge, all strive for a better understanding of how the human control system manages to organize the cooperation among the limbs. Neuroscientific approaches focus on the neuronal networks and pathways underlying rhythmic and discrete coordination patterns, in particular locomotion and bimanual coordination. Some chapter contributions concentrate on the identification of the locus of the central pattern generator underlying locomotion, whereas others are mainly concerned with the reflex modulation of these patterns as a result of sensory information. Scientists advocating a dynamical approach seek to uncover the equations of motion that govern movement coordination. They attempt to identify the dynamic states at which moving animals converge when provided enough time to settle down. Finally, some scientists are mainly concerned with a better understanding of goal-directed motor behavior and the changes in coordination that occur as a result of development and learning, that is, the modulation or overcoming of preexisting/preferred coordination modes with the goal of expanding the behavioral repertoire. Those who have a strong link with cognitive psychology direct their attention to a better understanding of the nature of the central representation underlying complex coordination and the movement features it comprises.

II Exploring the Neural Basis of Interlimb Coordination

A The Neural Control of Locomotion

One of the most intensively studied examples of interlimb coordination in the field of neuroscience is animal and human locomotion. Since Sherrington, three areas of interest have dominated experimental studies on locomotion: (1) the role of reflexes in locomotion; (2) the capability of the spinal cord to generate intrinsic rhythms; and (3) the control of the spinal cord by higher centers. At one time or another, attention has mainly been directed at one of these mechanisms for motor control. More recent studies have concentrated on the synthesis of these mechanisms into a general framework for nervous control (Shepherd, 1988). This also typifies the chapters on locomotion in this volume. The contributions refer to the study of locomotion in invertebrates such as the crayfish (Cattaert et al., Chapter 3) and higher vertebrates, including those using a quadrupedal gait, such as the cat (Kato, Chapter 4), and a bipedal gait, such as the human (Brooke et al., Chapter 6; Duysens & Tax, Chapter 5).

Pioneering work on locomotion was conducted by Grillner (1975, 1981) and Shik and co-workers (Shik, Severin, & Orlovsky, 1966), who spent considerable efforts in demonstrating the existence of a relatively autonomous neural network, called the central pattern generator (CPG) (see also Cattaert et al., Chapter 3, this volume; Duysens & Tax, Chapter 5, this volume). This confirmed earlier ideas put forward by T. Graham Brown in 1911, who demonstrated that the rhythmic alternation between flexion and extension is not reflex in origin but is generated by neurons located in the spinal cord. CPGs have been demonstrated in most locomotory networks found in invertebrates and vertebrates. The rhythm production generally results from both membrane properties of neurons and particular network connections.

Even though these patterns of interlimb coordination can be observed in the absence of afferent information, this should not be taken to imply that afference plays a minor role in normal locomotion. Brown (1911) was well aware of this when he suggested that afferent input was probably important in grading the component movements to the specific environmental contingencies. Since locomotion is a highly automated type of motor behavior, it is not surprising that interlimb reflexes have evolved to support the coordination of the limb movements during gait and to modulate the basic patterns during unexpected perturbations (Duysens & Tax, Chapter 5, this volume).

In Chapter 4 of this volume, Kato reviews his experimenal contributions of the past 15 years, which deal with locomotor coordination after horizontal and longitudinal separation of the spinal cord in spinal intact cats and spinal lesioned cats. Lateral hemisection of the spinal cord was carried out in order to disrupt descending and ascending long tracts unilaterally. These hemisected preparations do not show any differences in step length or in step time when compared with normal control cats. However, they do demonstrate evidence for less accurate foot placement responses when walking on grid surfaces. According to Kato, this suggests that interlimb reflex pathways serve to coordinate the spatial aspects of locomotion in quadrupedal gait. On the other hand, spinal transsection or double hemisection results in a disruption of the phase relations between the fore- and hindlimbs, and this points to the importance of descending signals from brainstem locomotor centers for achieving coordination among the limbs.

Some chapters specifically deal with the reflex modulation of locomotory activities. Cattaert and co-workers have investigated two locomotor systems in the crayfish (Crustacea): (1) swimming, accomplished by four pairs of paddles; and (2) walking, by means of four to five pairs of thoracic legs. They show some nice examples of sensory-motor interactions, which are analyzed at the cellular level. A comparison of both systems reveals the existence of similarities between their central commands. But, there exist essential differences as well, pertaining to the presence or absence of contact with rigid substra...

Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• Contributors
• Preface
• Acknowledgments
• Chapter 1: Topics on Interlimb Coordination
• Part I: The Neural Basis of Interlimb Coordination
• Part II: The Dynamics of Interlimb Coordination
• Part III: Modulation of Coordination Patterns through Practice and Experience
• Index