HUMAN GROWTH 3 Neurobiology and Nutrition

HUMAN GROWTH

Volume I Principles and Prenatal Growth

Volume 2 Postnatal Growth

Volume 3 Neurobiology and Nutrition

HUMAN GROWTH 3 Neurobiology and Nutrition Edited by

Frank Falkner The Fels Research Institute Wright State University School of Medicine Yellow Springs, Ohio

and

J.M. Tanner Institute of Child Health London, England

PLENUM PRESS· NEW YORK AND LONDON

Library of Congress Cataloging in Publication Data

Main entry under title:

Human growth.

Includes bibliographies and index. CONTENTS: v. 1. Principles and prenatal growth. - v. 2. Postnatal growth. - v. 3.

Neurobiology and nutrition. 1. Human growth-Collected work. I. Falkner, Frank Tardrew, 1918- II. Tanner,

James Mourilyan. [DNLM: 1. Growth. 2. Gestational age. WS103 H918] QP84.H76 612'.3 78-1440

ISBN-13:978-1-4684-0819-5 e-ISBN-13:978-1-4684-0817-1

DOl: 10.1007/978-1-4684-0817-1

© 1979 Plenum Press, New York Softcover reprint of the hardcover 18t edition 1979

A Division of Plenum Publishing Corporation 227 West 17th Street, New York, N.Y. 10011

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

Contributors

H.ALS Child Development Unit Harvard University Medical School Boston, Massachusetts

ROBERT BALAzs MRC Developmental Neurobiology

Unit Institute of Neurology London, England

KARL E BERGMANN Department of Pediatrics J. W. Goethe University Frankfurt/Main, West Germany

RENATE L. BERGMANN Department of Pediatrics J. W. Goethe University Frankfurt/Main, West Germany

INGEBORG BRANDT U niversitatats-Kinderklinik und

Poliklinik Bonn, Germany

T. B. BRAZEL TON Child Development Unit Harvard University Medical School Boston, Massachusetts

GEORGE F. CAHILL, JR. Joslin Diabetes Foundation, Inc. The Peter Bent Brigham Hospital and

Harvard Medical School Boston, Massachusetts

JOAQuiN CRA VIOTO Instituto Nacional de Ciencias y

Tecnologfa de la Salud del Nino Sistema Nacional para el Desarrollo

Integral de la Familia (DIF) Mexico City, Mexico

ELSA R. DELICARDIE Rural Research and Training Center Instituto N acional de Ciencias y

Tecnologfa de la Salud del Nino Sistema N acional para el Desarrollo

Integral de la Familia (DIF) Mexico City, Mexico

C. DREYFUS-BRISAC Centre de Recherches de Biologie du

Developpement Foetal et Neonatal H6pital Port Royal U niversite Rene Descartes Paris, France

PHYLLIS B. EVELETH Division of Research Grants National Institutes of Health Bethesda, Maryland

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vi

CONTRIBUTORS

CHRISTINE GALL Department of Psychobiology University of California Irvine, California

DERRICK B. JELUFFE Division of Population, Family and

International Health School of Public Health University of California Los Angeles, California

E. F. PATRICE JELUFFE Division of Population, Family and

International Health School of Public Health University of California Los Angeles, California

PAUL D. LEWIS Department of Histopathology Royal Postgraduate Medical School Hammersmith Hospital London, England

GARY LYNCH Department of Psychobiology University of California Irvine, California

PAMELA C. B. MACKINNON University of Oxford Oxford, England

LAURENCE MALCOLM Health Planning and Research Unit Christchurch, New Zealand

AMBRISH J. PATEL MRC Developmental Neurobiology

Unit Institute of Neurology London, England

T. RABINOWICZ Division of Neuropathology Centre Hospitalier U niversitaire Vaudois Lausanne, Switzerland

ALDO A. ROSSINI Joslin Diabetes Foundation, Inc. The Peter Bent Brigham Hospital and

Harvard Medical School Boston, Massachusetts

F. J. SCHUL TE University of G6ttingen G6ttingen, West Germany

J. P. SCOTT Center for Research on Social

Behavior Bowling Green State University Bowling Green, Ohio

J. M. TANNER Department of Growth and

Development Institute of Child Health University of London London, England

COL WYN TREVARTHEN University of Edinburgh Edinburgh, Scotland

E TRONICK Department of Psychology University of Massachusetts Amherst, Massachusetts

Preface

Growth, as we conceive it, is the study of change in an organism not yet mature. Differential growth creates form: external form through growth rates which vary from one part of the body to another and one tissue to another; and internal form through the series of time-entrained events which build up in each cell the special­ized complexity of its particular function. We make no distinction, then, between growth and development, and if we have not included accounts of differentiation it is simply because we had to draw a quite arbitrary line somewhere.

It is only rather recently that those involved in pediatrics and child health have come to realize that growth is the basic science peculiar to their art. It is a science which uses and incorporates the traditional disciplines of anatomy, physiology, biophysics, biochemistry, and biology. It is indeed a part of biology, and the study of human growth is a part of the curriculum of the rejuvenated science of Human Biology. What growth is not is a series of charts of height and weight. Growth standards are useful and necessary, and their construction is by no means void of intellectual challenge. They are a basic instrument in pediatric epidemiology. But they do not appear in this book, any more than clinical accounts of growth disorders.

This appears to be the first large handbook-in three volumes-devoted to Human Growth. Smaller textbooks on the subject began to appear in the late nineteenth century, some written by pediatricians and some by anthropologists. There have been magnificent mavericks like D' Arcy Thompson's Growth and Form. In the last five years, indeed, more texts on growth and its disorders have appeared than in all the preceding fifty (or five hundred). But our treatise sets out to cover the subject with greater breadth than earlier works.

We have refrained from dictating too closely the form of the contributions; some contributors have discussed important general issues in relatively short chapters (for example, Richard Goss, our opener, and Michael Healy); others have provided comprehensive and authoritative surveys of the current state of their fields of work (for example, Robert Balazs and his co-authors). Most contributions deal with the human, but where important advances are being made although data from the human are still lacking, we have included some basic experimental work on animals.

Inevitably there are gaps in our coverage, reflecting our private scotomata, doubtless, and sometimes our judgment that no suitable contributor in a particular field existed, or could be persuaded to write for us (the latter only in a couple of instances, however). Two chapters died on the hoof, as it were. Every reader will

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PREFACE

notice the lack of a chapter on ultrasonic studies of the growth of the fetus; the manuscript, repeatedly promised, simply failed to arrive. We had hoped, also, to include a chapter on the very rapidly evolving field of the development of the visual processes, but here also events conspired against us. We hope to repair these omissions in a second edition if one should be called for; and we solicit correspon­dence, too, on suggestions for other subjects.

We hope the book will be useful to pediatricians, human biologists, and all concerned with child health, and to biometrists, physiologists, and biochemists working in the field of growth. We thank heartily the contributors for their labors and their collective, and remarkable, good temper in the face of often bluntish editorial comment. No words of praise suffice for our secretaries, on whom very much of the burden has fallen. Karen Phelps, at Fels, handled all the administrative arrangements regarding what increasingly seemed like innumerable manuscripts and rumors of manuscripts, retyped huge chunks of text, and maintained an unruffled and humorous calm through the whole three years. Jan Baines, at the Institute of Child Health, somehow found time to keep track of the interactions of editors and manuscripts, and applied a gentle but insistent persuasion when any pair seemed inclinded to go their separate ways. We wish to thank also the publishers for being so uniformly helpful, and above all the contributors for the time and care they have given to making this book.

Yellow Springs and London

Frank Falkner James Tanner

Contents

Vl Neurobiology

Chapter 1

Neuroembryology and the Development of Perception

Colwyn Trevarthen

1. Introduction .................................................... 3 2. Innate Strategy of Perceptual Systems ............................. 5 3. Early Embryo. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11 4. Late Embryos and Lower Vertebrates ............................. 21 5. The Fetus: Reptiles, Birds, and Mammals. . . . . . . . . . . . .. . . .. .. . . .. . . 33 6. Late Fetus, Birth, and Infancy ...... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43 7. Conclusions..................................................... 73 8. References...................................................... 79

Chapter 2

The Differentiate Maturation of the Human Cerebral Cortex

T. Rabinowicz

1. Introduction .................................................... 97 2. Material and Methods. .. .. .. .. . . .. .. .. .. .. . . .. .. .. .. .. . . .. .. .. . . . 98 3. Frontal Lobe.. . . . .. . . . . . . .. .. . .. . .. . . .. . . . . . .. . . . . .. . . . . . .. . . .. . 98 4. Parietal Lobe ................................................... 107 5. Temporal Lobe.. . . . . .. . . .. . . . . . . .. .. .. . . . . .. . . . . . . . . . . . . . . . . . . .. 110 6. Occipital Lobe .................................................. 115 7. Limbic Lobe. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 119 8. General Considerations. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 121 9. References...................................................... 122

Chapter 3

Organization and Reorganization in the Central Nervous System: Evolving Concepts of Brain Plasticity

Gary Lynch and Christine Gall

1. Introduction .................................................... 125 2. Effects of Experience and Environment on the "Molar" Composition of

the Brain ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 126

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x CONTENTS

3. Reorganizing the Anatomy of the Developing Brain. . . . . . . . . . . . . . . . .. 127 4. Anatomical Plasticity in the Adult Brain . . . . . . . . . . . . . . . . . . . . . . . . . . .. 131 5. Discussion...................................................... 138 6. References...................................................... 141

Chapter 4

Developmental Aspects of the Neuronal Control of Breathing

F. J. Schulte

1. Brain Stem Respiratory Neurons .................................. 145 2. Chemoreceptor Regulation of Breathing. . . . . . . . . . . . . . . . . . . . . . . . . . .. 147 3. Mechanoreceptor Regulation of Breathing .......................... 148 4. Patterns of Fetal and Neonatal Respiration ......................... 149 5. Brain Mechanisms Responsible for the Preterm Infant's Difficulties in

Breathing: A Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 153 6. References...................................................... 154

Chapter 5

Ontogenesis of Brain Bioelectrical Activity and Sleep Organization in Neonates and Infants

C. Dreyfus-Brisac

1. Introduction .................................................... 157 2. EEG and Sleep of Full-Term Neonates. . . . . . . . . . . . . . . . . . . . . . . . . . . .. 159 3. EEG and Sleep of Preterm Infants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 164 4. Development of EEG and Sleep Organization during the First Three

Years of Life ................................................... 169 5. Conclusions..................................................... 175 6. References...................................................... 176

Chapter 6

Sexual Differentiation of the Brain

Pamela C. B. MacKinnon

1. Introduction .................................................... 183 2. Evidence for Sexual Differentiation of the Brain in Nonprimates . . . . . .. 185 3. Evidence for Sexual Differentiation of the Brain in Primates .......... 205 4. Differentiation of the Female Brain ................................ 210 5. Summary and Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 210 6. References...................................................... 212

Chapter 7

Critical Periods in Organizational Processes

J. P. Scott

1. Introduction .................................................... 223 2. Physical Growth and Behavioral Development-A Comparison ....... 223

3. Theory of Organizational Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 225 xi 4. Critical Periods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 226 5. General Theory of Critical Periods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 231 CONTENTS

6. Optimal Periods and Critical Periods .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 234 7. Vulnerable and Sensitive Periods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 238 8. Conclusion ..................................................... 238 9. References.... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 239

Chapter 8

Patterns of Early Neurological Development

Ingeborg Brandt

1. Introduction .................................................... 243 2. Survey of Methods .............................................. 245 3. Development.................................................... 250 4. Value for Determination of Postmenstrual Age: A Critical Evaluation.. 293 5. Prognostic Value ................................................ 298 6. References...................................................... 300

Chapter 9

Early Development of Neonatal and Infant Behavior

E. Tronick, H. Als, and T. B. Brazelton

1. Introduction .................................................... 305 2. Intrauterine Psychological Capabilities ............................. 306 3. Behavior of the Premature Infant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 306 4. Behavior of the Newborn. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 307 5. Modal Newborn Behavioral Development during the Neonatal Period.. 317 6. Behavior of the Infant in Context: The Infant-Adult Communication

System. .. .. .. .. .. .. .. .... .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 323 7. Summary....................................................... 325 8. References...................................................... 325

VII. Nutrition

Chapter 10

Nutrition and Growth in Infancy

Renate L. Bergmann and Karl E. Bergmann

1. Introduction .................................................... 331 2. Food Intake and Growth of Normal Infants under Controlled Conditions 331 3. Interrelationship of Growth and Nutritional Requirements: Model

Considerations .................................................. 350 4. Adverse Effects of Deficient or Excessive Intake of Some Nutrients on

Infant Growth. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 353 5. Summary and Conclusions.. . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . ... 357 6. References...................................................... 357

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CONTENTS

Chapter 11

Protein-Energy Malnutrition and Growth

Laurence Malcolm

1. Introduction .................................................... 361 2. Prenatal Growth. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 361 3. Early Postnatal Growth .......................................... 362 4. School Age to Maturity .......................................... 364 5. Development of Secondary Sex Characteristics. . . . . . . . . . . . . . . . . . . . .. 367

16. Skeletal Development. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 367 . 7. Dental Development ............................................. 368 8. Body Proportions. . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 369 9. Conclusion and Summary. . . . . . . .. . . . . . . . . . . . . . . . . .. . . . . .. . . . . .. .. 370

10. References...................................................... 371

Chapter 12

Population Differences in Growth: Environmental and Genetic Factors

Phyllis B. Eveleth

1. Introduction .................................................... 373 2. Population Differences in Body Size ............................... 374 3. Population Differences in Body Shape. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 379 4. Differences in Amount of Subcutaneous Fat ........................ 381 5. Skeletal Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 382 6. Sexual Maturation .................. , . . . . .. . . .. . . .. . . . . . . . . . . . . .. 384 7. Dental Maturation .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 386 8. Summary and Generalization. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 387 9. References...................................................... 388

Chapter 13

Epidemiological Considerations

Derrick B. lelliffe and E. F. Patrice lelliffe

1. Introduction: Interrelationships of Growth and Epidemiology ......... 395 2. Community Diagnosis and Practical Programs. . . . . . . . . . . . . . . . . . . . . .. 400 3. Nutritional Surveillance and Conclusions ........................... 404 4. References...................................................... 404

Chapter 14

Obesity

George F. Cahill, lr., and Aldo A. Rossini

1. Introduction .................................................... 407 2. Adipose Tissue. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 408 3. The Fat Cell. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 408 4. The Fat Mass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 409 5. Adipose Tissue Distribution. . . . . .. . . .. . . . . . . . . . . .. . . . . . . .. . . . . . . .. 410 6. Adipocyte Number .............................................. 410 7. Nutrition and Adipocyte Number and Size .......................... 411

8. Treatment ...................................................... 412 9. References...................................................... 412

Chapter 15

Nutritional Deficiencies and Brain Development

Robert Ba16zs, Paul D. Lewis, and Ambrish J. Patel

1. Introduction .................................................... 415 2. Some Comments on Methods ..................................... 416 3. Effect of Undernutrition on Cell Acquisition in the Brain. . . . . . . . . . . .. 416 4. Effect of Undernutrition on Brain Maturation. . . .. . . . . . . . . . . . . . . . . .. 434 5. Effects of Vitamin Deficiencies on Brain Growth .................... 455 6. Functional Consequences. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 462 7. References...................................................... 464

Chapter 16

Nutrition, Mental Development, and Learning

Joaquin Cravioto and Elsa R. DeLicardie

1. Introduction .................................................... 481 2. Some Problems Involved in the Assessment of the Role of Malnutrition 483 3. Sensory-Motor Development in Malnourished Infants. .. . . . . . . . . . . . .. 484 4. Early Malnutrition and Intelligence at School Age ................... 485 5. Early Malnutrition and Intersensory Organization.. . . . . . . . . .. .. . . . . .. 491 6. Visual Perception. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 497 7. Language Development .......................................... 497 8. Styles of Response to Cognitive Demands .......................... 500 9. Influence of Age and Duration of Malnutrition on Later Performance .. 503

10. Mechanisms of Action of Malnutrition ............................. 505 11. References...................................................... 508

VIII. History of Growth Studies

Chapter 17

A Concise History of Growth Studies from Buffon to Boas

J. M. Tanner

1. Buffon and the First Growth Study. . . . .. . . . . . . . . . . . . . . . . . . . . . . . . .. 515 2. Schiller and the Carlschule ....................................... 520 3. Goethe and the Recruiting Officers ................................ 524 4. Quetelet and the Mathematics of Growth ..... . . . . . . . . . . . . . . . . . . . . .. 526 5. Chadwick, Horner, and Villerme: The Beginning of Auxological Epidemi-

ology .......................................................... 535 6. Roberts, Galton, and Bowditch: Social Class and Family Likeness. . . .. 549 7. Educational Auxology: School Surveys and School Surveillance. . . .. .. 561 8. Franz Boas and D'Arcy Thompson ................................ 576 9. Coda ........................................................... 587

10. References................... . . . . . . . . .. . . . . .. . . . . . . . . .. . . . . . . . .. 587

Index .............................................................. 595

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CONTENTS

Volume 1

Contents of Volumes 1 and 2

I. Developmental Biology

1. Adaptive Mechanisms of Growth Control

Richard J. Goss

2. Human Biochemical Development

Gerald E. Gaul!, Fritz A. Hommes, and Jacques F. Raux

3. Developmental Pharmacology

Charlotte Catz and Sumner J. Yaffe

4. Glimpses of Comparative Growth and Development

R. A. McCance and Elsie M. Widdowson

II. Biometrical Methods in Human Growth

5. Statistics of Growth Standards

M. J. R. Healy

6. Sampling for Growth Studies

Harvey Goldstein

7. The Mathematical Handling of Long-Term Longitudinal Data

Ettore Marubini

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CONTENTS OF VOLUMES 1 AND 2

III. Genetics

8. Introduction to Genetic Analysis

Jean Ff"{!zal and Catherine Bonai'ti-Pellie

9. The Genetics of Human Fetal Growth

D. F. Roberts

10. The Genetics of Birth Weight

Elizabeth B. Robson

11. The Genetics of Adult Stature

C. O. Carter and W. A. Marshall

12. The Genetics of Maturational Processes

Stanley M. Garn and Stephen M. Bailey

IV. Prenatal Growth

13. Anatomy of the Placenta

Douglas R. Shanklin

14. Physiology of the Placenta

Joseph Dancis and Henning Schneider

15. Fetal Measurements

D. A. T. Southgate

16. Implications for Growth in Human Twins

Frank Falkner

17. Association of Fetal Growth with Material Nutrition

Jack Metcoff

18. Carbohydrate, Fat, and Amino Acid Metabolism in the Pregnant Woman and Fetus

Peter A. J. Adam and Philip Felig

19. Pre- and Perinatal Endocrinology

Pierre C. Sizonenko and Michel L. Aubert

20. Development of Immune Responsiveness

A. R. Hayward

21. Fetal Growth: Obstetric Implications

Karlis Adamsons

Volume 2

V. Postnatal Growth

1. Cellular Growth: Brain, Liver, Muscle, and Lung

Jo Anne Brasel and Rhoda K. Gruen

2. Cellular Growth: Adipose Tissue

C. G. D. Brook

3. The Methods of Auxological Anthropometry

Noel Cameron

4. Somatic Growth of the Infant and Preschool Child

Francis E. Johnston

5. Body Composition and Energy Needs during Growth

Malcolm A. Holliday

6. Puberty

W. A. Marshall

7. Prepubertal and Pubertal Endocrinology

Jeremy S. D. Winter

8. The Central Nervous System and the Onset of Puberty

Melvin M. Grumbach

9. Body Composition in Adolescence

Gilbert B. Forbes

10. Growth of Muscle Tissue and Muscle Mass

Robert M. Malina

11. Adipose Tissue Development in Man

Jerome L. Knittle

12. Bone Growth and Maturation

Alex F. Roche

13. The Fundamentals of Cranial and Facial Growth

Harry Israel, III

14. Skull, Jaw, and Teeth Growth Patterns

Patrick G. Sullivan

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CONTENTS OF VOLUMES 1 ANO 2

xviii

CONTENTS OF VOLUMES 7 AND 2

15. Dentition

Arto Demirjian

16. Secular Growth Changes

1. C. van Wieringen

17. The Influence of Exercise, Physical Activity, and Athletic Performance on the Dynamics of Human Growth

Donald A. Bailey, Robert M. Malina, and Roy L. Rasmussen

18. The Low-Birth-Weight Infant

Frederick C. Battaglia and Michael A. Simmons

19. Growth Dynamics of Low-Birth-Weight Infants with Emphasis on the Perinatal Period

Ingeborg Brandt