clinical disorders oforthoteb.com/upload/56122720318886269411605002422clinical... · 2016-07-29 ·...

Clinical Disorders of Balance, Posture and Gait

This page intentionally left blank

Edited byAdolfo M. Bronstein MD PhD FRCPProfessor of Neuro-Otology and Honorary Consultant NeurologistImperial College of Science and Technology, Charing Cross Hospital, London, UK

Thomas Brandt MD FRCPProfessor, Department of NeurologyLudwig-Maximilians University, Munich, Germany

Marjorie H. Woollacott PhDProfessor, Department of Exercise and Movement ScienceInstitute of Neuroscience, University of Oregon, Eugene,Oregon, USA

and

John G. Nutt MDProfessor, Departments of Neurology and Physiology & PharmacologyOregon Health Sciences University, Portland, Oregon, USA

A member of the Hodder Headline GroupLONDON

Clinical Disorders of Balance, Posture and GaitSecond edition

First published in Great Britain in 1996 by Arnold Reprinted in 1998This second edition published in 2004 by Arnold, a member of the Hodder Headline Group, 338 Euston Road, London NW1 3BH

http://www.arnoldpublishers.comDistributed in the United States of America byOxford University Press Inc.,198 Madison Avenue, New York, NY10016Oxford is a registered trademark of Oxford University Press

© 2004 Arnold

All rights reserved. No part of this publication may be reproduced ortransmitted in any form or by any means, electronically or mechanically,including photocopying, recording or any information storage or retrievalsystem, without either prior permission in writing from the publisher or alicence permitting restricted copying. In the United Kingdom such licencesare issued by the Copyright Licensing Agency: 90 Tottenham Court Road,London W1T 4LP.

Whilst the advice and information in this book are believed to be true andaccurate at the date of going to press, neither the authors nor the publishercan accept any legal responsibility or liability for any errors or omissionsthat may be made. In particular (but without limiting the generality of the preceding disclaimer) every effort has been made to check drug dosages;however, it is still possible that errors have been missed. Furthermore, dosage schedules are constantly being revised and new side-effectsrecognized. For these reasons the reader is strongly urged to consult the drug companies’ printed instructions before administering any of the drugsrecommended in this book.

British Library Cataloguing in Publication DataA catalogue record for this book is available from the British Library

Library of Congress Cataloging-in-Publication DataA catalog record for this book is available from the Library of Congress

ISBN 0 340 80657 5

1 2 3 4 5 6 7 8 9 10

Commissioning Editor: Joanna KosterDevelopment Editor: Sarah BurrowsProject Editor: Wendy RookeProduction Controller: Deborah SmithCover Design: Lee-May Lim

Typeset in 10/12 pt Minion by Phoenix Photosetting, Chatham, KentPrinted and bound in the UK by Butler & Tanner Ltd, Frome, Somerset

What do you think about this book? Or any other Arnold title?Please send your comments to [email protected]

http://www.arnoldpublishers.com

Contents

List of contributors vii

Preface to the second edition ix

Preface to the first edition xi

1. Posture and equilibrium 1Jean Massion and Marjorie H. Woollacott

2. Adaptive human locomotion: influence of neural, biological and mechanical factors on control mechanisms 20Aftab E. Patla

3. Development of balance and gait control 39Marjorie H. Woollacott, Christine Assaiante and Bernard Amblard

4. Classification of balance and gait disorders 63John G. Nutt and Fay B. Horak

5. Orthopedic assessment of gait disorders 74John H. Patrick and Louw van Niekerk

6. Clinical neurological assessment of balance and gait disorders 93Philip D. Thompson

7. Neuro-otological assessment in the patient with balance and gait disorder 99Adolfo M. Bronstein, Michael A. Gresty and Peter Rudge

8. Objective assessment of posture and gait 130Kenton R. Kaufman

9. Postural imbalance in peripheral and central vestibular disorders 146Thomas Brandt and Marianne Dieterich

10. Cerebellar gait and sensory ataxia 163Lewis Sudarsky

11. Gait and balance in basal ganglia disorders 173Bastiaan R. Bloem and Kailash P. Bhatia

12. Spastic movement disorders 207Volker Dietz

13. Frontal and higher level gait disorders 216Philip D. Thompson and John G. Nutt

14. Cerebrovascular disease and hydrocephalus 222José Masdeu

Clinical Disorders of Balance and Gait

Assessment of Balance and Gait Disorders

Normal and Developmental Aspects of Balance and Gait

15. Psychiatric aspects of dizziness and imbalance 245Rolf G. Jacob, Thomas Brandt and Joseph M. Furman

16. Syncopal falls, drop attacks and their mimics 286Bastiaan R. Bloem, Sebastiaan Overeem and J. Gert van Dijk

17. Rehabilitation of balance disorders in the patient with vestibular pathology 317Marousa Pavlou, Anne Shumway-Cook, Fay B. Horak, Lucy Yardley and Adolfo M. Bronstein

18. Neurological rehabilitation of gait and balance disorders 344Karl-Heinz Mauritz, Stefan Hesse and Cordula Werner

19. Psychosocial aspects of disorders affecting balance and gait 360Lucy Yardley, Marjan Jahanshahi and Richard S. Hallam

20. Balance control in older adults 385Pei-Fang Tang and Marjorie H. Woollacott

21. Falls and gait disorders in the elderly – principles of rehabilitation 404Peter Overstall

22. Syncope-related falls in the older person 422Rose Anne Kenny and Lynne Armstrong

Index 439

The Problem of Gait and Falls in the Elderly

Rehabilitation of Balance and Gait Disorders

vi Contents

Contributors

Bernard AmblardInstitute of Physiological and Cognitive Neurosciences (INPC),National Center of Scientific Research (CNRS), Marseille, France

Lynne ArmstrongConsultant in Elderly Care, Craigavon Area Hospital, Craigavon,Northern Ireland, UK

Christine AssaianteInstitute of Physiological and Cognitive Neurosciences (INPC),National Center of Scientific Research (CNRS), Marseille, France

Kailash Bhatia MD FRCPUniversity Department of Clinical Neurology, Institute ofNeurology and National Hospital for Neurology, London, UK

Bastiaan R. Bloem MD PhDAssistant Professor of Neurology, Department of Neurology,University Medical Centre St Radboud, Nijmegen, TheNetherlands

Thomas Brandt MD FRCPProfessor, Department of Neurology, Ludwig-Maximilians-Universität München, Klinikum Grosshadern, Munich, Germany

Adolfo M. Bronstein MD PhD FRCPAcademic Department of Neuro-Otology, Division ofNeuroscience & Psychological Medicine, Imperial College ofScience, Technology and Medicine, Faculty of Medicine,Charing Cross Hospital, London, UK

Marianne Dieterich MDProfessor of Neurology, Department of Neurology, Johannes-Gutenberg University, Mainz, Germany

V. Dietz MD FRCPParaplegic Centre, University Hospital Balgrist, Zurich,Switzerland

J. Gert van Dijk MD PhDDepartment of Neurology and Clinical Neurophysiology, LeidenUniversity Medical Centre, Leiden, The Netherlands

Joseph M. Furman MD PhDDepartments of Otolaryngology, Neurology, Bioengineering, andPhysical Therapy, University of Pittsburgh School of Medicine,Pittsburgh, PA, USA

Michael A. GrestyMRC Spatial Disorientation Group, Academic Department ofNeuro-otology, Division of Neurosciences and PsychologicalMedicine, Imperial College of Science and Medicine, MedicalSchool at Charing Cross Hospital, London, UK

Richard S. Hallam MSc PhDReader in Psychology, University of East London, London, UK

Stefan Hesse MDKlinik Berlin, Department of Neurological Rehabilitation, FreeUniversity Berlin, Berlin, Germany

Fay B. Horak PhDNeurological Sciences Institute and Department of Neurologyand Physiology & Pharmacology, Oregon Health & ScienceUniversity, Portland, Oregon, USA

Rolf G. Jacob MDDepartments of Psychiatry and Otolaryngology, University ofPittsburgh School of Medicine, Pittsburgh, PA, USA

Marjan Jahanshahi MPhil (Clin Psychol) PhDHonorary Reader in Cognitive Neuroscience, Institute ofNeurology, University College London, London, UK

Kenton R. Kaufman PhD PEAssociate Professor of Bioengineering, Director, BiomechanicsLaboratory, Consultant, Department of Orthopedic Surgery,Mayo Clinic/Mayo Foundation, Rochester, MN, USA

Rose Anne Kenny MD FRCP FRCPIProfessor and Consultant in Cardiovascular Research, RoyalVictoria Infirmary, Newcastle-upon-Tyne, UK

José C. Masdeu MD PhDProfessor and Chairman, Department of the NeurologicalSciences, University of Navarre Medical School, CUN,Pamplona, Spain

Jean MassionInstitute of Physiological and Cognitive Neurosciences (INPC),National Center of Scientific Research (CNRS), Marseille, France

Karl-Heinz Mauritz MDProfessor and Chairman, Klinik Berlin, Department of NeurologicalRehabilitation, Free University Berlin, Berlin, Germany

Louw van Niekerk MBChB(Pret), FRCS(Ed) FRCS (Orth)Consultant Orthopaedic Sports Surgeon, Friarage Duchess ofKent Military Hospital, Northallerton, North Yorkshire, UK

John G. Nutt MDDepartment of Neurology and Physiology & Pharmacology,Oregon Health & Sciences University, Portland, OR, USA

Sebastiaan Overeem PhDDepartment of Neurology and Clinical Neurophysiology, LeidenUniversity Medical Centre, Leiden, The Netherlands

Peter Overstall MB FRCPConsultant in Geriatric Medicine, County Hospital, Hereford, UK

Aftab PatlaGait and Posture Laboratory, Department of Kinesiology,University of Waterloo, Ontario, Canada

John H. Patrick MB FRCSOrthotic Res & Locomotor Assessment Unit, Robert Jones &Agnes Hunt Hospital, Oswestry, Shropshire, UK

Marousa Pavlou BA PTLecturer, Department of Physiotherapy, King’s College London,London, UK

Peter RudgeInstitute of Neurology, National Hospital for Neurology &`Neurosurgery, London, UK

Anne Shumway-CookNorthwest Physical Therapy Services, Seattle, WA, USA

Lewis Sudarsky MDDepartment of Neurology, Brigham and Women’s Hospital,Harvard Medical School, Boston, MA, USA

Pei-Fang Tang PhD, PTAssistant Professor, School and Graduate Institute of PhysicalTherapy, College of Medicine, National Taiwan University,Taipei, Taiwan

Philip D. Thompson MB PhD FRACPUniversity Department of Medicine, University of Adelaide, andDepartment of Neurology, Royal Adelaide Hospital, SouthAustralia

Cordula WernerJunior Researcher, Klinik Berlin, Department of NeurologicalRehabilitation, Free University Berlin, Berlin, Germany

Marjorie H. Woollacott PhDProfessor, Department of Exercise and Movement Science,University of Oregon, Eugene, Oregon, USA

Lucy Yardley MSc PhDReader in Health Psychology, Department of Psychology,University of Southampton, Southampton, UK

viii Contributors

Preface to the second edition

The reasons for writing a second edition of this book arerooted in the first one. First, disorders of balance and gaitare on the increase, as might be expected with our longerlifespan. Second, the first edition was so well received bycolleagues and reviewers that we felt it our duty to keepthis multidisciplinary effort alive. Problems with bal-ance, gait and posture are produced by such a diversity ofdisorders, in so many disparate systems, that a bookattempting to bring various disciplines together is arewarding and necessary task.

The seven-year gap between the first and second edi-tions means that the book has been almost completelyrewritten. John Nutt, who has specific expertise in move-ment disorders and related problems of gait, has joinedthe editorial team. New chapters dealing with criticalissues such as classification of balance and gait disorders,objective assessment of posture and gait, cerebrovasculardisease and hydrocephalus have been incorporated. Theimportant topic of syncope related falls is now covered intwo chapters, including one specifically devoted to this

problem in the elderly. Fifteen new authors have broughtnew expertise and complementary view points to the dif-ferent chapters. Examples are the chapters on psychiatricaspects of imbalance, where neurologists and psychia-trists present complementary views, and the chapter ondrop attacks, syncope-related falls and their mimics,where neurologists and autonomic nervous system specialists address these problems together.

As before, we did not intend to produce a mammothbook exhausting the field (and the reader). Our inten-tion was to bring together basic scientists and variousclinical specialists in order to present the range of prob-lems and to help busy clinicians to manage theirpatients. We hope we have succeeded.

Adolfo M. BronsteinThomas Brandt

Marjorie H. WoollacottJohn G. Nutt

Preface to the first edition

A crucial issue facing clinicians is the management of thepatient who has critically impaired walking abilities.Patients face the reality of being unable to look afterthemselves and the resultant pressure is transmitted torelatives and social services. The magnitude of this prob-lem has already begun to increase as the mean age of thepopulation in industrialized societies has risen.Unfortunately, the mechanisms underlying the produc-tion of human locomotion are complex and the natureof the disorders affecting locomotion are varied. Thus asimple solution to the problem of managing gait dis-orders is not available to us.

The diagnosis and management of the patient withabnormal balance, posture and gait presents the clinicianwith a formidable challenge. In no other set of disordersis it more genuine to think that what is wrong with thepatient can be due to impairments ranging from the topof the head to the tip of the toes! For example, disordersmay include various components of the motor system,the vestibular system, and the musculoskeletal appara-tus, giving rise to gait disorders or a sensation ofunsteadiness. In addition, psychological dysfunction canresult from, or present to the clinician, as a balance andgait problem. In older adults the involvement of multiplesystems in balance and gait disorders is most typical.

This book has been conceived with this multidiscipli-nary concept in mind. Although biased towards a clini-cal audience, we have attempted to provide a strong

physiological basis for a better understanding of mecha-nisms underlying balance and gait disorders. We havedivided the text into four sections dealing with normaland developmental aspects, assessment, disorders andrehabilitation of balance and gait plus a separate sectiondevoted to the problems of the elderly. The contributorscomprise neurologists, orthopedic surgeons, neuro-otol-ogists, geriatricians, psychologists, physiotherapists andphysiologists who have been encouraged to tread acrossfrontiers as is appropriate for such an interdisciplinarytask. It is therefore unavoidable that some overlap mayoccur, but we believe that the reader will be enriched bywitnessing the way similar topics are dealt with from avariety of viewpoints.

The aim of this book is not to exhaust any specific dis-ease resulting in impairment of gait, balance or posture.Such diseases will remain in the domain of the appropri-ate specialist but general guidelines and references areprovided for those interested. It is not our intention tocreate a new balance and gait specialist. Rather, we hopeto emphasize that whoever is dealing with patients withbalance and gait disorders can benefit from broadeningthe horizon of his or her own speciality.

Adolfo M. BronsteinThomas Brandt

Marjorie H. Woollacott1996

1Posture and equilibrium

JEAN MASSION AND MARJORIE H. WOOLLACOTT

INTRODUCTION

There are two different types of motor ability critical formotor coordination: the first involves voluntary motorcontrol and includes activities such as eye–hand coordi-nation function, and the second involves postural orequilibrium control. The latter is really the foundationfor all voluntary motor skills, with almost every move-ment that an individual makes being made up of both(1) postural components, which stabilize the body, and(2) the prime mover components which relate to a par-ticular movement goal.

Although clinicians understand the importance ofpostural control for activities such as standing, walkingand manipulation skills, there is no universal definitionof postural control, or a clear consensus on the mecha-nisms that underlie postural and balance functions. Inthis chapter we will first offer a broad definition of pos-tural control and then discuss research on the contribu-tions of different body systems to the control of balanceor posture.

In order to understand postural control as a behavior,we first need to understand its task. Initially, this involvesthe maintenance of the alignment of body posture andthe adoption of an appropriate vertical relationshipbetween body segments to counteract the forces of grav-ity and thus allow the maintenance of upright stance.Postural muscle tone is a primary contributor to themaintenance of vertical stance.

Once this alignment is achieved, the position of thebody’s center of mass must be maintained within specificboundaries in space, or stability limits, related to the indi-vidual’s base of support. Thus, a second part of the task ofpostural control is the maintenance of equilibrium.

Posture is also a key component of all perception–action systems and serves to maintain bodily orientation

to the environment. For example, an individual’s posturecan be considered a primary support for the explorationof the surrounding space in terms of perceptual analysisand motor action. For this exploration, the nervous sys-tem must have an accurate picture of the position of thebody segments with respect to each other and withrespect to space. The internal postural image or posturalbody schema provides this information and it is moni-tored by multisensory inputs. On the basis of this repre-sentation and according to the perception–action task,the orientation of one or several body segments (head,trunk, arm, etc.) will be selected as a reference frame forthe organization of the corresponding action.

Finally, posture also serves as a mechanical supportfor action. It organizes the coupling between the differ-ent segments as a function of the task and adjusts thejoint stiffness dynamically during the movement.

We begin this chapter with a discussion of posturalcontrol in relation to body alignment and the mainte-nance of bodily orientation to the environment. We willthen discuss the control of stability or balance control.Finally, we will consider posture as a mechanical supportfor action.

POSTURAL CONTROL DURING QUIET STANCE

Erect posture in humans is achieved by the superposi-tion of body segments (head, trunk and legs) along thelongitudinal axis. This superposition is such that itshould fulfil the two functions of posture. The first is theantigravity function. The superposition of segments isperformed against the force of gravity and the associatedground reaction forces. The postural tone, which is pre-dominantly distributed among the extensor muscles,plays an important role in this antigravity function.

Introduction 1Postural control during quiet stance 1Genetic model of posture control 3Hierarchical model of postural organization 4Multisensory convergence and balance control 7

Postural control in response to balance disturbances 8Posture control and movement 12Conclusions 15References 16

There is an additional constraint, which is equilibriummaintenance. This means that the positioning of bodysegments (which is only restricted by the mechanicallimits of joint movement) should be such that the pro-jection of the center of gravity (CG) remains inside thesupport base under static conditions.

A second function of posture is to serve as an inter-face with the external world for perception and action. Itmeans that the orientation with respect to space of givenbody segments such as the head, the trunk or the arm areused as a reference frame. The reference frame may beused either to perceive the position of the body’s move-ment with respect to the external world or to organizemovements toward a target in external space.

Taking into account the functions of posture accord-ing to the context and the task, two modes of posturalorganization have been proposed.

First, a global organization of posture is mainlyrelated to equilibrium control. It is represented by theinverted pendulum model described by Nashner andMcCollum.1 The reference value to be regulated for equi-librium control is still a matter of discussion. Balance,stricto sensu, is preserved when the center of pressure(CP) remains inside the support base (i.e. the surfaceunder the feet). Under static conditions this correspondsto the projection of the CG.

However, under dynamic conditions, as, for example,initiation of gait, the CG is accelerated by a torque at thelevel of the ankle joint created by activating muscles con-trolling that joint; this causes a shift of the CP,which movesaway from the CG projection. Thus, both CP position andCG projection onto the support base should be taken intoaccount for equilibrium control in dynamic conditions.According to the modeling of Paï and Patton,2 the borderof the stability limits can be predicted in dynamic condi-tions by a combination of three parameters: the CP posi-tion, the CG horizontal position and the CG velocity.

In order to regulate the CG position, which is locatedat the level of the pelvis, the whole body can be moved asan inverted pendulum around the ankle joint. However,as will be commented on later, these oscillations are veryslow (frequency around 0.2 Hz) because of the high inertia of the body. In case of fast perturbations, fast cor-rections are required. Other body segments with lowerinertia (trunk around the hip, thigh around the knee) arethen moved for fast corrections.3

Interestingly, the constraints related to body inertiaare not only important for equilibrium control. They arealso a key characteristic for the organization of move-ments. For example, it is possible to couple a set of jointsby increasing the corresponding joint stiffness. Thisresults in creating a new ensemble with an increasedinertia corresponding to that of the whole set of seg-ments coupled together. Droulez and Berthoz4 intro-duced the concept of topological organization of posturein order to describe this reorganization of body inertia.They provided two examples. When reading a paper

while walking, stiffness of the arm, trunk and head isincreased in order to create a new high inertial ensemblethat will reduce the movements of the arms with respectto the head. Conversely, unlocking the arm from thetrunk occurs in tasks where the stability of the handposition in space should be preserved independentlyfrom the trunk oscillations, as when the subject is walk-ing holding a full glass in the hand.

A second mode of organization is modular organiza-tion, which is used for orienting segments such as the headand trunk (which serve as a reference frame for perceptionand action) with respect to space. The various segments ofthe kinematic chain from the feet to the head are not con-trolled as a single functional unit, but as a superposition ofindividual ‘modules’. Each module is tied to the next oneby a set of muscles which has its own central and periph-eral control, aimed at maintaining the reference positionof the module. Martin5 has reported that postencephaliticpatients that had lost the ability to maintain the head axisvertical during normal life held the head permanentlyinclined on the trunk. When asked to raise the head by avoluntary movement, they were able to do so for sometime. There was thus dissociation between an automaticregulation of the head position, which was lost, and itsvoluntary control, which was preserved.

The head is the site of different categories of sensors,such as the retina, the labyrinthine afferents and the neckmuscle proprioceptors. Each category of receptors hasbeen shown to be able to stabilize the head. The head canbe stabilized with respect to gaze,6 verticality7 and to thetrunk.8 Orientation and stabilization of the trunk axis,which is the largest axis of any body segment, is critical.9

Stabilization of the trunk has also been observed withrespect to vertical in the frontal plane during leg move-ment10 and during locomotion11 or during oscillatorymovements of the supporting platform.12 Interestingly,maintaining equilibrium through the global organiza-tion of posture and preserving the orientation of bodysegments with respect to space may be conflicting ingiven motor acts through the modular control of pos-ture. For example, there will be a conflict between equi-librium maintenance and holding a full glass of wine bythe hand (local posture) when a postural disturbanceoccurs that endangers balance. In this case, the subjectwill lose balance, take a support with the other hand andkeep the glass full. The modular organization of posturecan serve to regulate posture itself. The stabilization ofthe head in space during locomotion is used as a naviga-tional inertial platform for the evaluation of the visual orlabyrinthine inputs. These inputs signal changes of bodyposition with respect to the external world.13

Another important role of this modular organizationof posture is to serve as an egocentric reference frame forthe organization of movement. For example, during areaching task, head and trunk axes are reference valuesfor the calculation of the target position with respect tothe body (as shown by neck vibration experiments)14 and

2 Posture and equilibrium

for the calculation of the hand trajectory.15 Also, duringmanipulation of heavy objects, the forearm position isstabilized and serves as a reference frame for this task.9

How the various modes of postural organization arecentrally controlled has been a matter of discussions andtwo main models have been proposed, the ‘geneticmodel’ and the ‘hierarchical model.’

GENETIC MODEL OF POSTURE CONTROL

In a classical view of postural control, based on the workof Magnus16 and Rademaker,17 each animal species isconsidered to have a reference posture or stance, which isgenetically determined. According to this view, posturalcontrol and its adaptation to the environment is basedon background postural tone and on the posturalreflexes or reactions. These reactions are considered tooriginate from inputs from the visual and vestibular sys-tems (localized at the level of the head) and from thesomatosensory system, with inputs at the level of the dif-ferent body segments.

According to this classical view, the main constraintfor building up the reference posture, which is stance, isconsidered to be the effect of gravity on the body seg-ments. The gravity vector is considered to serve as a ref-erence frame, the so-called geocentric reference frame,18

for the positioning of the different body segments withrespect to each other and to the external world.

Three main functions are identified in the geneticmodel of posture: (1) an antigravity function; (2) bodysegment orientation with respect to gravity; (3) theadaptation of posture to the body orientation in space.

Antigravity function

The antigravity function provides a support for the bodysegments against the contact forces exerted by theground due to gravity and contributes to equilibriummaintenance.

Postural tone is the main tool for building the anti-gravity posture. It is predominantly observed at the levelof the limbs, back and neck extensor muscles and the mas-seter muscle of the jaw. The main force vector of thesemuscles counteracts the effect of gravity when the subjectis standing on a support surface. Decerebrate rigidity,which is observed after midcollicular decerebration inanimals, is a caricature of this background postural tone.19

Interestingly, postural tone depends on the integrityof the myotatic reflex loop and is suppressed by sectionof the dorsal roots. Therefore, decerebrate rigidity hasbeen called ‘gamma’ rigidity, in contrast to the ‘alpha’rigidity observed in the quadruped after cerebellar ante-rior lobe lesions, which is preserved after dorsal root sec-tion. Since postural tone is under the control of themyotatic reflex loop, one possible mechanism for con-

trolling erect posture is the stretch reflex, which wouldbe able to oppose any deviation from the initial posture,as pointed out by Lloyd.20 However, recent research indi-cates that normal young adults typically do not showmonosynaptic stretch reflex responses when respondingto threats to balance during quiet stance21–23 and thathigher levels of control are involved.

A series of postural reflexes contribute to the anti-gravity function: they adapt muscle force to body weight.Examples include the myotatic reflexes and the positivesupporting reactions which adjust the leg and trunkmuscle tone to the body weight.

The postural reactions are aimed at restoring balance inface of an internal disturbance. According to Forssberg,24

they are based on a set of inborn reactions that are selectedand shaped during ontogenesis.

Orientation of the body segments withrespect to the gravity vector

The gravity sensors of the lateral line organ, together withlight-sensitive afferents, serve to orient the longitudinalbody axis of fish with respect to gravity. In mammals,where the body is segmented into head, trunk and legs,the otoliths and vision serve for orienting the head withrespect to the gravity axis. The orientation is horizontal inthe cat and vertical in humans; the orientation of theother segments is a function of that of the head. Therighting reflexes described by Rademaker17 are an illustra-tion of this concept. As first shown by Etienne-JulesMarey, when a cat falls from an inverted position, thehead is first reoriented along the horizontal plane, thenthe trunk orientation with respect to the head is restoredand finally the leg axis becomes vertical. The head orien-tation in space is stabilized by the vestibulocollic reflexes,which play an important role during locomotion.

Other reflexes serve to orient the foot with respect tothe support. These include the placing reactions. Thereare three placing reactions: the tactile placing reaction,which causes flexion followed by extension of the leg inresponse to cutaneous stimulation; and the visual andlabyrinthine placing reactions, both eliciting extensionof the forelimbs when the animal is dropped toward theground. Other reflexes such as the hopping reaction, areaimed at reorienting the leg with respect to the gravityaxis.25

Adaptation of the antigravity posture to thebody segment posture or movement

A third function of the genetic organization is to adjustantigravity posture to ongoing activity. Examples of thisare the labyrinthine reflexes, which adjust the posturaltone as a function of the head position in the frontal orsagittal plane. For example, when the whole body isinclined toward one side, the otolith inputs from that side

Genetic model of posture control 3

induce an increased postural tone on the same side. Theneck and labyrinthine reflexes illustrate another exampleof adaptation of posture to ongoing activity. They orientthe leg and trunk posture as a function either of the neckorientation in space or of the pelvis orientation in space.For example, turning the head toward the right induces

an extension of the fore and hind limbs toward the sameside and a flexion of the limbs of the opposite side. In con-trast, turning the trunk toward the same side provokes aflexion of the ipsilateral forelimb and an extension of theipsilateral hindlimb (Fig. 1.1).26

Summary

To conclude, the three main functions of the geneticorganization of erect posture (i.e. the support of thebody against gravity, the orientation of the body withrespect to the gravity vector and the adaptation of thebody posture to the ongoing head and trunk movement)are critical for adapting erect posture to the environmentand to ongoing activity. These functions are controlledby spinal cord (propriospinal circuits) and brainstempathways. Some reflexes, such as the tactile placing reac-tion include motor cortex pathways.

HIERARCHICAL MODEL OF POSTURALORGANIZATION

The genetic model of posture has been challenged for sev-eral reasons. First, the postural reactions to stance distur-bance have been shown to be flexible.1,27 For example,when a balance disturbance occurs while standing, themain muscles involved in the correction are the leg mus-cles. If the subject holds on to an additional support withthe hands, the postural reactions will involve mainly thearm muscles. These, and other observations are not com-patible with a reflex organization and suggest a spatio-temporal flexibility of the response according to taskconstraints.

Second, postural control has been analysed in abehavioral context during the performance of voluntarymovements. Anticipatory postural adjustments havebeen described during the performance of goal-directedmovements. They are aimed at both preserving balanceand the orientation of body segments during the perfor-mance of the movement and at assisting the movementin terms of force and velocity.28 Interestingly, anticipa-tion means prediction of the postural disturbancebecause of the movement. This prediction would dependon internal models built by the brain, which would mapthe surrounding space, the body characteristics and theirinteraction. This idea was proposed by Bernstein29 on thebasis of his observations on motor learning and wereextended to posture by Gurfinkel and co-workers.30–32

The hierarchical model of posture proposes that twolevels of control exist. The first is a level of representationor postural body schema; the second is a level of imple-mentation for postural control.

The concept of body schema was first proposed byHead.33 In its adaptation to posture, the internal repre-


Figure 1.1 Comparison between neck and lumbar reflexes.Reproduced from Tokizane T, Murao M, Ogata T, Kondo T.Electromyographic studies on tonic neck, lumbar andlabyrinthine reflexes in normal persons. Jpn J Physiol1951;2:130–46, with permission from the Center for AcademicPublications, Japan.

Tonic lumbar reflex

Tonic neck reflex

(a) Stance(b) Dorsiflexion(c) Ventroflexion

(d) Rotation right(e) Deviation right

(a) (b)

(d) (e)

(c)

(a) (b)

(d) (e)

(c)

sentation of body posture, or body schema has beenhypothesized to be partly genetically determined andpartly acquired by learning. It includes three mainaspects: (1) a representation of the body geometry, (2) arepresentation of body kinetics, mainly related to theconditions of support, and (3) a representation of thebody orientation with respect to gravity (vertical).

Geometric representation of the body

Research suggests that the individual’s geometric repre-sentation of the body depends mainly on the informa-tion provided by the proprioceptive Ia afferent inputs.Studies using minivibrators to excite eye, neck and anklemuscles afferents34,35 have explored the contributions ofproprioceptive inputs from these muscles both to per-ception of body sway and to actual posture control dur-ing quiet stance. It was found that vibration to the eyemuscles, the neck muscles or the ankle muscles of astanding subject with eyes closed produced body sway,with the sway direction depending on the musclevibrated. When these muscles were vibrated simultane-ously, the effects were additive, with no clear dominationof one proprioceptive influence over another. When thebody was prevented from moving during the tendonvibration, it created an illusion of movement.

This suggests that proprioception from all parts of thebody plays an important role in the maintenance ofquiet stance body posture. The experiments also suggestthat, when an individual is standing, there is a kinematicchain formed by the Ia inputs from muscles around eachjoint, informing the nervous system about the positionof each joint with respect to the remaining parts of thebody. It is interesting that vibration of the ocular musclesalso induced postural reactions. This indicates that theymonitor the position of the eyes with respect to the headand thus are able to estimate the position of a visual tar-get in terms of head coordinates.

The output of the spindle primary afferent inputs isinterpreted differently by the central nervous systemdepending on such factors as the selected referenceframe of the subject (for example, is the body the refer-ence frame, or are three-dimensional environmentalcoordinates the reference frame) and the presence ofgravity. As mentioned above, when an individual isstanding and when body weight is exerted on a support-ing surface, the proprioceptive Ia afferent inputs monitorboth body displacement and velocity of displacement.The effect of Achilles tendon vibration when the eyes areclosed is to cause postural sway in response to the erro-neous Ia input that mimics the displacement of the limb.However, under microgravity conditions36 or when anindividual is sitting, tendon vibration produces no pos-tural reactions. This means that the monitoring of bodyposture by proprioceptive inputs depends a great deal ongraviceptors.

It is also interesting that the postural responseinduced by galvanic stimulation of vestibular receptorsdepends on the body geometry and the postural bodyschema.32,37 For example, it has been demonstrated thatwhen a subject is standing normally, cathodic stimula-tion of one labyrinth elicits a shift of the center of grav-ity in the frontal plane toward the same side. However,when the head is turned to the right, the same stimula-tion elicits a displacement of the center of gravity back-wards. The result shows that the postural responsedepends on the head position with respect to the trunk.The same change in the direction of the posturalresponse is observed when head and trunk together arerotated to the right.

How is the head and trunk position monitored withrespect to the legs? Vibration of the right gluteus max-imus with the trunk fixed induces an illusory rotation ofthe head–trunk segment to the right. When galvanicvestibular stimulation is performed during right gluteusmaximus vibration, it provokes a backward sway as if thehead (and trunk) was actually rotated to the right. Thisobservation elucidates the role of the Ia proprioceptiveinputs stimulated by vibration in reorienting the pos-tural reaction and thus monitoring the head–trunk posi-tion with respect to the legs (Fig. 1.2).

Figure 1.2 Galvanic stimulation of the right labyrinth. Thearrow indicates the stimulated side. Center of pressure recordedfrom a force platform (according to ref. 32). When the head isstraight, the postural reaction to anodic stimulation is orientedto the right. When the head (or head and trunk) is turned to theright, the postural reaction to the same stimulus is orientedbackward. The same backward-oriented postural reaction isobtained by galvanic stimulation during a vibration of thegluteus maximus, which provokes an illusion of head–trunkrotation to the right.

Cat

hode

Ano

de

Hierarchical model of postural organization 5

Representation of body kinetics

Two issues concerning body kinetics should be men-tioned: (1) the nervous system’s evaluation of the sup-port conditions (this concerns the orientation of bodysegments with respect to the gravity axis; see next sec-tion), and (2) the calculation under dynamic conditionsof the inertia of different body segments, providing anaccurate estimation of the center of gravity position.

During stance, reaction forces are exerted by the sup-porting platform on the body. They are the main basisfor the maintenance of the erect posture. It is generallyconcluded that stance results from a ‘bottom up’ (that is,support surface oriented) maintenance of balance, onthe basis of these reaction forces. Whether these reactionforces are perceived and how they might be perceived isstill partly unanswered. The foot sole receptors togetherwith proprioceptive inputs monitoring the ankle jointangle play an important role in this respect.38

Several studies have shown that the organization ofpostural reactions depends on the conditions of support.For example, when the standing subject is holding a leverwith the hands, the postural reactions previously seen inthe leg muscles now move to the arm extensors.39 Thus,when part of the body support is taken by the hand, thepostural reactions to a stance disturbance involve mainlythe arm extensor muscles in place of the leg muscles.When the body weight is absent, as under water, the pos-tural reactions tend to disappear.40 There is thus an inter-nal representation of the support conditions, whichselects the appropriate actuators for optimizing the equi-librium maintenance.

A second aspect of body kinetics involves the inertialproperties of the segments. These properties are auto-matically taken into account for the regulation of bal-ance. For example, after adding a 10 kg load on theshoulder, the regulation of the center of gravity duringan upper-trunk bending is just as efficient as without aload.41 There is also evidence indicating that perceptionof body inertia does exist.42 This would explain why aregulation of the body center of mass still exists inmicrogravity during multisegmental movements such astrunk bending.43

Orientation with respect to vertical

The orientation of the body with respect to vertical inthe frontal plane and in the sagittal plane is a primaryconstraint for erect posture in a world in which theeffects of gravity must be taken into account. Which sen-sors indicate that the body posture is appropriately ori-ented with respect to vertical and which ones are usedfor stabilizing the selected orientation? There are no sta-tic sensors that directly monitor the center of gravityprojection to the ground. The body orientation withrespect to vertical in the frontal and sagittal plane is reg-

ulated by sensors located in the head and in other bodysegments.

As mentioned earlier, body posture results from thesuperposition of multiple segments from the feet to thehead. How is the orientation of the segments withrespect to the vertical calculated and how is the orienta-tion of the individual segments controlled in order tomaintain equilibrium? In this respect, according toMergner and Rosemeier,44 there are two main modes ofrepresentation of the body segments with respect to theexternal world, depending on the reference valueselected for this calculation.

In a top-down mode, the labyrinthine informationfrom the otoliths is used as a reference value for calculat-ing the head orientation with respect to the vertical. Thecalculation of the position of the trunk, pelvis, leg andfeet segments in space is performed with respect to thehead position in space. This mode is the first to emergeduring ontogenesis, with the early stabilization of thehead in space.24 A second mode, a bottom-up mode, usesthe support surface (under the feet) as a reference valuefor the calculation of the pelvic position in space. Thismode is mainly related to equilibrium control. It emergeslater during ontogenesis, with stance and locomotion.

Four sources of information regarding orientationwith respect to verticality are the labyrinthine and visualsensors located in the head, the haptic sensors and thebody graviceptors.

LABYRINTHINE SENSORS

Information about the gravity vector is provided by theotoliths. The vertical orientation of the head in the darkis generally attributed to their activity.16,17 The distribu-tion of the otoliths in the vertical and horizontal planeprovides information on the inclination of the head withrespect to vertical both in the sagittal and in the frontalplane. Since the otolith receptors also monitor the linearacceleration along the horizontal and the vertical axes,the information about the gravity vector is biased whenthe subject (or the head) is moving. It is still unclear towhat extent these sensors contribute to the determina-tion of vertical.

The labyrinthine receptors also play an importantrole in stabilizing the head and in body orientation.Linear acceleration is monitored by the otoliths andangular acceleration (pitch, roll and yaw) by the threepairs of semicircular canals.

VISUAL SENSORS

Visual static input, involving the vertical or horizontalstructure of the visual frame (the objects within thevisual field), is used for orienting the body axis.45

Research has shown that providing a biased visual framemodifies both the perception of vertical and posturalorientation.


The stabilization of orientation on the basis of visualinput depends mainly on visual inputs detecting move-ment. Through this information the visual system mon-itors head and body displacement with respect to theexternal world. This type of information is called vec-tion. The linear displacement of the visual frame withinthe peripheral visual field provokes body sway in thedirection of the displacement of the visual frame, withthe intensity of the sway depending on the velocity andon the spatial frequency of the visual frame.46

Sinusoidal displacements of the visual frame are asso-ciated with sinusoidal postural sway, with no phase shiftbetween the two, indicating a coupling between bothoscillations.47 Circular vection in the frontal plane causesbody inclination toward the direction of the vection.48,49

The direction of postural reactions can be interpreted inthe following ways. The displacement of the visual scenebackwards when the subject is standing mimics the situ-ation of the body falling forward, in a direction oppositeto the moving scene. The backward postural sway in thedirection of the moving scene thus mimics the normalcompensatory reactions that would occur when the sub-ject was actually falling forward.

The visual and labyrinthine inputs are located in thehead and they help to orient the head position. However,as the position of the head with respect to the trunk isnot fixed, their influence on body posture and, morespecifically, on balance control depends on the evalua-tion of head position with respect to the trunk. As men-tioned earlier, this evaluation is made by the neck muscleproprioceptors.

HAPTIC SENSORS

A simple contact of the hand or of the fingers with anexternal surface can be used as a reference frame for cal-culating the body oscillations with respect to that surfaceand to correct the oscillations with a latency of around50 ms. Haptic cues are very efficient in stabilizing pos-ture, especially by handicapped patients when using acane. Interestingly, when the support on which the handis in contact is rhythmically moving, some subjects showbody sway at the same frequency without phase shift,indicating a feed-forward control.50

BODY GRAVICEPTORS

A fourth category of sensors that serve for the orienta-tion with respect to verticality is represented by the ‘so-called’ body graviceptors. The existence of bodygraviceptors was first proposed by Gurfinkel et al.12 inorder to explain the ability of subjects to stabilize thetrunk when the support surface was moving sinusoidallyand by Mittelstaedt51 who provides evidence for gravi-ceptors in the area around the kidney. Riccio et al.,52

using a specific set-up to dissociate the axis for balancecontrol from the vertical axis, indicated that the per-ceived orientation of the body depends both on the

gravity vector and on the orientation of the ground reaction force exerted by the subject to control balance.

Indirect evidence concerning the role of body gravi-ceptors on body orientation was provided by experi-ments on the postural orientation of divers when underwater. It was shown that, when under water, the bodyorientation was always tilted forward with respect to ver-tical, suggesting incorrect information from body gravi-ceptors contributing to the body’s orientation under thisabnormal weight condition.53

Experiments by Dietz and colleagues54,55 have also pro-vided evidence in favor of body graviceptors. When asubject standing on a platform under water in a pool isgiven support surface perturbations to balance, posturalreactions are absent. Since the water pressure cancelsnormal body weight, the researchers compensated forthe lack of body weight in the subjects by adding loads atthe level of the different joints. Under these conditions,the postural corrective reactions in response to a distur-bance of the support platform returned as a function ofthe weight added at each joint.

Further experiments were performed in which hori-zontal loads were placed on subjects lying supine, thuscreating forces on joints equivalent to standing vertically.Under these conditions, the subjects showed posturalreactions similar to those observed during quiet stand-ing, when the support surface to which the feet wereattached was disturbed. Dietz et al.55 suggested that grav-iceptors were monitoring the force exerted by the subjectto oppose the external forces. In normal stance, thesegraviceptors would monitor the force vector exerted ateach joint to oppose gravity and this information wouldcontribute to an internal representation of the verticalaxis. A putative candidate for the monitoring of this sen-sory information is the Golgi tendon organ, which mea-sures the number of active motor units at a given time ineach muscle used in postural control.56

In addition to specific graviceptors, the stabilizationof balance by body sensors depends mainly on cutaneousfoot sole sensors which monitor the amplitude and thedirection of the contact forces exerted by the body ontothe ground. Experiments that support these conclusionshave shown that replacing a firm support surface by afoam surface or cooling the foot sole results in posturalinstability,45,57,58 whereas vibration of the foot solerestricted to front or back parts induces postural sway38

in a direction that would oppose the swaying of the per-son toward the front or the back part of the feet.

MULTISENSORY CONVERGENCE ANDBALANCE CONTROL

The use of sensory information from multiple sources,including the visual, vestibular and somatosensory sys-tems, is a key feature of the neural control of both body

Multisensory convergence and balance control 7

orientation with respect to vertical and stabilizationagainst external disturbances.

There are two opposite interpretations concerningthe role of the multisensory afferents. According to oneview, the multiple sensory afferents are used to build upthe vertical reference value on which the body will bealigned. This hypothesis has been put forward byHlavacka et al.59 to explain the postural reorientationthat is observed after combined proprioceptive andvestibular stimulation. The misperception of the bodymidline when unilateral neck muscles are vibrated orwhen unilateral vestibular galvanic stimulation is per-formed supports this interpretation.60

Another interpretation is that the multiple sensoryinputs serve for monitoring the error of the actual pos-ture with respect to a reference value defined by othersensors. The forward sway of the body during tibialisanterior vibration in the standing subject has been inter-preted in the following way. The vertical reference valueis provided by a set of graviceptors. The artificial Ia inputinduced by the tibialis muscle tendon vibration is inter-preted by the central nervous system as indicating astretching of that muscle and a backward body sway withrespect to the vertical. The forward body sway is viewedas a correction of posture in response to the artificial Iaafferent inputs indicating backward sway.

One possible use of redundant sensory informationin the regulation of posture is that different set of sensorsare put into action according to the source or the veloc-ity of the postural disturbance. The sensitivity range ofeach category of sensors is different. For example, visualinput gives sensitive information related to low-velocitydisplacements of the body, whereas labyrinthine inputsare sensitive to high rates of acceleration.

Two modes of interaction between these inputs havebeen identified by manipulating one category of inputs,the other being unchanged, or by depriving the subjectof one or several sources of sensory information.

Additive effect

Usually, each input adds its effect to the effect of theother inputs. Thus, visual vection, by itself, will producepostural changes when the other inputs are unchanged.In addition, the body orientation will be biased withrespect to vertical when the visual reference frame isinclined, even though the labyrinthine and propriocep-tive inputs are unchanged. In this case, there is a sensoryconflict between the two types of information about ver-ticality and the resulting postural orientation is interme-diate with respect to the orientation prescribed by eachcategory of sensors.

The additive effect of the various inputs in posturecontrol may partly explain the compensatory mecha-nisms involved when one of the inputs is suppressed. Asshown by Horak et al.,61 in patients with labyrinthine

lesions, postural control is relatively well preserved,though only visual and somatosensory inputs are avail-able. However, disturbance of one of the remaininginputs (vision or somatosensory) markedly decreases thepatient’s ability to balance.

Selection

When conflicts between the information from one typeof input and the others arise, one way of resolving theconflict is to select one input which becomes dominant.For example, Achilles tendon vibration produces back-ward body sway with eyes closed because the somatosen-sory system is signaling stretch to the gastrocnemius/soleus muscles and thus forward sway. However, whenvision is available, the vibration has no postural effect.One could regard this as indicating that the retinal inputis dominant and the erroneous input is disregarded. Analternative explanation is that, with eyes open, bothvision and vestibular inputs are signaling that no move-ment is taking place, and somatosensory inputs are thusthe only inputs signaling movement. In this case the sin-gle conflicting input is disregarded.34

It should be stressed that there are individual differ-ences in the dominance patterns of the three sensoryinputs. Some subjects rely more on vision, while othersrely more on somatosensory inputs.

POSTURAL CONTROL IN RESPONSE TOBALANCE DISTURBANCES

In the last section we reviewed research pertaining tobalance control during quiet stance. In many ways this isthe simplest form of balance control, since the individualis simply maintaining quiet stance. We will now move onto discuss research on balance control in conditionswhere there are external threats to balance, such as bal-ancing while standing on a bus which is starting andstopping unexpectedly. This is somewhat more difficultthan simply controlling background sway and requiresthe ability to respond to perturbations to balance differ-ing in direction, amplitude and velocity.

Strategies and synergies

A researcher who has influenced research in postural andmovement control considerably is Nicholai Bernstein, aRussian investigator, who argued on theoretical groundsthat it would be difficult for the brain to regulate inde-pendently the incredible number of motions of the manymechanical linkages of the body and the activities of theassociated muscle groups.29 He thus hypothesized thatthe nervous system organizes movement in a hierarchi-cal manner, with higher levels of the nervous system


activating lower level synergies, which are groups ofmuscles constrained to act together as a unit. This wouldthus free up the higher levels of the nervous system forother roles, such as adapting responses to changing taskconditions. He hypothesized that such actions as breath-ing, walking and postural control would use synergies tocoordinate the activation of muscles as a unit.

In order to test this hypothesis, researchers haveexplored the characteristics of muscle responses activatedwhen a subject is exposed to external threats to balance.Gurfinkel and his colleagues performed the first extensiveexperiments on the contributions of the peripheral andcentral neural control mechanisms to posture duringquiet stance.62,63 They showed that the excitability levels ofthe monosynaptic stretch reflex decrease during stancecompared with less demanding postural tasks such aslying down, sitting or standing with support. Why wouldthis be the case? They suggested that this would allow pos-tural control to be dominated by longer latency responses(latencies of 70–125 ms, which may be spinally orsupraspinally mediated), which are more adaptable andthus more useful in dealing with stance balance controlunder a wide range of conditions. Gurfinkel and his col-leagues proposed that this reorganization in neural con-trol of posture was the result of the functioning of centralprograms which coordinate the activity of different muscle groups during postural control.

Other research by Nashner21 and Nashner andWoollacott64 has further explored Bernstein’s hypothesisby examining whether the responses activated in musclesof the leg and trunk in response to perturbations to balance are part of a pre-programmed neural response orsynergy or are the result of independent stretch and activation of individual muscles, owing to a simplemechanical coupling of ankle and hip motion during theperturbation.

Subjects were asked to stand on a platform whichcould be moved unexpectedly in the forward or back-ward direction or rotated, to cause ankle dorsiflexion orplantarflexion (Fig. 1.3). The different types of platformmotions destabilized balance in different ways, requiringthe activation of different muscle groups in order toregain balance. The activity of muscles which contributeto the control of the movements of the ankle, knee andhip was monitored.21,64

The results showed that, in response to backward plat-form translations causing anterior sway, gastrocnemius,the stretched ankle muscle was activated approximately90 ms after platform movement onset, followed sequen-tially by the hamstrings muscle and the paraspinal mus-cles at approximately 20-ms intervals. Note that thegastrocnemius response is about 50 ms later than mono-synaptic stretch reflex latencies, suggesting that it involvesmore complex neural pathways. Forward translationscaused backward sway and activation of the stretched tibialis anterior muscle, followed by the quadriceps andabdominals (Fig. 1.4).

Was this response the result of a synergic coupling ofthese muscles or, alternatively, the result of independentstretch of the individual muscles? In order to answer thisquestion the authors changed the mechanical couplingof the ankle and hip motions by giving the subjects plat-form rotations, which directly rotated the ankles withoutcausing movements at the other joints. These platformrotations caused activation of the same groups of legmuscles, thus suggesting that it was movement in a singlejoint, the ankle joint, that was activating the responses inmultiple muscles.21,64

Experiments were also performed to test whetherankle joint rotation is required to activate the response.In these experiments the platform was moved forward,but during the movement it was rotated in order to keepthe ankle joints at a constant 90°, thus eliminating anklerotation. Under this condition, the muscle responseswere delayed. Because the response was delayed it wasconcluded that the early response was elicited primarilyby ankle joint inputs, while a later response possibly acti-vated by vestibular and/or visual inputs, served to stabi-lize balance. This evidence supported the hypothesis thatbalance is controlled by neurally programmed synergies,and since the coupling of the muscles served the func-tion of stabilizing ankle sway, the response was termedthe ‘sway synergy’.1,21

Postural control in response to balance disturbances 9

Figure 1.3 Diagram of the hydraulically activated platformused to perturb the balance of standing subjects. The platformmay be translated in the antero-posterior direction or rotatedabout an axis collinear with the ankle joints (reproduced fromref. 109 with permission from The American PhysiologicalSociety).

Are strategies versus synergies invariant?

In further research, Horak and Nashner65 found thatunder conditions in which it was difficult to use ankletorque to balance (standing on a surface that was muchshorter than the foot), subjects mainly used motion atthe hip to compensate for threats to balance. Under thiscondition, forward and backward platform movementswere compensated for by activating the thigh and trunkmuscles on the unstretched aspect of the leg (see Fig.1.4c,d).65 This muscle response pattern or synergyrestored balance primarily through movement at the hipand was termed the ‘hip strategy’ as opposed to the ‘anklestrategy’ by which balance is restored primarily throughmovement at the ankle.

Although the responses of select muscles and bodymovement patterns associated with balance recoverygive some information on motor control strategiesunderlying balance, the calculation of joint torques usedin postural recovery gives information on the sum of

forces provided by all the muscles acting at a given joint.Thus, one can observe the work of additional musclesbeyond those recorded through electromyographs(EMGs).

Researchers66,67 have used this technique to explore theconditions under which subjects use ankle vs. hip strate-gies when recovering balance on a normal surface. Theytested the hypothesis that ankle strategies are used pri-marily for low velocity (center of mass stays well withinthe stability limits) threats to balance while hip strategiesare used for higher velocity threats (center of mass movescloser to the limits of stability). It has been shown that, asplatform movement velocities gradually increase from10 cm/s up to as much as 55–80 cm/s, subjects increasemuscle forces at the ankle, and then begin to add in forcesat the hip at a certain critical threshold point. This pointvaries across subjects. Pure hip strategies, previouslyobserved by monitoring EMG patterns when subjectsresponded to postural perturbations while standing on anarrow support surface65 were not found.66,67


Figure 1.4 Examples of the muscle activation patterns observed in response to (a) backward platform movements causing forwardsway; (b) forward platform movements causing backward sway. These activate the ankle synergy, with responses starting in thestretched ankle muscle, followed by the leg and trunk muscles. (c,d) Muscle response patterns observed when subjects are balancedon a short support surface (restraining the use of ankle torque) while the platform moved backward (c) or forward (d), and activatedthe hip synergy (adapted from ref. 65).

How could strategy be defined with respect to synergyand is this distinction between two concepts justified?During voluntary movement, the strategy is defined asthe path that is selected for reaching a goal. For example,during a reaching task designed to pick up an object ona table, the usual trajectory of the hand is a straight line.When an obstacle is present on this straight-line trajec-tory, a curvilinear trajectory is performed (see, for example, ref. 68). Straight-line and curvilinear trajecto-ries can be defined as strategies. The execution of thestrategy is realized by muscle patterns or synergies,which are the implementation of the strategy.

The same distinction between strategy and synergywas introduced in the postural domain by Horak andNashner.65 The ankle strategy and the hip strategy aretwo different ways of reaching the same goal of restora-tion of balance. These strategies are defined in terms ofkinematics (i.e. changes in the body geometry). In orderto control the strategy, muscle patterns or synergies areobserved which produce the appropriate muscle force.Under the usual environmental conditions, both strate-gies and synergies are invariant (i.e. the same muscle pat-tern is associated with a given ‘strategy’). This explainswhy strategy and synergy are often used as equivalentterms in many papers. However, when the external con-straints change, then the muscle synergy should changein order to achieve the same ‘strategy.’

The experiments of Macpherson27 provide evidencethat by changing the direction of stance disturbance inthe cat, the strategy remains invariant whereas the mus-cle synergies change. In contrast to the ankle and hipstrategies reported by Horak and Nashner,65 which aredefined in terms of kinematics, Macpherson described astrategy in terms of ground reaction forces in the cat: thebiomechanical strategy used by the cat involved primar-ily the hindlimbs and showed invariance in the directionof the vector of force they generated. For any of 16 per-turbation directions, the system made a simple two-choice response for vector direction: either backward/outward or forward. This behavioral strategy clearly sim-plifies the control process. However, the muscle synergiesassociated with this strategy were more variable. Some ofthe muscles were co-modulated, including the hip anddistal muscles such as the gastrocnemius, and thus mayhave been activated by a central command. However,others, such as the gracilis, were controlled indepen-dently. It was thus concluded that in cat postural control,invariances exist for (1) the direction of force generationby the two hindlimbs (i.e. the strategy), and (2) thegrouping of certain hindlimb muscles, which were partof the synergy. However, the independent control ofother muscles indicates that they may be used to ‘tune’the synergy in order to produce the biomechanical goalof the production of specific ground reaction forces.69

Investigations of the flexibility of muscle synergieswere also performed in humans. The evidence from pre-vious research supports the concept of the existence of

fixed postural synergies when subjects are perturbed inthe anterior/posterior direction. However, it is alsoimportant to determine if using a variety of differentangles of platform motion to perturb balance, includingthose in the lateral direction, would result in the activa-tion of only a small number of fixed synergies, or whethermuscle response patterns would show a continuous vari-ation, as the angle of perturbation was moved from ante-rior/posterior to lateral. If synergies vary continuouslywith angle of perturbation, it weakens the hypothesis thatbalance is controlled by fixed muscle response patterns.In order to answer this question further experiments wereperformed,70 in which the balance of subjects was per-turbed as in the above experiments, but subjects wereasked to pivot at 15° increments between blocks of trials.

It was noted that the pattern of responses in direc-tions near the sagittal plane (300–15°) showed a rela-tively constant onset latency relationship betweenmuscles, with responses in the gastrocnemius, ham-strings and trunk extensors, as predicted, along with anearly response in the abdominals (probably because ofthe high velocity of perturbation: 25 cm/s versus 13 cm/sused in prior experiments). Muscle patterns were similarfor tibialis anterior, quadriceps and abdominals (with anearly trunk extensor response) for directions of165–225°. For other perturbation angles, however,latency relationships varied continuously and sharptransitions in latency and/or amplitude were not seen.

The authors mention that a limitation of the studywas that EMG recordings were taken primarily frommuscles involved in flexion and extension of the leg andhip, and not muscles that would be responsive to pertur-bations in the lateral direction, so they could notdescribe a ‘lateral synergy.’70 Thus, as a whole, the strategyrepresents the invariant aspect of the postural reactionsrelated to equilibrium control, whereas the muscle syn-ergies are partly fixed, partly flexible.

What makes the muscle synergies flexible? By com-paring the respective contribution of mono- and bi-articular muscles in postural control and in other tasks,van Ingen Schenau et al.71 indicated that the biarticularmuscles are sensitive to a large variety of peripheralinput and might tune the force vector provided by themonoarticular muscles in order to adapt it to the exter-nal constraints.

Adaptation of postural synergies

The above evidence suggests that the postural responsesynergies may be fine-tuned according to the task. Isthere also evidence for fine-tuning of postural responsesynergies in other situations? Research on humans indi-cates that there are changes in the muscle response para-meters within a synergy across successive trials,suggesting that the neuromuscular response synergiesmay be fine-tuned.1,72 It has been found, for example, that

Postural control in response to balance disturbances 11

the amplitude of ankle synergy movements activated byplatform rotations (described above) is progressivelyreduced over 10 trials because under these conditions thesway synergy is destabilizing, causing more sway than theperturbation itself. This change in amplitude has beentermed adaptation, since the response is fine-tuned to fita new task context.73

Additional research has indicated that with repeatedexposure to horizontal platform displacements, subjectsshow a reduction in the amplitude of antagonist anklemuscle responses, corresponding to smaller displace-ments of the body,72 as if the subjects were changing theirpostural set during the course of the experiment.

Sensory inputs contributing to the controlof perturbed stance

What are the relative contributions of the somatosensory,visual and vestibular systems to postural responses tosupport surface perturbations? Research performed byDietz and colleagues suggests that the contribution of thesomatosensory system is much greater than that of thevestibular system.74 In this study, muscle response ampli-tudes and onset latencies were compared for stance per-turbations of two types. The first perturbation consistedof forward and backward support surface movements,while the second perturbation consisted of a forward orbackward displacement of a load (2 kg) attached to thehead, stimulating the vestibular system (the response wasnot present in patients with vestibular deficits), but notankle joint somatosensory inputs. For comparable accel-erations, leg muscle responses elicited by the head pertur-bations were about 10 times smaller than the responsesinduced by the displacement of the feet. Since compara-ble accelerations were used for the two perturbations,Dietz et al.74 concluded that vestibular inputs play only aminor role in recovery of postural control when the sup-port surface is displaced horizontally.

Although vestibular inputs play a minor role in com-pensation for horizontal support surface displacements,they appear to be more important in compensating forperturbations in which the support surface is rotatedtoes-upward. This perturbation stretches and activatesthe gastrocnemius muscle, which destabilizes the subject,and a compensatory response in the tibialis anteriorserves to restore stability. It has been shown that thecompensatory response in the tibialis anterior muscle,used to restore balance, is activated by the visual andvestibular systems when the eyes are open. When theeyes are closed it is primarily (80 per cent) activated bythe vestibular semicircular canals.75

The above studies, examining postural control inresponse to transient horizontal perturbations to stance,suggest that neurologically intact adults tend to rely onsomatosensory inputs for the control of horizontal per-turbations to balance.

POSTURE CONTROL AND MOVEMENT

One of the main tasks in motor control is to orient thebody with respect to the external world. This orientationis necessary for the appropriate coding of the informa-tion collected by the sensory organs on the state of theenvironment. In this respect, the orientation of individ-ual segments and especially of head and trunk (see ref. 9)is critical.

Anticipatory postural adjustments

Anticipatory postural adjustments were first describedby Belen’kii and colleagues76 in association with armmovements, and since then many investigations in bothhumans and in cats have been devoted to exploring theirfunction, their central organization and their acquisi-tion.9,77 In their initial work, Belen’kii et al.76 showed thatwhen standing adults make rapid arm-raising move-ments, shorter latency postural responses are also acti-vated in the muscles of the legs. For example, responsesin the biceps femoris of the leg were activated 80–100 msafter the onset of the signal to start the movement com-pared with those for the prime mover of the arm(150–200 ms) and thus preceded the onset of the pri-mary mover muscle response by about 50 ms. These pos-tural adjustments act to compensate in advance forchanges in posture and equilibrium caused by the move-ment. This view on the function of the anticipatory pos-tural adjustments was also proposed by Cordo andNashner39 and by Bouisset and Zattara.78,79

Are the muscle synergies observed in postural reac-tions also ‘utilized’ for anticipatory postural adjustments?In one set of experiments by Cordo and Nashner39 stand-ing subjects were asked to make a rapid arm flexionmovement. As in the studies of Gurfinkel and his col-leagues, it was found that postural responses occurred inthe muscles of the leg in advance of the prime movermuscles of the arm. It is of interest that the same muscleresponse organization which was previously found to sta-bilize posture after an external threat to balance (gastroc-nemius, hamstrings and trunk extensors) was used tostabilize posture before activation of the prime movermuscle (biceps) in the arm flexion task.39

An important characteristic of postural adjustmentsassociated with movement is their adaptability to taskconditions.80 For example, in the experiments describedabove,39 when the subjects leaned forward against a hori-zontal bar at chest height, thus stabilizing the trunk andeliminating the need for postural adjustments in the legs,the leg postural adjustments were reduced or disap-peared. This suggests that there is a preselection of thepostural muscles to be used in anticipatory adjustments,as a function of their ability to contribute appropriatesupport.39


GOAL OF THE ANTICIPATORY POSTURAL ADJUSTMENTS

Is the goal of the anticipatory postural adjustment tocontrol balance or posture (i.e. the center of gravity andthe center of pressure position during movement, or,alternatively, the position or orientation of given bodysegments)? One should remember that voluntary move-ment perturbs posture and/or equilibrium for two rea-sons. First, the performance of a movement of the armor the trunk while standing changes the body geometryand thus displaces the center of gravity position, result-ing in equilibrium disturbance. The second reason is thatthe internal muscular forces that are at the origin of themovement are accompanied by reaction forces acting onthe supporting body segments and will tend to displacethem. This will disturb both the position of these seg-ments and equilibrium.

In many tasks (for example arm raising while stand-ing) the anticipatory postural adjustments serve to con-trol balance and to stabilize posture. However, for othertasks, such as trunk bending or bimanual load-liftingtasks, two types of anticipatory postural adjustments canbe identified with respect to their goal, those aimed atstabilizing the center of gravity during movement and

those aimed at stabilizing the position of body segments.A third goal of the anticipatory postural adjustments isto provide the dynamic support of the postural chainfrom the ground to the moving segments in order toimprove the performance in terms of force or velocity.

Bouisset and Le Bozec81 and Bouisset et al.82 intro-duced the concept of ‘posturokinetic capacity’ as anassessment of the capacity of the postural chain to assistthe movement. This capacity is related to the control ofthis chain for counteracting the reaction forces associ-ated with movement performance and also for dynami-cally contributing to the movement force and velocityusing the many degrees of freedom from the ground tothe moving segments.83,84

AN EXAMPLE OF ANTICIPATORY POSTURALADJUSTMENT: THE BIMANUAL LOAD-LIFTING TASK

The stabilization of the position or orientation of bodysegments85,86 is exemplified by the bimanual load-liftingtask. This type of stabilization can be seen independentlyfrom the control of the center of gravity during biman-ual tasks, when one arm is used to stabilize or hold anobject and the other is used to manipulate or lift the

Posture control and movement 13

Figure 1.5 Comparison between imposed and voluntary unloading in a normal subject (average of 20 trials). (a) Force trace recordedfrom a force platform (F) during unloading of 1 kg weight imposed by the experimenter. Elbow angle was measured by apotentiometer at the elbow joint axis (P). Note the upward rotation. The integrated electromyograph of the brachioradialis showed areduction of activity after a latency of 30 ms (unloading reflex). (b) Voluntary unloading. Note the reduced elbow rotation, the‘anticipatory’ inhibition of the brachioradialis, time locked with the activation of the biceps of the voluntary arm.

object. For example, during a bimanual load-lifting task,where one forearm was maintained horizontal and sup-ported a 1 kg load, and the other hand lifted the load, theforearm position did not change during unloading (Fig.1.5). This was because of an inhibition of the elbow flexors of the postural forearm, which preceded the onsetof unloading by a short period. This anticipatory pos-tural adjustment was correlated with the onset of thebiceps activation of the lifting arm and minimized theforearm disturbance which should normally occur, andis seen when unloading is caused by the experimenter. Asimilar type of anticipatory postural adjustment is seento stabilize ‘grip force’ in advance of a disturbance87 or tominimize the mechanical impact of a hammer manipu-lated by the subject to test the tendon reflex of the otherarm’s triceps.88

An insight into the central organization of the antici-patory postural adjustments during bimanual load-lift-ing tasks was provided by testing the task in patients.89 Itrevealed that the anticipatory postural adjustmentsremained unchanged after callosal section. This suggeststhat the control of these adjustments did not occurthrough a direct callosal connection between the cortexcontrolling the moving side and the cortex controllingthe postural side, but by a subcortical connectionbetween the cortex responsible for the movement andthe networks responsible for the anticipatory posturaladjustment.

Moreover, anticipatory postural adjustments wereimpaired after a cortical lesion extending to the supple-mentary area region or to the motor cortex. As theimpairment occurred for lesions contralateral to the pos-tural forearm (and not to the moving arm), the authorsconcluded that the anticipatory postural adjustment net-works were under the control of these contralateral cor-tical areas. It is suggested that the role of these networksis to select the segments utilized as a reference frame forthe movement and to gate on the appropriate networkfor stabilizing the corresponding postural segment dur-ing the movement.

Further investigations on the central organization ofanticipatory postural adjustments are crucial for theunderstanding of the neurological deficit specificallyrelated to their dysfunctioning.

How is the control organized?

A main difficulty for understanding postural control isthe complexity of the biomechanical constraints under-lying human posture. The body is supported by a narrowsupport base, where the action and reaction forces takeplace. The body is a multi-joint chain, which includessegments of different mass and inertia, linked by muscleswith their visco-elastic characteristics. Each single jointmovement is associated with dynamic interaction withother segments of the chain; these movements change

the impact of external forces such as gravity on the bodysegments, thus complicating the regulation of posture.

One main concern for understanding the control is tofind out how a reduction of the number of degrees offreedom can be achieved in order to simplify the con-trol.29 The multi-joint chain is not specific to posture;thus, in this respect, the problems of control are com-mon to that of any multi-joint movement. The specificaspect of posture in this control is related to the need tocontrol balance and/or the body segment orientationduring the motor act.

A first concept regarding simplifying control is that of‘reference posture’. This concept is in line with the equi-librium point theory of Bizzi et al.90 and the lambdamodel of Feldman and Levin,91 and related to the spring-mass properties of the musculo-skeletal system.

In the development of the lambda model, it was pro-posed that the critical threshold length for each muscle(which is the threshold for the myotatic reflex) is set inorder to define a given reference postural configuration.91

The control of a referent posture would consist in settingthe critical length for the whole set of body muscles at anappropriate value. This concept is attractive due to itsrelative simplicity and meets a number of observations.For example, forward and backward trunk bendings areaccompanied by opposite displacements of lower bodysegments and as a result the center of gravity positionremains inside the support surface.92 This kinematic syn-ergy with a strong coupling between segment angles43,93

remains under microgravity conditions94 and seems to bea behavioral invariant, independent of external con-straints, as would be expected from the referent posturehypothesis. If the kinematic pattern is invariant, theEMG patterns do adapt to the constraint. As proposed byBabinski,95 the coordination between equilibrium andmovement, as revealed by the study of upper trunkmovements, seems to be under the control of the cere-bellum.96 It is not yet clear how far this model is able toaccount for the dynamic interaction between segmentswhich disturbs movement performance and balance.

The inverse dynamic model was proposed by Ito97 andby Gomi and Kawato;98,99 it implies that an internal modelof the body segments kinematics and dynamics doesexist. When performing a goal-directed movement,the dynamical interactions between segments which disturb the trajectory have to be compensated. A feed-forward inverse dynamic model is built up which correctsin advance for these dynamic interactions. The cerebel-lum would be the site where the inverse model is stored.As the dynamic interactions between segments are amajor source of balance disturbance during movement,one might think that the inverse model would accuratelycontrol balance during movement performance.

A third possibility for postural control during move-ment is derived from the observation on hip and anklestrategies for restoring balance.65 The hip and anklestrategies are considered as basic multi-joint movement


units of the biomechanical system which can be scaledboth in terms of kinematics and kinetics.100,101 In a tasksuch as trunk bending, one is used for performing themovement (hip synergy), the other for balance control(ankle synergy) by accelerating the CG forward, in anopposite direction to the CG acceleration resulting fromthe hip flexion. Thus, two parallel controls would be pre-sent, one responsible for the movement, the other for theanticipatory postural adjustment.

LEG MOVEMENTS

Movements of the legs are a source of disturbance of bal-ance because they take part in body support; thus a dis-placement of the center of gravity is observed precedingleg movement onset to compensate for this disturbance.The center of gravity shift occurs, for example, duringthe initiation of gait, standing on tip-toes or on the heels,or raising one leg.8,102–104

The neural control by which the center of gravity shiftstoward a new position compatible with equilibrium dur-ing movement, is clearly different from the neural controlresponsible for the anticipatory position adjustmentwhich prevents center of gravity displacement duringmovement such as occurs during upper trunk bending. Itcan be compared to a goal-directed movement except thatthe goal is expressed not in terms of geometry (object inspace) but in terms of forces (new center of gravity position). This type of control is related to equilibriumconstraints and disappears under microgravity condi-tions.105 Its central organization in humans is still an openquestion. However, ablation experiments in quadrupedsperforming leg-raising tasks suggests that this type ofcontrol is highly dependent on motor cortical areas.106

Integrating postural responses into thestep cycle

Studies on the control of balance during unperturbedgait suggest that this task is very different from the taskof balance control during stance.107 During walking, thecenter of gravity moves outside the base of support ofthe feet and thus creates a continuous state of imbalance.Falling is prevented by placing the swinging foot aheadof and lateral to the center of gravity as it moves forward(see Chapter 4).

A key aspect of balance during locomotion is the con-trol of the mass of the head, arms and trunk (the HATsegment) with respect to the hips, since this is a largeload to keep upright. It has been hypothesized by Winterand colleagues108 that the dynamic balance of the head,arms and trunk is controlled by the hip muscles, withalmost no involvement of the ankle muscles. They sug-gest that this type of control is more efficient since thehip has a much smaller inertial load to control (that ofthe HAT segment) than the ankles, which would have tocontrol the entire body.

Although balance control during unperturbed gaitappears to be controlled by hip musculature, compensa-tions for balance perturbations during gait have beenshown to be controlled primarily by responses in theankle and thigh musculature.109–111 In experiments inwhich the balance of young adults was disturbed at dif-ferent points within the stance phase of gait, it wasshown that the young adult elegantly modulates posturalresponse organization primarily in the leg and thighmuscles to compensate for disturbances.

Thus, when the foot slipped forward at heel-strike,which slowed forward momentum of the body, aresponse was elicited in anterior bilateral leg muscles(tibialis anterior) as well as anterior and posterior thighmuscles. These muscles showed early (90–140 ms), highmagnitude (four to nine times the activity in normalwalking) and relatively long-duration bursts.111 Althoughproximal hip muscle activity was often present duringthe first slip trial in young adults, it tended to adapt awayduring subsequent trials. As shown previously for recov-ery of balance during quiet stance, muscle response pat-terns to balance threats during walking were activated ina distal to proximal sequence.

CONCLUSIONS

Postural or equilibrium control is considered to be thefoundation for voluntary skills, because almost everymovement that an individual makes is made up of both(1) postural components, which stabilize the body and(2) the prime mover components which relate to a par-ticular movement goal.

The task of postural control involves the maintenanceof the alignment of body posture, of stability, or bodilyorientation to the environment and also serves as amechanical support for action.

Postural tone depends on and is modulated throughthe myotatic reflex loop, tonic labyrinthine reflexes, thetonic neck refl

clinical disorders oforthoteb.com/upload/56122720318886269411605002422clinical... · 2016-07-29 ·...

Documents