Development of Normal Fetal Movements: The First 25 Weeks of Gestation

Development of Normal Fetal Movements

Alessandra Piontelli

Development of Normal Fetal Movements The First 25 Weeks of Gestation

13

ALESSANDRA PIONTELLI Department of Maternal/Fetal Medicine Clinica Mangiagalli University of Milan Milan, Italy E-mail: [email protected]

With the assistance of: Luisa Bocconi, Chiara Boschetto, Elena Caravelli, Florinda Ceriani, Isabella Fabietti, Roberto Fogliani, Alessandra Kustermann, Umberto Nicolini✝, Sarah Salmona, Beatrice Tassis, Laura Villa, Cinzia Zoppini. Department of Maternal/Fetal Medicine, University of Milan, Clinica Mangiagalli - Fondazione IRCCS Ca’ Granda, Ospedale Maggiore, Policlinico di Milano, Italy

ISBN 978 88 470 1401 5

e ISBN 978 88 470 1402 2

DOI 10.1007/978 88 470 1402 2 Library of Congress Control Number: 2010923295 © Springer Verlag Italia 2010 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in databanks. Duplication of this publication or parts thereof is permitted only under the provisions of the Italian Copyright Law in its current version, and permission for use must always be obtained from Springer. Violations are liable to prosecution under the Italian Copyright Law. The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Product liability:The publishers cannot guarantee the accuracy of any information about dosage and application contained in this book. In every individual case the user must check such information by consulting the relevant literature. Cover illustration: Ikona S.r.l., Milan, Italy Typesetting: Ikona S.r.l., Milan, Italy Printing and binding: Grafiche Porpora S.r.l., Segrate, Milano Printed in Italy Springer Verlag Italia S.r.l. Via Decembrio 28 I 20137 Milan Springer is a part of Springer Science+Business Media

To my mother and to all our mothers

Preface

This work sees the light for various reasons. There is a general lack of detailed information about the earliest stages of human motor development. The reasons for this are explained more fully in the Introduction; here we may simply state that, apart from their intrinsic interest, earlier phenomena are fundamental to the comprehension of later phenomena rooted in them, whether pathological or normal. This is especially so in the rapidly developing young organism. At birth the neonate is catapulted into a profoundly different physical and social environment requiring extremely diverse functioning: suffice it to mention aerial respiration, no longer being fed through the placenta and the cord, and the full impact of gravity on neonatal movements. The neonate generally adapts smoothly to the transition, as it has been equipped to do so during the 9 months of pregnancy. However, the study of the early stages of fetal motor development should not be exclusively directed towards the understanding of functioning in the neonate. Fetuses undergo constant and very rapid changes throughout pregnancy. Equally, the intrauterine environment varies continuously. The young organism is continually reshaped in more or less subtle ways and its functions modify, develop, become redundant or are incorporated almost beyond recognition into subsequent ones. Fetuses are perfectly adapted to each step of their rapid development. Only some functions are fully and wholly anticipatory and uniquely geared toward postnatal life. In other words, at any given gestational age fetuses are to be considered in themselves and in relation to their environmental conditions. On this basis, preparatory or mixed functions and their evolution can be teased out. Besides trying to bring to light a severely neglected topic, some other reasons motivated me to write this work. Relatively recent technologies such as 4D ultrasonography once seemed to hold the promise to revolutionize fetal studies; however, 4D ultrasound produces not real-time images, but computerized reconstructions of the fetus in motion. As such, it fails to capture essential features of most fetal movements. On the other hand, 4D ultrasound does offer some sensational and easily readable images. Researchers with little or no experience in the field are increasingly drawn to the 4D technique by its deceptive accessibility and apparent ease of interpretation. This often results in far-fetched conclusions being reached over very thin ice. In a few years’ time new technologies will certainly bring about a true revolution in fetal studies. However, future studies will also always require a thorough basic knowledge of fetal functioning and how it changes. For the moment this basic knowledge can only be acquired by dipping into a mixture of techniques, using the best each has to offer. With the recent invasion of ultrasound pictures, and ‘special effects’ images which have been totally artificially constructed, fetuses and their behaviour and development are often referred to as ‘wonders of nature’. Almost nothing makes us feel that we are witnessing

VII

Preface

a miracle of nature like watching a new life unfold. Others regard the miracle of life as a gift from God. This latter stance, legitimate as it may be, belongs to religion, not to the study of nature. The sense of wonder, whether based upon compelling religious beliefs or sentimental and emotional reactions, impinges strongly on society’s attitudes, on decisions about the fetus, and ultimately on the lives of many women deemed to be mere containers of the ‘miraculously’ unfolding life. Fetal behaviour is fascinating, but it can be analysed. By relying on observational data, this work hopes to re-establish a balance in favour of evidence. Having spent many years working in this field I felt that the time had come to gather together all the accumulated knowledge about the first 25 weeks of pregnancy, the time span on which I have always focused my attention. My professional background is somewhat multi-faceted. After graduating in medicine I specialized in psychiatry and neurology, trained amongst other things as a ‘baby-watcher’ following the principles of ethology in England, but then went back to medicine and, albeit not formally, became an expert in obstetrics and fetal behaviour by pursuing my research in the main maternity hospital in Italy, my native country, for almost 20 years. By propounding a fresh look at our first movements and the rapid changes they undergo, I hope to elicit renewed interest in the reader in this vastly unexplored but fascinating field. I also hope this will result in further research bringing about true advances in our still rudimentary understanding of this neglected area of knowledge. Milan, April 2010

Alessandra Piontelli

Acknowledgements

The help and support of many individuals were critical in making this work a reality. These include former and current staff, students, and nurses of the Department of Maternal Fetal Medicine at the Clinica Mangiagalli of the University of Milan. I am greatly indebted to Professor Fedele for allowing me full access to the Clinic. This book could not have seen the light of day without the help and the teachings of the late Umberto Nicolini, of Alessandra Kustermann, and of, in alphabetical order: Stefano Acerboni, Luisa Bocconi, Chiara Boschetto, Elena Caravelli, Florinda Ceriani, Isabella Fabietti, Roberto Fogliani, Leo Gallo, Sarah Salmona, Beatrice Tassis, Laura Villa, and Cinzia Zoppini. Most of these persons will be further acknowledged in each chapter for helping me collect the material and for independently reviewing it. Thank you Lucy for always being so available and kind. The pregnant mothers who so generously agreed to be part of all these studies have obviously been essential to this work. I am greatly indebted to all of them. This work could not have been made possible without the help of Carlo Castellano and his enormous generosity in allowing Esaote S.p.A. (Genoa, Italy) to lend me the equipment specifically chosen for the various requirements of this work. Carlo and Ileana, you have been marvellous friends. All the technicians and local directors of Esaote have been excellent in solving the many problems of ultrasonographic research. A special thank to Dr Testa and Dr Schiavi, and to Emilio Busato for technical help. In their special training courses, Heinz Prechtl, Christa Einspieler, Giovanni Cioni, and Paolo Ferrari have been fundamental teachers for learning to observe fetal and neonatal motions. Heinz and Christa were so kind as to ask me to speak at to two meetings in Graz. These symposia were invaluable for meeting extraordinary people, and for learning and testing out some of my thoughts. I am particularly grateful to Peter Wolff for some long discussions in Graz, Boston, and Milan. Many other special colleagues and friends have been at my side at various stages of my work. Particular thanks go to Antonio d’Elia, Daniel Stern, Colwyn Trevarthen, Elizabeth Spillius, Jerry Bruner, the late Mauro Mancia and the late Elizabeth Bryan, and to Diane Garcia and all my friends in Los Angeles. Giannis Kougioumouzakis in Crete has always provided a wonderful arena to test out my ideas and share them with him and with an exceptional audience. I am also grateful to the anonymous reviewers of the manuscript for their valuable suggestions. A very special thank you goes to my editor Donatella Rizza for being so accessible, helpful, and encouraging. Working with her and with all the staff at Springer-Verlag Italia has been a real pleasure. Chris Benton as usual has carefully and patiently revised my English. Andrea Sommaruga

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has helped me with figures and computer work, and Sergio Belfiore with photographic material. Luigi with Filippo and Roberto have been always lovingly and unfailingly by my side. Ultimately, of course, the responsibility for what I say in this book remains mine alone.

Acknowledgements

Contents

1

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1

General Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

7 8 11 12 16 16

1.1 1.2 1.3 1.4 1.5

2

Startles, Twitches and Clonuses. . . . . . . . . . . . . . . . . . . . . . . . . . . 19 2.1 2.2 2.3

3

19 25 27

Hiccups . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Yawning. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gasping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

29 33 36

Fetal Breathing Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 4.1 4.2 4.3 4.4 4.5

5

Startles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Twitches. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Clonuses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Hiccups, Yawning and Gasping . . . . . . . . . . . . . . . . . . . . . . . . . . . 29 3.1 3.2 3.3

4

General Movements: 7 16 weeks . . . . . . . . . . . . . . . . . . . . . . . . . Length of the Feet and Epidermal Ridges . . . . . . . . . . . . . . . . . . . General Movements: 17 25 weeks . . . . . . . . . . . . . . . . . . . . . . . . General Movements: Frequency and Duration . . . . . . . . . . . . . . . Central Pattern Generators. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Fetal Breathing Movements: General Features . . . . . . . . . . . . . . . Fetal Breathing Movements: Non-Coincidence with other Behavioural Events . . . . . . . . . . . . . . . . . . . . . . . . . . . Apnoeic Pauses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Possible Functional Significance. . . . . . . . . . . . . . . . . . . . . . . . . . Neurological Substrate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

40 41 42 44 45

Swallowing, Sucking, and Handedness as Inferred from Fetal Thumb Sucking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 5.1 5.2 5.3 5.4 5.5

Swallowing and Sucking: General Features . . . . . . . . . . . . . . . . . Swallowing: Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Fetal Swallowing: Possible Functions. . . . . . . . . . . . . . . . . . . . . . Swallowing: Possible Regulation . . . . . . . . . . . . . . . . . . . . . . . . . Handedness in the Human Fetus as Assessed by Thumb-Sucking . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

49 50 53 54 54

XI

Contents

6

Localized Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 6.1 6.2

7

Basic Emotions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-Modal Integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preparing for Post-Natal Communications . . . . . . . . . . . . . . . . . . Parental Reactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Yawning: a Form of Communicating? . . . . . . . . . . . . . . . . . . . . .

Sleep in Children . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Behavioural States in Premature Infants and Mature Fetuses . . . Early Fetal Functioning: Rest-Activity Cycles and Clusters of Activities. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.3.1 Ontogeny of Sleep and its Possible Precursors . . . . . . . . . . . . . . .

88 88 89 92

Twin Fetuses and Twin Myths . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 9.1 9.2 9.3 9.4 9.5 9.6 9.7 9.8

10

78 80 82 83 85

Rest-Activity Cycles, Clusters and the Ontogeny of Sleep . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87 8.1 8.2 8.3

9

61 71

Facial Expressions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77 7.1 7.2 7.3 7.4 7.5

8

Hand and Arm Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Leg Movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Beginnings of Intrapair Stimulation and its Relevance for Our Knowledge of the Sensory Capacities of All Fetuses. . . . Features of Rest Cycles Revealed by Twins . . . . . . . . . . . . . . . . . Similarities and Differences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Behavioural Individuality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Universal Myths . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Twins: Open to Mutual Communication . . . . . . . . . . . . . . . . . . . . Maternal Emotions and their Impact on the Twin Fetus . . . . . . . . Bereavement in the Twin Fetus . . . . . . . . . . . . . . . . . . . . . . . . . . .

97 99 100 104 104 105 105 106

Conclusions. Movement is Life . . . . . . . . . . . . . . . . . . . . . . . . . . . 107 10.1 10.2 10.3 10.4 10.5

Fetal Movements: Varied and Varying Functions . . . . . . . . . . . . . Shaping a Sense of our Boundaries. . . . . . . . . . . . . . . . . . . . . . . . Building a Body Schema and a Proto-Sense of Self . . . . . . . . . . . Forming the Cortical Homunculus and its Curious Layout?. . . . . Building on Expressive Repertoire . . . . . . . . . . . . . . . . . . . . . . . .

107 109 110 111 112

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115 Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131

Introduction

Keywords Fetus • Neonate • Movements • Gestation • Premature • Ultrasound

Normal human fetal movements during the first 25 weeks of gestation have generally been overlooked. The beginnings of fetal activities have in the main been regarded as chaotic and disorganized, and as such not worthy of detailed investigation. In reality, fetal movements during the first 25 weeks of pregnancy are simply organized differently to those in later periods, and are in any case functional to the various stages of development of that time span. However, quite apart from the neglect suffered by this specific period, all research on human fetal movements seems to have come to a standstill in recent years, whilst myths surrounding our first movements have flourished. Our origins have always fascinated us, and the origins of our movements are particularly fascinating as they initiate many vital phenomena. Historically, Aristotle can be considered the father of embryology. He was the first scholar to challenge the traditional view of existence as beginning only at birth; his investigations began at or soon after conception and were always grounded in direct observation. Based as it is on the observation of movements from their very beginning, in this particular sense this work could be regarded as ‘Aristotelian’. Aristotle dissected many animals, possibly including human embryos, and observed their changes throughout the various stages of pregnancy. He attributed increasing degrees of animation to the growing embryo. According to his theories, the embryo started its development in a ‘vegetative’ state. A ‘sentient’ phase then followed until 16 20 weeks, when ‘quickening’, the stage of pregnancy at which the mother begins to sense fetal movements, began and the embryo was thought to have irrevocably achieved a ‘raA. Piontelli, Development of Normal Fetal Movements. © Springer Verlag Italia 2010

tional soul’. Following Aristotle, many scholars continued to regard quickening as the sign that the fetus had finally emerged from the chain of its former vegetable and animal hazy states and attained ‘ensoulment’ or ‘animation’, a term derived from the Latin anima (soul). Other scholars, mainly basing their interpretations on analysis of the Old Testament, considered the first breath as the true beginning of human life. Still others regarded viability as the indication that the fetus had fully entered the human world. Opponents of all these theories of ‘delayed ensoulment’ contended that the embryo possessed a soul from conception and was fully human long before it quickened and long before it took its first aerial breath. These concepts were debated for centuries amongst various religious communities, and similar arguments, though refined and updated, are still largely at the basis of pro-choice and pro-life debates. When the fetus attains a ‘rational soul’ or, as we would call now it, ‘awareness’ and ‘consciousness’, continues to be an unanswered question which will not be touched upon in this book. The very concepts of consciousness and awareness are far from being clarified and still await both differentiation and convincing consensual definitions. Furthermore, the attainment of consciousness is not an either/or phenomenon, but one that is built gradually and takes on different gradations and shades during its development. It may possibly be easier to state when a fetus cannot sustain consciousness than when it can. It was only when scientists stopped looking for the ‘soul’ that a truly observational and scientific interest in the fetus began. Towards the turn of the nineteenth century, several disciplines split from philosophy, making it

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possible for proper fetal research grounded in reality to start. William Preyer, a German embryologist and physiologist, can be considered the true father of fetal studies. Preyer wrote in 1885 a seminal treatise, ‘Spezielle Physiologie des Embryo’(‘Special Physiology of the Embryo’), in which he dealt with the sensorimotor functions of the human fetus, giving expression to many far-reaching intuitions [1]. However, the means available to early scientists were very limited. They could only observe the excursions of the maternal abdominal wall or try to infer the behaviour of the fetus from that of premature infants. After Preyer’s pioneering work, the subject stagnated for about 50 years, and it was only between the 1920s and the 1940s that fetal studies saw a remarkable resurgence. Several scholars observed fetuses after spontaneous miscarriage or abortion by caesarean section. Significant contributions were made by the Swiss neurologist and psychiatrist Myeczyslaw Minkowski [2], who observed the behaviour of surgically removed fetuses; by Davenport Hooker [3], an American anatomist, who added cinematic documentation and tactile stimulation to the observation of moribund human aborted fetuses; and by Hooker’s collaborator Tryphena Humphrey [4]. Their investigations, pursued by testing and directly observing the early human fetus, provided numerous basic concepts, many of which are still fundamental today. Another historical classic is Arnold Gesell’s The Embryology of Behavior, published in 1945, which describes and illustrates the physical and behavioural development in the human from embryo to fetus, and from fetus to neonate [5]. Other relevant contributions came from scientists observing and experimenting with various animals. However, the majority of the studies performed in these years were strongly influenced by the otherwise remarkable work of Sherrington and Pavlov centring on reflexes, and as a consequence of this, a ‘reflexogenic’ view of fetal motions became prevalent whereby they were considered to be invariably generated by unidentified stimuli. After this extraordinary blossoming, the subject was largely abandoned until the introduction of ultrasound in the mid-late 1970s. Ultrasound, by offering the unprecedented possibility of observing the undisturbed and unharmed fetus in its natural environment, opened a completely new era for the study of fetal activities, which not surprisingly underwent an unparalleled renaissance. The belief in the reflexogenic nature of human fetal movements was promptly and fully dispelled. Ultrasonographic investigations of human fetal motor development were pioneered by Birnholz and colleagues [6], Ianniruberto

Introduction

and Tajani [7], and deVries, Visser and Prechtl [8 10]. The studies of Prechtl and his followers have been particularly influential. Prechtl, a developmental neurologist, was initially a student of Konrad Lorenz, one of the founders of ethology. Ethology is the branch of zoology studying animal behaviour within its natural environment as well as in the laboratory. The pictures of Lorenz immersed in a pond observing the greylag goose or walking about followed by a young ‘imprinted’ duck have become icons of naturalistic studies. Prechtl applied many of the principles of ethology to fetal studies. Amongst other things, he furnished an accurate account of the evolution of fetal movements throughout pregnancy and a so-called ‘ethogram’, the description and definition of various fetal movements. This classification, based as it was on terminology used for the premature and the neonate, has been almost universally adopted, fostering mutual understanding amongst researchers in the field. Grounded as they are in the observation of the human fetus within its natural milieu, studies of fetal movements, including the present volume, are largely rooted in ethology. Niko Tinbergen, the other founder of ethology, who won the Nobel Prize for Medicine in 1974 together with Konrad Lorenz and Karl von Frisch, also had a significant influence on fetal studies. Tinbergen thought that scientists always needed to pay attention to four fundamental kinds of explanation when faced with any behaviour: function, causation, development, and evolutionary history [11]. These questions are still of primary relevance for those attempting to study human fetal behaviour. Whenever feasible each motor phenomenon described in this book will be examined in the light of Tinbergen’s four queries. However, to return to where we started: despite the importance of Prechtl’s leading work and perhaps because of its intimidating significance except for a few valuable additions, the study of human fetal motor functioning, in particular during the first 25 weeks of pregnancy, seems to have come to a halt. According to deVries, one of the pioneers in the field, human fetal motor research peaked between 1980 and 1990 and declined thereafter [12]. Even during this ‘golden age’ the first half of pregnancy was usually overlooked. Out of 109 relevant articles examined by deVries, 83% dealt with the second half of pregnancy only. As a result of this stagnation, the same data are quoted repeatedly and fairly uncritically, and our knowledge of the origins of fetal movements can be said to be still at the embryonic stage. Apparently contrasting with this stagnation in fetal

3

studies, a great wave of visually enthralling depictions of the ‘marvels’ of the womb have contributed to make many pseudo-experts believe that all the mysteries have been solved. Not only that, but since early fetuses move a lot, neglecting this period has fostered an ever growing body of myths and legends. Early fetuses are often regarded as highly evolved creatures functioning even better than neonates. Several reasons lie behind this state of affairs. Other branches of science investigating prenatal life have advanced enormously, but these advancements have barely touched on fetal movements. Embryologists have given us invaluable insights into the earliest stages of development by describing molecular, cellular and structural bodily changes and their evolution with minute accuracy. However, embryology focuses primarily on the initial phase of life the so-called embryonic period, which ends between 7 and 8 weeks of gestation. Furthermore, embryologists work mainly at a molecular and cellular level or on anatomical preparations derived from dead animals, including aborted human fetuses. Because of this methodological tendency, most embryologists, of necessity, do not take into account a relevant aspect of all embryos and fetuses: their frequent movements. Unlike embryologists, obstetricians are directly involved with the live fetus and its maternal environment. However, obstetricians are understandably not much interested in fetal movements, a topic which they tend to regard as secondary, especially during a pre-viable phase of development. Up until mid-gestation, obstetricians focus primarily on a variety of crucial matters ranging from ruling out ectopic implantation, establishing pregnancy dating, chromosomal testing and checking fetal anatomical morphology. Most of these concerns have an important bearing on clinical and parental decision making, and on determining the type and frequency of subsequent examinations. The time span from 22 to 25 weeks’ gestation is a grey area where survival ex utero is becoming increasingly possible, albeit often at high cost. Clearly, the survival rates of extremely premature infants (defined as infants born before 28 completed weeks of gestation) increase with gestational age. Currently the chances of survival are almost nil at 22 weeks and approximately 60% at 25 26 weeks [13]. Despite enormous medical progress, surviving infants born at less than 26 weeks’ gestation still show very high rates of life-long consequences including cerebral palsy (up to 36%), mental retardation (up to 47%), chronic lung disease (up to 61%),

blindness (up to 25%), and deafness (up to 7%) [14]. Neonatologists caring for these infants predominantly direct their clinical and research efforts on trying to keep these infants alive and avoiding all the above-mentioned complications. Motor functioning in the premature infant is looked at with a clinical eye as an indicator of whether current and future functioning will be normal or pathological. In addition, despite the many continuities between prenatal and postnatal life, obstetrics and neonatology have remained largely separate fields. Perinatology, the branch of medicine devoted to the perinatal period, should in theory have bridged the gap. As pointed out by the first professor of child development, the psychologist Arnold Gesell in 1945, extremely premature infants, born before 28 weeks, are to be considered ‘fetal infants’ with a dual nature, being at once extrauterine fetuses and prenatal neonates [15]. However, obstetricians specializing in perinatal medicine care for high-risk pregnancies, and perinatologists working in the intensive care unit deal with high-risk infants. While the division is no longer absolute, motor development once more understandably tends to be overlooked as of secondary concern. Developmentalists, on the other hand, have studied in depth the behaviour of the premature infant, trying to infer fetal functioning from it. Unlike the fetus, the premature infant can be directly and continuously observed. Various parameters and functions can be checked and verified. Nevertheless, extremely premature infants are not equivalent or wholly comparable to fetuses in utero. Although such infants largely remain ‘true to their fetality’ by adhering to their natural sequence of maturation, they live in a very different external environment that impacts profoundly upon their functioning [4]. Moreover, developmentalists, by starting the description of the motor and emotional behaviour of the infant from birth, tend to ignore the prenatal history of many neonatal phenomena with which they are not acquainted. The prevailing view of development also stresses a linear progression. Following this outlook the fetus is regarded solely as preparing to become a neonate, just as the neonate is regarded as practising to become an adult, in a linear sequence. Attention to preparatory and anticipatory functions generally prevails. This outlook does not take into account that fetuses inhabit a very different environment from the neonate and even more so from the adult. Furthermore, the intrauterine environment is subject to changes to which the fetus has to adapt. Such adaptations, named ‘ontogenetic adaptations’ by Oppenheim [16], may in-

4

volve particular morphological, biochemical, physiological and behavioural mechanisms which are different from those of the neonate and even more so from those of the adult. All these may require modification or even abandonment before the neonatal stage is attained. Wellorganized neonatal functioning does not spring into action without preceding steps, nor are all fetal activities geared towards postnatal existence. Many are simply functional to a particular phase, and still others have both a preparatory and an adaptive component. On the other hand, those researchers who study fetal behaviour prefer to focus on the movements of the fetus approaching birth and on how they link with those of the neonate. At this stage the physician has several possibilities of intervention, including inducing birth. Research and clinical efforts usually concentrate on detecting signs of distress and alarm. In addition, fetal movements during the early stages of pregnancy are commonly considered chaotic and ‘disorganized’ and as such have been generally disregarded. In contrast with this, all movements to be found in the near-term fetus are widely considered to be already present by 16 weeks’ gestation. Whilst it is true that the overall gestalt of fetal motions allows a particular movement to be identified and classified using the same designation throughout, such motions are nevertheless executed in varying ways at different gestational ages. During pregnancy, fetal dimensions, proportions, neurological and generally speaking physiological functioning, as well as intrauterine factors all change at a dazzling pace. Growing fetal constriction is just one example of macroscopic change. If only for this reason, movements cannot be performed uniformly at 10 weeks’ and at 25 weeks’ gestation. Another important reason for the lack of advances in the study of early fetal movements has been the wait for new technological developments. So far, dynamic ultrasonography offered a two-dimensional (2D) and only partial picture of the fetal body, especially in the second half of pregnancy. Three-dimensional and, more recently, 4D ultrasonography seemed to hold great promise for fetal studies, and researchers have been waiting for these and other new refinements. Three-dimensional ultrasonography can give us beautifully detailed static pictures of the fetal body. These images have enhanced our knowledge of fetal anatomy, as well as providing a valuable tool for detecting some anatomical malformations. However, good 3D pictures are not always easy to obtain. For instance, when the uterus becomes crowded it becomes almost impossible to visualize the fetal face if the cord or

Introduction

the hands are in the way. In other words, the target of a study is easily lost. Four-dimensional ultrasonography has added the dimension of movement to the images the fourth dimension referred to in the name. Four-dimensional ultrasound has shown that fetal movements start earlier than was thought, and allow more precise reading of some movements. The work of Asim Kurjak has been particularly influential in this field [17,18]. However, 4D images (like 3D images) are computerized reconstructions of fetal motions, and as such do not allow us to capture many of the features of real-time movements, such as speed, quality, tempo and precise sequence, or to visualize very fast movements such as breathing, startles or hiccups. These are not secondary issues for the study of movements. Nor are fast movements of secondary relevance for fetal functioning. Sensational 3D and 4D images are beginning to invade all sorts of publications ranging from obstetrics treatises to magazines. Frequently these are touched up using Photoshop or similar programs in order to make them look more appealing. A true revolution in fetal studies will be brought about by the advent of real-time 4D ultrasonography. In the observations reported in this volume these new technologies have been used alongside traditional 2D realtime ultrasonography. The most rewarding application of 4D ultrasonography turned out to be the investigation of the beginnings and evolution of hand movements and of various facial expressions. In contrast to the relative decline of human fetal studies, those of animal fetuses, because they are open to various kinds of experimentation, have continued to flourish and give us fundamental information which for obvious reasons cannot be obtained from the human fetus. The leap from other species to humans is not always pertinent; however, whenever appropriate, animal studies will be referred to throughout this book. The studies of developmental psychobiologists an interdisciplinary field encompassing developmental psychology, biological psychology, neuroscience and many other areas of biology too numerous to mention have all been particularly influential. It must suffice to mention here almost at random the fundamental work of just a few, such as Jeffrey Alberts [18], Myron Hofer [19], George Michael [20, 21], Celia Moore [20], Peter Hepper [22], Scott Robinson [23], Carolyn Rovee-Collier [24] and William Smotherman [23] and their colleagues, who, along with many others, through the use of experimentation

References

have all given us essential understandings into fetal life. Enormous advances have also been made in disparate fields ranging from genetics to molecular biology and histology. While some reference will be made to these, it is beyond the scope of this book, which deals with the macroscopic phenomenon of fetal movements, to discuss in detail the findings of these highly specialized fields. Neuroimaging, particularly using magnetic resonance imaging (MRI), is also contributing a great deal of information on the growth and development of the fetal body in general and of the central nervous system in particular. However, a thorough discussion of the rapidly accumulating data is also beyond the scope of this book. This volume aims to serve other researchers in the field, clinicians, developmentalists, and ultimately parents if possible. By understanding normal motor functioning, obstetricians may become alert to unusual phenomena which could in turn lead to further, lengthier and longitudinal observation. Neurologists may be encouraged to derive from it meticulous fetal ‘developmental milestones’ that might eventually lead to a long-awaited neurological examination in utero. A thorough knowledge of normal early fetal functioning may assist neonatologists and paediatricians in understanding phenomena that turn out to be pathological in the premature infant and, hopefully, may lead to the devising of new ways to cope with them. It may aid developmentalists to judge which phenomena are rooted in the physiology of our prenatal past and to distinguish these from other phenomena that arise ex novo or belong to the pathology of the present. Finally, parents of severely premature infants may also be helped to look at their tiny babies in a different way. Knowing that fetuses of the same gestational age are barely social creatures may help them to feel less frustrated and at the same time less guilty for not providing ‘adequate’ care and stimulation to their fetal infants. They may also start regarding some phenomena such as gaze avoidance or hiccups not as signs of ‘stress’, ‘avoidance’ or ‘refusal to relate’, portending psychological catastrophes later on, but as perfectly functional phenomena linked to the true age of their infants. Since this book is addressed principally to specialists in various fields other than fetal studies, the language has been kept as plain and as descriptive as possible, and a glossary has been added at the end. All observations discussed in this book are derived from both general and targeted investigations. Each observation (no matter whether general or targeted) lasted an hour, took place at the same time of the day after a

5

standard meal, was recorded on DVD or tape, and was later analysed off-line by two or more researchers. Save for twins, a cross-sectional approach was utilized, and each week 30 subjects were investigated for a general view and 30 more for a targeted one in relation to fetal breathing movements, leg and arm movements, and sucking and swallowing motions. Thirty pairs of twins were observed longitudinally twice a month from week 10 till the end of pregnancy. Facial expressions were studied cross-sectionally in 10 women from week 10 to week 25 with 3D and 4D ultrasounds. Throughout this book ‘weeks’ refer to gestational age calculated from the date of the last menstrual period not to conceptional age. As to the organization of this book, Chapter 1 deals with the most noticeable motor phenomena arising first, general movements. Chapter 2 deals principally with startles, another frequent movement which starts during early prenatal life, and with twitches and clonuses, in order of decreasing frequency. Chapter 3 deals with three phenomena whose functional significance is still largely obscure: hiccups, yawning, and gasping; all three, however, have been linked to some extent with fetal breathing. Chapter 4 describes fetal breathing motions. Chapter 5 describes swallowing and sucking motions and discusses handedness as inferred from fetal thumb sucking. Chapter 6 deals with localized motions, focusing in particular on arms and hand movements as well as those of the legs. Chapter 7 describes the beginning of facial expressions and their evolution. Chapter 8 deals with rest activity cycles, clusters of various motions, and with some hypotheses on the ontogeny of sleep. Chapter 9 describes differences and similarities in the motions of twin fetuses and discusses their meaning for all fetuses. In addition, the host of ‘fetal myths’ that burden twin fetuses are analysed and dispelled. Finally, in Chapter 10 some considerations of a more speculative nature are discussed.

References 1. Preyer W (1885) Spezielle Physiologie des Embryo. Grieben, Leipzig 2. Minkowski M (1922) Über frühzeitige Bewegungen, Reflex und muskuläre Reaktionen beim menschlichen Fötus and ihre Beziehungen zum fötalen Nerven and Muskelsystem. Schweiz Med Jahrbuch 52:721 724 and 751 755 3. Hooker D (1952) The prenatal origin of behavior. University of Kansas Press, Lawrence, Kansas 4. Humphrey T (1978) Function of the nervous system during prenatal life. In: Stave U (ed) Perinatal physiology, 3rd edn.

6 Plenum, New York 5. Gesell A (1945) The embryology of behavior. In: Classics in de velopmental medicine, 2nd edn (1988). Lippincott, Philadelphia 6. Birnholz JC, Stephens JD, Faria M (1978) Fetal movement patterns: a possible means of defining neurologic develop mental milestones in utero. Am J Roentgenol 130: 537 540 7. Ianniruberto A, Tajani E (1981) Ultrasonographic study of fetal movements. Semin Perinatol 5:175 181 8. de Vries JIP, Visser GHA, Prechtl HFR (1982) The emergence of fetal behaviour. 1: Qualitative aspects. Early Hum Dev 7:301 322 9. de Vries JIP, Visser GHA, Prechtl HFR (1984) Fetal motility in the first half of pregnancy. In: HFR Prechtl (ed) Continuity of neural functions from prenatal to postnatal life. Spastics International Medical Publications, London 10. de Vries JIP, Visser GHA, Prechtl HFR (1988) The emergence of fetal behaviour. 3: Individual differences and consistencies. Early Hum Dev 16:85 103 11. Tinbergen N (1951) The study of instinct. Oxford University Press, Oxford 12. de Vries JIP, Fong BF (2006) Normal fetal motility: an overview. Ultrasound Obstet Gynecol 27:701 711 13. Brodsky D, Oullette MA (2008) Transition of the premature infant from hospital to home. In: Brodsky D, Oullette MA (eds) Primary care of the premature infant, chap 1. Saunders, Philadelphia, pp 1 8 14. Wilson Costello DE, Hack M (2006) Follow up for high risk neonates. In: Martin RJ, Fanaroff AA, Walsh MC (eds) Care of the premature infant, vol 2, 8th edn, chap 39. Mosby, Philadelphia, pp 1035 1043

Introduction 15. Gesell A (1945) The embryology of behaviour: the beginnings of the human mind (1988 edn). Mac Keith Press, London 15. Oppenheim RW (1984) Ontogenetic adaptations in neural development: towards a more ‘ecological’ developmental psychobiology. In: HFR Prechtl (ed) Continuity of neural functions from prenatal to postnatal life. Spastics International Medical Publications, London 16. Jackson D, Kurjak A (eds) (2004) An atlas of 3D and 4D sonog raphy in obstetrics and gynecology. Informa Healthcare, London 17. Kurjak A, Azumedi G (eds) (2007) The fetus in three dimen sions: imaging, embryology and fetoscopy. Informa Health care, London 18. Ronca AE, Alberts JR (2000) Physiology of a microgravity environment. Selected contribution: effects of spaceflight during pregnancy on labor and birth at 1 G. J Appl Physiol 89:849 854 19. Hofer MA (1995) Roots of human behavior. WH Freeman Company, Plymouth, Michigan 20. Michel GF, Moore CL (1995) Developmental psychobiology: an interdisciplinary science. MIT Press, Cambridge, Massa chusetts 21. Hopkins B, Barr RG, Michel GF et al (eds) The Cambridge encyclopedia of child development. Cambridge University Press, Cambridge, UK 22. Hepper PG (ed) (1991) Kin recognition. Cambridge Univer sity Press, Cambridge, UK 23. Smotherman WP, Robinson SR (1990) Behaviour of the fetus. CRC Press, Boca Raton 24. Rovee Collier C, Lipsitt LP, Hayne H (eds) (2000) Progress in infancy research, vol 1. Lawrence Erlbaum, Philadelphia

General Movements

1

With the assistance of Florinda Ceriani, Isabella Fabietti, Roberto Fogliani and Alessandra Kustermann

Keywords General movements • Central nervous system • Central pattern generators • Motor patterns • Brainstem • Lordosis • Opisthotonus • Kyphotic • Volar pads • Popliteal angle • Hypotonia • Myotubes • Primitive stepping • Supine kicking • Nuchal tone

General movements, also called total pattern or holokinetic movements (from the Greek holos meaning whole and kinema meaning motion) emerge as periodic bursts of whole-body activity and are one of the earliest and most dramatic forms of fetal movement. In 1929, the American anatomist Coghill, studying the aquatic stage of development of the amphibian lizard Amblystoma, was the first to describe and distinguish between ‘total and partial patterns of motion’. Coghill postulated that the same distinction could apply to human fetuses, which he viewed as similar to amphibians: creatures living in an aquatic medium, but preparing to enter a terrestrial one [1]. Then, in the early 1950s, Hooker noted that local movements appeared later in development than ‘total pattern’ ones [2]. Because his observations were performed directly on human fetuses, Hooker’s remarks are still widely quoted in reference to the emergence of particular fetal sensitivities. However, it was only with the advent of ultrasonography that naturally occurring general movements were observed in the healthy fetus living within its natural environment and differentiated from localized motions. Using ultrasound, the Austrian physician Reinold [3] was the first to distinguish strong and brisk movements involving the entire body from movements ‘confined to fetal parts’. Similar descriptions were given by other physicians, especially Juppila [4] and Van Dongen and Goudie [5]. During the 1980s, detailed classifications of various movement patterns were expounded. AlA. Piontelli, Development of Normal Fetal Movements. © Springer Verlag Italia 2010

though these taxonomies were similar, the one developed by Prechtl and his collaborators [6] eventually became the one universally adopted in scientific circles, due partly to its particular accuracy and partly to Prechtl’s own renown in the field of child neurology. General movements were described as non-stereotyped motions in which ‘the whole body is moved but no distinctive pattern or sequence of body parts can be recognized… Movements of limbs, trunk and head are rapid, but smooth in appearance.’ Prechtl and his collaborators noticed the first appearance of general movements at between 8 and 9 weeks, and described their qualitative changes in time as follows. At 8 9 weeks general movements were said to be slow and limited in amplitude. At 10 12 weeks they were described as more forceful and rapid, with limbs, trunk and head all involved in the motion. After 12 weeks general movements became ‘more variable in speed and amplitude’, and their duration was noted to vary from about 1 to 4 min. As Prechtl said, general movements ‘wax and wane’, and, ‘however variable these movements are, they are always graceful in character’ [6]. Besides these qualitative aspects, quantitative characteristics and individual consistencies and variations were described. In parallel with this widely quoted and authoritative work, interpretations attaching an emotional meaning to fetal movements have continued to proliferate. The most frequent comment one hears from parents and obstetricians alike when a fetus starts a burst of generalized motion

8

is: ‘Look, it is waking up.’ Given their dramatic quality, general movements are also often interpreted as signs of hyperactivity and anxiety, whereas, in fact, brief episodes of wakefulness are a late acquisition in pregnancy, and anxiety-driven states of hyperactivity only belong to life after birth. Technical refinements, in particular transvaginal and 4D ultrasonography, have shown general movements to start about 1 week earlier than was previously thought, right at the start of the fetal period, between 7 and 8 weeks [7]. From the very beginning general movements are not stereotypical, but performed in unpredictable combinations, constantly adapted to the ever changing internal and external environmental conditions. Even during the initial, greatly ‘simplified’ stages, general movements are never exactly alike. The fetus can start coiling slightly on one side of the body rather than the other; the upper or the lower segment of the trunk can be involved; a slight extension of the head, a little stretching of the spine or a rudimentary movement of one limb can follow. All combinations are different. Twins, because they allow simultaneous observation of two fetuses using one or the other co-twin as a control, highlight beautifully the non-stereotyped quality of general movements [8]. With advancing gestation, the complexity and variation of movement increase enormously. Body proportions, muscle length and composition, ossification (from the Latin ossae meaning bones), connections with and within the central nervous system, and spatial constrictions, to name but a few factors, change at a dazzling pace, allowing fetuses to perform new modes of movement. Adaptation and calibration of motor patterns takes place as the fetus grows and develops. At the same time, some forms of movement become redundant or impossible.

1.1 General Movements: 7-16 weeks Before 10 weeks, general movements are barely perceptible and have an oscillatory, swimming-like quality. Operators and parents alike frequently comment on these motions, saying that the fetus looks like a ‘little fish’. The head and the trunk periodically coil moderately on one side or the other, and the spine occasionally arches back, frequently accompanied by a slight extension of the head. At this early stage, general movements do not cause positional changes and limbs hardly

1 General Movements

participate in their execution. By the late embryonic stage, corresponding to 7 8 weeks, limb buds have changed into differentiated limbs, and ‘human’ hands and feet with separate fingers and toes have formed [9]. However, in terms of length and size, the limbs are small relative to the head and trunk. Hip and shoulder joints are not yet fully independent and mobile, while trunk muscles are more developed than limb muscles (Fig. 1.1). Between 10 and 13 weeks general movements are propelled by the axial component of the body, the head and the trunk. Shoulders and trunk act in synchrony. The spine stretches back, provoking a marked arching of the entire body followed by rotation of one shoulder and finally of the head. The head, by pointing into the uterine wall, can occasionally act as a pin around which the whole body moves. Head rotations on the other hand are very limited both in frequency and in amplitude, as the neck has not yet reached full anatomical autonomy. Though some independent arm and legs movements can be noted, generally the limbs follow the axial component fairly passively. Stretching of the spine continues to be important, and will remain relevant throughout. At 14 weeks, when stretched backwards the spine displays extreme lordosis or arching (Fig. 1.2). When not arched back the spine is wholly kyphotic (meaning flexed forward or gibbous). Although later in pregnancy the spine becomes more flexible and articulate, only after birth will its alignment develop with cervical and lumbar lordosis, allowing erect stance. At around 15 16 weeks the head can rotate and extend fully. Given its relative proportions and weight it can set the whole body in motion by itself. A rotation or a stretch of the head can unbalance the rest of the body and trigger a cascade of motions. However, from 14 weeks onwards legs and feet increasingly participate in setting the whole body in motion. Legs no longer move only simultaneously: alternate movements have started. The speed and amplitude of alternate movements is not comparable to those achieved a few weeks later, but from now on legs become essential pivots and driving forces of motion. Predominantly legs are extended till the feet touch the uterine wall, push against it and impart a thrust to the whole body (Fig. 1.3). At this stage the arms play a less relevant role in general motions. On the other hand, arms and hands have become a principal component of localized motions. Besides alternating movements, legs can now trigger

1.1 General Movements: 7-16 weeks

9

a

b

c

d

a

Fig. 1.1 Early anatomy and bodily proportions. a, b Fetuses at 8 weeks’ and 9 weeks’ gestational age, re spectively. The head and trunk are extremely large relative to the limbs in length and size. Hip and shoulder joints are not independent of the axial com ponent of the body, and the neck is not anatomically independent of the trunk. The earliest general move ments can only consist in slight stretches and coils of the head and the trunk. c, d Fetus at 11 weeks’ gestational age. The limbs have become longer, the head has become slightly smaller compared to the trunk, and the neck has lengthened and attained partial anatomical independence. Trunk muscles begin to be developed. Although limbs start to accomplish some independent movements, they clearly cannot drive the entire body, but rather are trailed by it

b

Fig. 1.2 Curvature of the spine. a Fetus at 14 weeks’ gestation. The spine displays extreme lordosis, almost giving the impression of an opisthotonic posture a posture characterized by hyperextension of the back and neck muscles, and arching forward of the trunk. In life after birth opisthotonus is seen especially in severe cases of meningitis and decerebration. b Fetus at 20 weeks’ gestation. The spine still displays considerable lordosis. However, a slight curvature begins to be noticed at the level of the lumbar tract

10

1 General Movements

a

b

c

d

Fig. 1.3 Alternate and articulated leg movements. a d Fetus at 16 weeks’ gestation. Alternate and articulated leg movements have become an essential component of general movements. The fetus points its legs (a); alternate leg motions impart a thrust (b); the fetus has turned round, and well articulated leg motions contribute to bring about further positional changes (c, d)

a

b

Fig. 1.4 ‘Locust’ jump. Fetus at 16 weeks’ gestation. a The fetus is ‘sitting’ with its legs bent to the limit. The femur is almost in contact with the tibia (each seen in white, like all ‘bony’ parts) and presumably with the fibula (not visualized here). b The legs are suddenly re leased and stretched, imparting a jump like thrust to the whole body

1.2 Length of the Feet and Epidermal Ridges

general movements by acting in a spring-like manner. Fetuses frequently ‘sit’ in the ‘fetal position’ with the spine flexed forwards and bend their legs to the limit till these and the forelegs are in tight contact with each other as well as with the lower abdomen. Extreme leg bending is probably favoured by composite factors ranging from laxity of ligaments to sparse ossification, allowing a degree of bone flexibility that will no longer be possible a few weeks later. All these factors change rapidly. For instance, bone formation is not a once and for all phenomenon, but more commonly starts from so-called ossification nuclei, small areas of bony tissue, and spreads from there to the rest of the limb or spine. Ossification is not wholly complete at birth [9]. Spatial constrictions, too, now favour the loading of the axial body on the legs. Additionally, during this kind of movement the hands are almost constantly placed on the knees, both stabilizing and locking them, while at the same time increasing the pressure exerted by the legs and feet against the uterine wall. While crouched in this way fetuses push forcefully and simultaneously with both feet against the uterine wall for 6 10 s. Their feet are then suddenly released and their legs elongated, thrusting the whole body with force (Fig. 1.4). This kind of thrust can be compared to the jumping of a locust, although the locust has a totally different structure of the legs, which are also folded and positioned in a completely different way. As with lo-

11

custs, however, fetal jumping may be dependent on the storage and subsequent rapid release of energy to make the leap possible [10 12].

1.2 Length of the Feet and Epidermal Ridges Interestingly, fetuses have ‘big feet’. Up until 25 weeks, fetal feet are almost as long as the femur (Fig. 1.5). Big feet may, amongst other things, have the function of maximising the push, with a consequent increase of stored energy. After 16 weeks, ‘locust jumping’ continues to occur occasionally, but spatial constrictions do not make it easy for the fetuses to ‘jump’. Another factor may be of relevance. By 14 weeks epidermal ridges have formed on the soles of the feet as well as on the palms of the hands. In 1929 Harold Cummins, an American professor of microscopic anatomy, published a paper, ‘The topographic history of the volar pads in the human embryo,’ in which he described how epidermal ridges are preceded by the formation of the so-called volar pads, a swelling in the mesenchyme, or connective tissue, of the palms and soles. Initially the ridges are not fixed because ‘the skin possesses the capacity to form ridges, but the alignment of these ridges are as responsive to stresses in growth

Fig. 1.5 Foot and femur: rela tive proportions. At 12 13 weeks the length of the foot almost equals that of the fe mur. A slight (less than 0.5 cm) discrepancy can be noted between weeks 13 and 16. From week 17 to week 19, foot and femur are the same length, and at week 20 the foot is minimally longer

12

1 General Movements

a

b

c

d

Fig. 1.6 Sliding motions. Fetus at 17 weeks’ gestation. a By pointing its feet and bending its legs, the fetus lifts up the rest of its body. b The feet are suddenly released and the fetus slides downwards along the surface of the uterus. c, d With some variation in the pointing of the legs causing an arching of the lower spine and a forward bending of the head, a similar sliding motion is finally achieved

as are the alignments of sand to sweeping by wind or wave’ [13]. In addition to their relevance to forensic investigation and palmistry, ridges have the other function of causing a friction between the ridged surface and any other surface with which it may come in contact namely, the fairly slippery placenta and/or uterine wall. In other words, ridged feet can push forcefully against the uterine wall without easily sliding away. In fact, other non-ridged surfaces like the back of the body are used to perform sliding motions along the uterine wall which well-anchored feet make possible (Fig. 1.6). Feet remain relevant for the mechanics of motions up to 25 week and beyond. Though less so, even at birth they are still particularly long. From 14-15 weeks alternating leg movements performed in increasingly different combinations are used to cause a rotation of the entire fetal body. Generally speaking, extension of the legs is now largely replacing flexion in initiating general movements.

1.3 General Movements: 17-25 weeks Some other broad modes seem important. Fetuses stretch their legs and arch their spines backwards until the head and both feet are firmly pressed against the wall. By using these two hinges fetuses then turn their shoulders, thorax, and finally pelvis, rotating their body with their legs following last of all. Occasionally knees can also be used as hinges. In contrast to legs and feet, up to 18 weeks the arms seem to act mainly as balancers or equalizers, with limited active participation in the thrust that sets general movements in motion. This balancing function possibly allows the body more flexibility of movement in different planes whilst also minimising its effort. By carefully reducing, correcting and compensating the turbulent motions of other bodily parts, arms provide

1.3 General Movements: 17-25 weeks

continuous adjustment to the moving organism. Until the end of pregnancy the arms are actually longer than the legs, favouring this ‘balancing’ role (Fig. 1.7). From 18 20 weeks, however, the arms too begin to participate increasingly in the initiation and execution of general movements. During this period, fetal constraint has become ever more relevant. Fetuses still move a lot, but all bodily parts are now more and more in contact with the placenta and the uterine wall. Besides the legs, the spine, the head, elbows, knees and shoulders all become important points of support and thrust. At around 18 20 weeks a particular form of motion begins to be observed. The growing uterus is hardly an even surface. Lumps, protuberances, small gorges, temporary and presumably hard areas of contraction can all be noted. Fetuses start using these bumpy areas as support planes. They lean their forearms and hands, trunk or abdomen on the surface. The head, aided by the decreased pull of gravity, is raised, but is encased between the shoulders, which are regularly and markedly elevated. On the whole the image of the upper part of the body seen in profile reminds us of a gibbous animal such as the wild bison or the African gnu. With the rest of the body supported by one of these surfaces, the legs display a vigorous, fast trotting motion (Fig. 1.8). If this kind of motion slows down it is reminiscent of some crawling patterns seen in the infant: the abdomen in contact with the supporting surface while the body and legs are pulled along by the arms only. It is also especially reminiscent of so-called ‘bunny hopping’ and is possibly a forerunner of these movements [14, 15]. The spine has by now acquired more flexibility of movement and various regions can display at least temporarily different curvatures. By leaning against a ‘sur-

13

face’ with the abdomen while keeping a near-horizontal spine and raising their head, fetuses achieve almost complete extension of the legs, as if practising to stand up. This motion too is reminiscent of the movements of infants trying to raise themselves up by leaning against a surface, be it a chair or their mother’s legs. Elongation and semi-flexion of the lower limbs increasingly become main thrusting modes. Extreme folding of the legs is usually noted when fetuses are in a cycle of rest. Legs can also be fully extended above the head with a minimal (60°) is observed and continues to be so until 23 25 weeks. Heel-to-head contact, which could be noted previously, is no longer observed. Both parameters are indicative of muscular tone and are evaluated in severely premature and premature infants to determine their gestational age as well as being signs of prognostic value. From 18 to 25 weeks leg movements are carried out with increasing speed, variety and skill. However, environmental constrictions are also increasing and flexion largely prevails over extension. The feet in particular can dorsiflex to the limit until they touch the leg. So-called ‘primitive reflexes’ involving leg movements which are noticed at birth in the healthy neonate have a long prenatal history. Stepping motions, as seen in the ‘stepping reflex’, are frequently performed. When stepping, fetuses clearly are not supported by an adult. However, within the uterus they execute stepping motions with environmental support, which is sometimes minimal. Stepping movements occur mostly when fetuses are lying on their backs. However, support can also be found the other way round when they lay their torso on some uterine protuberance as they would on a chair or on their mother’s lap after birth. From 23 25 weeks the forearms alone can sustain stepping motions. Besides these general norms, the intrauterine watery medium allows postures and movements which are not to be seen for quite a while in the neonate and the child living under the full impact of gravity after birth. Albeit for a very brief lapse of time (a few seconds), fetuses can perform ‘mature’ movements or take on ‘mature’ postures. They can sit unsupported with their heads

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a

b

Fig. 6.14 a Fetus at 13 weeks’ gestation. The first alternate leg movements can be noted. b Fetus at 15 weeks’ gestation. Using the head as a support, the fetus performs some semi standing al ternate stepping motions. Besides neurological and extensive bodily changes, the watery medium in which the movements are performed seems to have a big impact on the variety and range of the movements

raised, they can hop on one leg once or twice, and they can attain an almost erect stance with their knees slightly bent. However, this does not mean that fetuses are more ‘mature’ than neonates, as is frequently implied when the ‘miraculous’, ‘wondrous’ nature of their activities is mentioned and illustrated in glossy images. Simply, the watery medium allows them to execute and prepare for activities which will be carried out in a steady and sustained way in life after birth. Aquatherapy, also called water or swimming therapy, or hydrotherapy, is increasingly used to help patients suffering from infantile cerebral palsy. As defined by Dorland’s Medical Dictionary, the term ‘cerebral palsy’ comprises a group of motor disorders characterized by ‘delayed or abnormal motor development’ [23]. These

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motor problems, besides affecting the autonomy of the patient, can also cause serious muscular damage due to spasticity (or stiffness) in the muscles. When immersed in water, patients are less affected in their movement by their hypertonus or increased muscular tone, improve their coordination and endurance, and can perform movements such as walking, kicking and jumping which they are not able to carry out once back in their normal environment. Although cerebral palsy is predominantly caused by brain damage suffered during delivery and, especially, during intrauterine life, the overwhelming majority of fetuses do not suffer from cerebral palsy and spasticity. Like spastic children, however, within the amniotic fluid fetuses can perform, albeit momentarily, movements that they could not carry out in a terrestrial environment. Premature infants born at the same gestational age are totally unable to move in the same way. Severely premature infants barely move at all. Fetal leg ‘exercise’, easily carried out in the amniotic fluid, is vital for muscular and bone development, as is shown by the contractures and skeletal deformities found in fetuses suffering from prolonged and severe oligohydramnios (from the Greek words oligos meaning scarce and hudor meaning water). Club feet are just one of these deformities. Severe cases of oligohydramnios may be treated with amnio-infusion, the introduction of particular solutions into the amniotic sac to prevent deformities as well as other complications. Besides muscle and bone development, and a preparatory function for movements to be performed after birth, leg movements may have other important roles. Localized movements do not solely elicit tactile sensations, they are also an important source of proprioceptive information (from the Latin word proprius meaning one’s own, and perception) the information that we receive about the position, balance and movement of our body or any of its parts, the relative position of the body parts to each other, the position of the body in space, and the nature of the objects with which the body comes in contact. Proprioception allows us to adjust our stance constantly and reflexively to ongoing movements (Fig. 6.15). The terms ‘proprioception’ and ‘kinaesthesia’ are often used interchangeably, and the definition of and distinction between these terms are hotly debated. As a term, ‘kinaesthesia’ (or movement sense) places a greater emphasis on motion and relates to the capacity to locate the body and its related segments in space by

6 Localized Movements

a

b

c

Fig. 6.15 Legs as a source of proprioceptive and tactile feedback. a c Fetus at 20 weeks’ gestation. The fetus is observed in different planes. The feet are clearly an important source of tactile feed back. However, each single movement (and not only of the legs) is also a source of proprioceptive feedback. Both tactile and pro prioceptive feedback could be considered the initial ground on which a proto self begins to be based

sensing movement, weight and position. The term ‘proprioception’, on the other hand, refers mainly to a feedback mechanism. When the body moves or is moved,

References

information about this motion is returned to the central nervous system, which makes continuous adjustments in the movements. To complicate matters further, the term ‘haptic’ is also frequently used. ‘Haptic’ relates to the sense of touch in all its forms. For reasons of simplicity, the more commonly used terms ‘proprioceptive’ and ‘proprioception’ are used in this book. Legs movements, like all movements, are an important source of proprioceptive feedback information. Proprioceptive information is derived from so-called proprioceptors, sensory receptors located in the muscles, tendons and joints, and integrated from information arising from vestibular receptors, as well as from visual, auditory and tactile receptors. Visual and auditory information are clearly absent in the period considered in this work. Vestibular feedback, on the other hand, is most likely to be functional. Vestibular feedback pertains to the perception of balance, head position, acceleration and deceleration. Vestibular information is obtained from the semicircular canals in the inner ear. However, since vestibular perception includes the perception of gravity, fetal vestibular perception is likely to be different to that of the postnatal stage and adapted to the different requirements and environmental conditions characterizing fetal life. Sensorimotor demarcation and a proto-sense of self are possibly built progressively during prenatal life through tactile and proprioceptive information as well as vestibular feedback. This point will be explained in detail in the concluding chapter.

References 1. Ulrich BD (1997) Dynamic systems theory and skill development in infants and children. In: Connolly KJ, Forssberg H (eds) Neurophysiology and neuropsychology of motor development. Mac Keith Press, London 2. Bizzi E, Hogan N, Mussa Ivaldi FA, Giszter S (1994) Does the nervous system use equilibrium point control to guide single and multiple joint movements? In: Cordo P, Hranad S (eds) Movement control. Cambridge University Press, New York 3. Gandevia SC, Burke D (1994) Does the nervous system depend on kinaesthetic information to control natural limb movements? In: Cordo P, Hranad S (eds) Movement control. Cambridge University Press, New York 4. Jirasek JE, Keith LG (2001) An atlas of the human embryo

75 and fetus. Informa Healthcare, London 5. Haywood KM, Getchell N (2001) Life span motor development, chap 4: Development and aging of the body systems. Human Kinetics, Champaign, Illinois, pp 63 82 6. Piontelli A (2006) On the onset of human fetal behavior. In: Mancia M (ed) Psychoanalysis and neuroscience, chap 15. Springer, Milano Berlin Heidelberg, pp 415 442 7. Haywood KM, Getchell N (2001) Life span motor development, chap 5: Early motor development. Human Kinetics, Champaign, Illinois, pp 85 100 8. Lederman SJ, Klatzy RL (1998) The hand as a perceptual system. In: Connolly KJ (ed) The psychobiology of the hand. Chapter 2, Mac Keith Press, London, pp 16 35 9. Newell KM, McDonald PV (1997) The development of grip patterns in infancy. In: Connolly KJ (ed) The psychobiology of the hand, chap 12. Mac Keith Press, London, pp 232 256 10. Napier J, Tuttle RH (1993) Hands. Princeton University Press, Princeton, New Jersey 11. Jones LA, Lederman SJ (2006) Human hand function. Oxford University Press, Oxford 12. Latash ML (2008) Neurophysiological basis of movement, 2nd edn, chap 24: Prehension. Human Kinetics, Champaign, Illinois, pp 241 248 13. Wilson FR (1999) The hand. Vintage Books, London 14. Rocaht P (1993) Hand mouth coordination in the newborn: morphology, determinants, and early development of a basic act. In: Savelsbergh GJP (ed) The development of coordination in infancy, chap 10. Elsevier, Amsterdam, pp 265 288 15. Kurjak A, Azumedi G (2003) Fetal hand movements and facial expressions in normal pregnancy studied by four dimensional sonography. J Perinat Med 31:496 508 16. Dodwell PC, Muir DW, DiFranco D (1976) Responses of infants to visually presented objects. Science 194:209 211 17. Bard C, Fleury M, Gagnon M (1990) Coincidence anticipation timing. An age related perspective. In: Brad C, Fleury M, Hay L (eds) Development of eye hand coordination across the life span. University of South Carolina Press, Columbia, pp 283 305 18. Butterworth G, Verweij E, Hopkin B (1997) The development of prehension in infants. Br J Dev Psychol 15:223 236 19. Gallagher S (2005) How the body shapes the mind. Oxford University Press, Oxford 20. Paillard J (1999) Body schema and body image: a double dis sociation in deafferentiated patients. In: Gantchev GN, Mori S, Massions J (eds) Motor control today and tomorrow. Akademico Izdatelstvo, Sofia 21. Rossetti YG, Rode G, Boisson D (1995) Implicit processing of somaesthetic information: a dissociation between where and how? Neuroreport 6:506 510 22. Mishara AL (2005) Body self and its narrative representation in schizophrenia. In: De Preester H, Knockaert V (eds) Body image and body schema. John Benjamins, Amsterdam 23. Dorland’s Medical Dictionary (2007) 31st edn. Saunders, Philadelphia

Facial Expressions

7

With the assistance of Florinda Ceriani, Roberto Fogliani and Alessandra Kustermann

Keywords Physiognomy • Vocalizations • Anger • Disgust • Fear • Happiness • Sadness • Surprise • Tongue protrusion • Cross-modal integration • Mirror neurons • Autism

The introduction of 4D ultrasonography has made it possible to study the ontogeny and development of facial expressions in utero, albeit with some limitations. Interest in facial expressions dates back to antiquity and for centuries had to do with reading facial morphology or so-called ‘physiognomy’ (from the Greek words physys meaning nature and gnosis meaning knowledge). Aristotle wrote the first treatise on physiognomy in which he compared physiognomic traits of various people with animals. Such traits were assumed to indicate various tendencies ranging from stupidity to courage. Still today we say that so-and-so has an equine or horse-like face or an aquiline nose (from the Latin aquila meaning eagle). Pythagoras, Hippocrates and Galen used physiognomy as an important medical investigative tool for diagnosing pathology (from the Greek pathos meaning to suffer or display an emotion, and the Latin patior indicating suffering and affliction). If someone had a bilious face or was a lymphatic type, it was considered to indicate a possible weakness of the underlying apparatuses. In the Middle Ages facial morphology shifted from providing clues about temperament to indicating fate. We still say that someone has a ‘ominous face’ [1, 2]. In the eighteenth century, under the influence of a Swiss protestant pastor, Johannes Caspar Lavater, people started looking for traces of sanctity and marks of God in the eyes and creases and lines of the face. Cesare Lombroso (1835 1909), an Italian jurist and physician and the founder of ‘criminal anthropology’, introduced yet another change by A. Piontelli, Development of Normal Fetal Movements. © Springer Verlag Italia 2010

looking for criminal tendencies in those unfortunate individuals who carried marks of having never progressed from animals or from ‘savages’ [1]. The first to fully introduce emotions in face-reading was the French neurologist Guillaume-Benjamin Duchenne de Boulogne (1806 1875) who, in taking up Galvani’s studies on muscular contraction applying electrical stimuli to frogs’ limbs, applied small electric shocks to the facial muscles of his patients to understand and demonstrate the functioning of facial expressions. His distinction between a felt and a false smile was particularly important for later studies. The differentiation between felt versus false facial expressions has been the subject of innumerable researches and is still hotly debated. According to Duchenne, the ‘felt’ smile is accompanied by ‘wincing’ the lateral contraction of a facial muscle called orbicularis oculi, which regulates the closure of the eyelids. A portion of the muscle is not controlled by volition. Its involuntary contraction would thus reveal the spontaneity or otherwise of a socalled ‘Duchenne’ or ‘non-Duchenne’ smile [3]. Although not universally accepted, this distinction is still widely used. Duchenne’s work had a great influence on Darwin, who is universally credited with having regarded facial motion as displays of emotions in his work ‘Expression of the emotions in man and animals’. The word ‘expression’ is derived from the Latin exprimere meaning representing and showing with clarity. Darwin started observing facial expressions in animals and in the hu-

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7 Facial Expressions

man newborn, namely his cousin’s son and his own children. Darwin wrote that facial expressions are universal, not learnt, but biologically determined, and are the product of man’s evolution. Darwin also claimed that there are specific inborn emotions which are expressed even in the neonate and serve a basic survival function. However, Darwin did not regard expressions as having a communicative function, nor were facial expressions of particular interest to him. Following Darwin’s work the study of facial expressions has become a central theme in many disciplines ranging from psychology to genetics [4].

7.1 Basic Emotions The communicative and emotional sides of facial expressions, originally neglected by Darwin, have become particularly hot topics. Especially relevant is the work of Ekman and Friesen, who in 1971 distinguished six

primary emotions each accompanied by a distinct facial expression. These so-called basic emotions are anger, disgust, fear, happiness, sadness and surprise [5] (Fig. 7.1). Although mixed emotions and correlated mixed expressions are increasingly being recognized, Ekman and Friesen’s classification is still widely used. Currently debates and research centre on many topics. Those relevant to the fetus are the innateness of facial expressions, their universality, communicative function, and changeability through experience [6 10]. To solve these and other basic questions, scientists have been searching for nocturnal non-vocalizing primates, or for blind and possibly deaf neonates. Grimacing without the possibility of using vision and audition would imply a genetically programmed innate reflex motion, without any imitational or learnt component. So far nobody has been able to find these ‘experiments in nature [6]. Yet the human fetus studied longitudinally could be such an ‘ideal’ creature. Audition and, especially, vision begin to function late in the fetus, and

a

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Fig. 7.1 From 25 weeks’ gestation fetuses can display the facial expressions accompanying so called ‘basic emotion’. a c, e g Fetuses at 25 weeks’ gestation. d Fetus at 20 weeks’ gestation. All basic emotions are displayed by the facial expressions of the fetuses. a The expression displayed by this fetus could be classified as anger. The cavity under the nose is not due to a malformation, but to the current limitations of our equipment. b The expression displayed by this fetus could be classified as disgust. c The expression displayed by this fetus could be classified as fear. d The expression displayed by this fetus could be classified as happiness. Fetus d is younger than the others, the smile being the first facial expression to be noted in fetuses. e The expression displayed by this fetus could be classified as sadness. f The expression displayed by this fetus could be classified as surprise

7.1 Basic Emotions

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a a

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Fig. 7.2 Blank expression in the early fetus. a, b Fetuses at 13 weeks’ gestation. At this early stage fetuses display a static, blank expression. Muscle, skin and bone formation as well as innerva tion are all still in the early stages and do not allow more varied facial expressions

vocalizations only start after birth. Before 14 16 weeks the fetal face generally looks impassively blank and it would probably be classified as ‘static’ by those trying to study facial expression in the adult (Fig. 7.2). In 1971 Van Hoof observed smiling in several primates, and since then smiling has been considered amongst the most universal and phylogenetically old signals [11]. Anatomically speaking, a smile is the simplest of all expressions, as it requires in its simplest form the contraction of only one facial muscle, the greater zygomatic, innervated like the overwhelming majority of muscles involved in facial expressions by the facial or seventh cranial nerve and its branches. Central or peripheral palsy of the facial nerve impinges deeply on facial expressions on the affected side. The smile is the first facial expression which appears in the fetus. Occasional smiles can be noted from around 15 to 16 weeks. Fetuses begin to smile slightly more consistently between 18 20 weeks and they do so predominantly during cycles of rest (Fig. 7.3). According to

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Fig. 7.3 Early smiles. a Fetus at 20 weeks’ gestation. b, c Fetuses at 17 weeks’ gestation. All fetuses smile. Smiling is the simplest of all facial expressions and the first facial expression to be dis played clearly

Duchenne’s classification, up to 25 weeks fetal smiles would be categorized as ‘false’ [3], not only as the eyes

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a

necessarily do not participate in the expression, but also because the involvement of the lower face and especially of the forehead in the smile is limited. One could say that initially fetuses barely smile. By 25 weeks fetal smiles have evolved to big smiles (Fig. 7.4). From mid-pregnancy facial expressions begin to appear consistently, including ‘negative emotions’ which require the involvement and coordination of more than one muscle. Both positive and negative expressions surface in particular during cycles of rest. Surprise is hardly noted before 25 weeks. However, surprise is the briefest of our facial expressions, lasting only a fraction of a second [3]. It could be that 4D ultrasonography cannot capture it as it cannot capture other fast movements such as startles or breathing. Disgust, on the other hand, can occasionally be noted. Tongue protrusion per se is not properly a facial expression. However, in many cultures it indicates varying degrees of hostility towards the addressee. In utero tongue protrusion cannot have a derogatory connotation, although many parents interpret it as such and laugh. Tongue protrusion begins to be observed at about 18 20 weeks. Tongue protrusion also evolves: it starts as a straight sticking out of the tongue, and develops into more complex lateral motions (Fig. 7.5). Some opening movements of the mouth, apparently non-classifiable as expressions, begin to surface between 24 and 25 weeks. Comparing these with the facial display of neonatal vocalizations, the similarity is striking. Neonatal vocalizations are overwhelmingly composed of vowels. Clearly fetuses do not vocalize in utero; however, they may be preparing to do so after birth (Fig. 7.6). All these are unlearnt movements.

7.2 Cross-Modal Integration

b

Fig. 7.4 Full smile. Fetus at 25 weeks’ gestation. The fetus can now display a full smile. In addition to the wide opening of the mouth, ‘wincing’ can also be noted. This smile lasted more than 10 s

In 1977 Andrew Meltzoff and Keith Moore published a ground-breaking paper, ‘Imitation of facial and manual gestures by human neonates,’ in which they described how infants between 12 and 21 days old can imitate adult facial (and manual) gestures. Subsequently infants were found capable of imitation from birth [12]. Early facial imitation had been previously regarded as impossible. For instance, Piaget thought that facial imitation did not occur before 8 12 months [13]. The research had widespread implications for a range of studies

7.2 Cross-Modal Integration

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Fig. 7.5 Tongue protrusion. a c Fetuses at 25 weeks’ gestation. All fetuses protrude their tongue. However, tongue protrusion is executed in different ways and indicates different facial expressions. a Tongue protrusion is accompanied by wide opening of the mouth, corrugation of the forehead and tightening of the eyelids. The fetus seems to be crying angrily. b The opening of the mouth is minimal, with just the tongue sticking out. The tip of the tongue is slightly curled and the face rather impassive. The fetus seems to be ready to lick something. c Tongue protrusion is minimal, with wide opening of the mouth. The eyelids are slightly raised and the forehead distended. The etus seems to be ready to utter a sound

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Fig. 7.6 Preparing to utter vowels. a Fetus at 20 weeks’ gestation. b Fetus at 25 weeks’ gestation. Both fetuses look as if they could utter a vowel, possibly an O or an E. c, d Fetus at 22 weeks’ gestation. The mouth can be seen as a black hole. The nostrils are clearly visible in c and the nose appears as an oblong protuberance in d. Both mouth openings were of short duration, unlike yawns, nor was mouth opening repeated as in swallowing. In c the fetus seems to be uttering an A, and in d an O

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and topics. Relevant to fetuses and to neonates is socalled cross-modal integration, the integration of information from different sensory modalities. Fetuses do not use vision while in utero and yet they do imitate some facial expression in the adult soon after birth. How can they do so? In the Meltzoff and Moore experiment the assumption was that in order to imitate a facial gesture such as a tongue protrusion or mouth opening it was necessary for the infant to translate its experience from one sense modality, vision in the infant very close to its first vision into another sense modality, proprioception [14]. The question, which became known as the Molyneux question, was first raised by the Irish scientist and politician William Molyneux in a famous letter dated 7 July 1688 to the philosopher John Locke, and reformulated in a second letter dated 2 March 1693 as follows: Suppose a man born blind, and now adult, and taught by his touch to distinguish between a cube and a sphere of the same metal, and nighly of the same bigness, so as to tell, when he felt one and the other, which is the cube, which is the sphere. Suppose then the cube and the sphere placed on a table, and the blind man be made to see: quaere, whether by his sight, before he touched them, he could now distinguish and tell which is the globe, which is the cube? [15, 16]. Basically Molyneux was asking whether tactile sensation could be transferred to vision in someone who had been born blind. Historically, answers to the Molyneux problem have been related to the issue of the first perception in the newborn. The Meltzoff and Moore experiment showed that perception is intermodal from the start. Experience in one sense ‘educates’ other sense modalities [14, 17 19]. Fetuses start practising facial gestures and expressions close to mid-pregnancy. From then on fetuses display facial expressions that we would classify as smile, or cry, or even silent vocalizations, and they certainly stick out their tongues. One could thus turn the matter round and say that facial expressions which have long been practised in utero are transferred to the visual modality at birth. This response would thus not be pure imitation but some form of recognition. Infants ‘recognize’ with sight what they have long rehearsed in utero. The work of Rizzolati and his colleagues seems to hold a promising response to Molyneux’s query, with the discovery of so-called mirror neurons. Mirror neurons would provide, amongst other things, an ‘action recognition’ mechanism, meaning the capacity to rec-

7 Facial Expressions

ognize the action and the intention in the other. The mirror neuron system is most likely to be the substrate not only of action understanding the understanding of other’s intentions but possibly of emotion reading and empathy [20, 21]. Humans share mirror neurons with monkeys; however, it is understandable that little research has been conducted so far with humans and infants. Nevertheless, it could be postulated that the nascent mirror neurons of the neonate would allow it to recognize the action of the other and respond by, for example, opening its mouth wide or sticking out its tongue. Other researchers working with infants have postulated that they can appreciate correspondence between their own actions and those of others who are interacting with them [22].

7.3 Preparing for Post-Natal Communications The practising of facial expression and silent vocalizations in utero may be relevant because of another implication. Through facial expressions we can read the intentions and states of the other. If neonates were born without an expressive repertoire, their caregivers would be at a loss in trying to understand and respond to their needs. The pre-verbal child needs to be able to produce facial expressions in order to express its requirements (Fig. 7.7). If an infant cries, the mother takes an action and picks it up, cradles, feeds or puts it down to sleep according to various characteristics associated with the cry. The infant smile is a powerful tool to captivate the attention of the caregiver and elicit a sympathetic response, driving him or her to become involved in an interaction. The same can be said of infant vocalizations, which stir the mother to engage in a so-called proto-conversation. The term ‘proto-conversation’ was first coined by Elizabeth Bates in the 1970s to describe how infants respond to their mothers’ talk with appropriately timed smiles or coos, in give-and-take dialogue-like pattern [23]. Tactile and kinetic (meaning stimulation by motion or motions) modes can be added to the proto-conversation. In this dialogue, mothers talk in ‘baby talk’ or ‘mother-ese’, more properly called ‘child-directed speech’. The intonation of baby talk is different from that of ordinary adult speech, being high pitched, with short and simple words, repetitions, and many glissando variations. Baby talk contributes to

7.4 Parental Reactions

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Fig. 7.7 a-f Relaxed and sound asleep. All these fetuses look relaxed and sound asleep. The images were taken during a cycle of rest. However, wakefulness is only noted towards the end of gestation. Mothers looking at infants with a ‘sound asleep’ facial expression would not normally attempt to wake them. Even an ‘asleep’ expression (accompanied by other signs after birth) does thus communicate a need which the caregiver is able to understand, in this case the need to sleep. ‘Sound asleep’ is quite different from the blank expression seen in Fig. 7.2, which disquiets mothers as they cannot read it

mental development and to the development of speech [23]. Although fetuses are clearly a long way away from speech, when engaged in displaying facial expressions they may be paving the way for future language as well as for other future social interactions. In contrast to many other movements, facial expressions practised in utero may have an entirely anticipatory role, and a primary one for the start of intersubjectivity, the entry in a social world. During the fetal stage facial expressions do not have a direct and immediate communicative purpose. Fetuses prepare to communicate and by birth are equipped to do so, but within the uterus they have nobody to communicate with.

7.4 Parental Reactions Having said this, it is interesting to hear and see parental reactions to facial expressions during a scan. The impassive, blank 3D or 4D image of a fetal face before 16 weeks is perceived as strange and disquieting by

most mothers, who comment, ‘It looks like an alien’ or ‘It is almost frightening’. The face is supposed to be communicative, emotional and relational par excellence. A blank face elicits unsettling and alarmed feelings. On the other hand, whenever fetuses display a facial expression, an emotional state is immediately attributed to whatever the expression is. When negative expressions are displayed, some go as far as wanting to soothe the unborn. These same expressions will play a very important role in eliciting parental care after birth, and especially so during the pre-verbal period. However, had we not unveiled the expression with the ultrasound scan, no mother would find the ‘blank’ fetus frightening, just as no mother would think of soothing the fetus because at that moment it looks as though it is crying. Facial expressions in utero last only 1 3 s (Fig. 7.8). The ‘crying’ fetus spontaneously ceases to do so after 2 3 s. Prolonged ‘crying’ is not observed. Nevertheless, 4D ultrasonography, by reconstructing and ‘freezing’ the image of the crying fetus, also freezes time and

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Fig. 7.8 a-d Rapidly changing expressions. Fetus at 20 weeks’ gestation. These four images were captured only seconds apart from each other. Facial displays rapidly change even minimally in utero as in life after birth

speed. Mothers seeing the frozen image dilate time and worry that the cry may be long-lasting. One should ask whether these facial displays may have some hedonic tone. The question has been thoroughly investigated à propos of pain. The Royal College of Obstetricians and Gynaecologists set up a working party on fetal awareness and issued a report in October 1997 [24]. On pages 15 and 16 the report states: ‘In conclusion, the thalamus begins to mature earlier than the cortex but its function beyond a simple relay depends on connections with higher levels of the nervous system which do not begin before 22 weeks’ gestation.

A functional cortex is essential if the fetus is to be aware or to perceive external events… Relatively little is known about human cortical development but a critical fact is that thalamocortical connections are first observed penetrating the frontal cortical plate at 26 34 weeks’ gestation. Therefore, before that time there is no sensory input to the cortex’ [24]. Up until 25 weeks, just as for pain, a hedonic tone is hard to postulate, and even harder to demonstrate. Matters could be different for a slightly older fetus, and even very different for a fetus approaching birth. Communicative purposes are not immediately rele-

7.5 Yawning: a Form of Communicating?

vant during intrauterine life. Fetuses may be preparing for communication, but they certainly do not need to communicate their emotional states in utero. During the first half of pregnancy the substrate that could support emotions or even perceive sensations is simply not there. As Peter Hepper says, sensing is not to be equated with perceiving a more complex operation involving the interpretation of the sensations to give them meaning [25]. We just do not know when perceiving starts. Possibly, just as with consciousness, perceiving is not an either/or phenomenon but one that is gradually built up with varying degrees and shades. Probably a 20- to 25-week fetus can only sense what a mature neonate can perceive, and up to 25 weeks when fetuses smile they are not expressing a deep inner state of joy. They may possibly sense pleasurable or unpleasurable perceptions. However, this is difficult to demonstrate.

7.5 Yawning: a Form of Communicating? Finally, a few additional words on yawning. Provine, the researcher who studied many of its facets, considered it a facial expression with a communicative function after birth. Jean Piaget was the first to make an important observation in 1951: that children started yawning in response to seeing a yawn only during the 2nd year of life [13]. Subsequently, Provine [26] and Anderson and Meno [27] proved experimentally that contagiousness of yawning did not start reliably in children under 6 years old. This finding aroused a lot of interest from two main points of view. Following the seminal studies of Meltzoff and Moore [12], it has long been known that newborns are capable of recognizing

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and imitating most facial expressions. Many scientists wonder why they do not do the same with such a dramatic facial expression as a yawn. Recently, yawning has met with renewed interested linked with studies of mirror neurons and autism. So-called autistic spectrum disorders are characterized by a more or less profound impairment in communicative capacities and shared social interactions. Autistic individuals have problems in relating to others and in reading other people’s emotional states. In particular, they are unable to display empathic reactions when others show pleasure, fear or pain. Empathy is connected with the capacity to recognize, understand and share the emotions of others [28]. A number of anatomical and functional studies all seem to point to disfunctioning of the above-mentioned mirror neuron system in autism [29, 30]. The fetus and the neonate generally are not ‘autistic’, yet, as Piaget pointed out, they cannot imitate and possibly decode yawns in others [13]. This is just an hypothesis, but what if one turned the matter round and saw yawning as an albeit unconscious form of communicating various states to the caregiver. When mothers see a neonate yawning, they assume, depending on the context, that the child must be sleepy, waking up, or even hungry. In other words, at the neonatal stage yawning could be an important tool for directing the efforts of the caregiver onto ‘the right track’ (Fig. 7.9). Up to 2 years of age, and before they become fully verbal, children need a lot of empathic understanding on the part of those caring for them. Furthermore, sleep and hunger are two basic and vital states. A caregiver can miss many other nuances, but not these vital needs.

Fig. 7.9 Fetal yawn. Fetus at 22 weeks’ gestation (the same as in Fig. 7.6 c, d). The mouth, seen as a black hole, is wide open and the yawn lasted 6 s. Interestingly, this rather non human image (the fetus seen from below looks almost like a rat) had an ‘infec tious’ impact on the mother, who started yawning too

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Yawning, unlike crying and screaming, elicits empathy and sympathy, not irritation, anxiety or exasperation, thus simplifying the task. Furthermore, in children yawning would not need to be bidirectional. When babies and children are tired, and they communicate this by yawning, the caregiver usually takes the initiative to put them to bed. At such moments they may like to be lulled to sleep, or be read a repetitive story, but clearly are not willing to engage in complex social interactions. On the other hand, though, babies (and young children) are not keen to recognize fatigue or boredom in their caregiver’s face when she or he yawns while they may be needing or demanding some action or interaction. As the saying goes, ‘Children’s needs come first’. Mother or father may be tired, but still have to prepare some food or be asked to participate in some story-telling or preparatory ritual for sleep. If this were the case, fetuses yawning in utero would be displaying a preparatory and anticipatory function, helping them to have their vital needs better understood and more easily met by those caring for them after birth.

References 1. Physiognomy: Webster’s timeline history, 1226 2007. Icon Group, San Diego 2. Khune L (1917) The science of facial expressions. New edn 2008. Health Research, Pomeroy, Washington 3. Duchenne de Boulogne GB (1862) The mechanism of human facial expression. Cuthbertson RA (ed and trans) (1990) Cam bridge University Press, Cambridge 4. Ekman P (2006) Darwin and facial expressions: a century of research in review. Malor Books, Cambridge, Massachusetts 5. Ekman P, Friesen WV (2003) Unmasking the face, 10th edn. Malor Books, Cambridge, Massachusetts 6. Fridlund AJ (1994) Human facial expressions: an evolutionary view. Academic Press, San Diego 7. Izard CE (1971) The face of emotion. Appleton, New York 8. Russell JA (1994) Is there universal recognition of emotion from facial expression? Psychol Bull 15:102 141 9. Hinde RA (1985) Was ‘the expression of emotions’ a misleading phrase? Animal Behav 33:985 992 10. Kagan J (1978) On emotions and its development: a working paper. In: Lewis M, Rosenblum LA (eds) The development of affect. Plenum Press, New York 11. Van Hoof JARAM (1976) The comparison of facial expressions

7 Facial Expressions in man and higher primates. In: von Cranach M (ed) Methods of inference from animal to human behaviour. Aldine Press, Chicago 12. Meltzoff AN, Moore MK (1977) Imitation of facial and man ual gestures by neonates. Science 198:75 78 13. Piaget J (1951) Play, dreams and imitation in childhood. Nor ton, New York 14. Spelke E (1976) Infants’ intermodal perception of events. Cogn Psychol 8:553 560 15. Degenaar M, Lokhorts GJ (2005) Molyneux problem. In: Stan ford Encyclopedia of Philosophy. http:/plato.stanford.edu/en tries/molyneux problem/. Accessed 12 Feb 2010 16. John Locke (1690) An essay concerning human understand ing, 2nd edn. Clarendon Press, Oxford 17. Gopnik A, Meltzoff AN, Kull P (1999) The scientist in the crib. William Morrow, London 18. Schmuckler MA, Jewell DT (2007) Infants’ visual proprio ceptive intermodal perception with imperfect contingency information. Dev Psychobiol 49:387 398 19. Russel JA, Fernandez Dol JM (1998) The psychology of fa cial expressions. Cambridge University Press, Cambridge 20. Rizzolati G, Fadiga L, Fogassi L, Gallese V (2002) From mirror neurons to imitation: facts and speculations. In: Meltzoff AN, Prinz W (eds) The imitative mind: development, evolution, and brain bases. Cambridge University Press, Cambridge 21. Rizzolati G, Sinigaglia C (2008) Mirrors in the brain: how our minds share actions, emotions, and experience. Oxford University Press, Oxford 22. Stern DN (1985) The interpersonal world of the infant. Basic Books, New York 23. Bates E, Bretherton I, Snyder LS (1991) From first words to grammar: individual differences and dissociable mechanisms. Cambridge University Press, Cambridge 24. The Royal College of Obstetricians and Gynaecologists (1997) Fetal awareness: report of a working party. RCOG Press, London 25. Hepper PG (1992) Fetal psychology. An embryonic science. In: Nijhuis JG (ed) Fetal behavior: developmental and peri natal aspects. Oxford University Press, Oxford 26. Provine RR (1989) Contagious yawning and infant imitation. Bull Psychon Soc 27:125 126 27. Anderson JR, Meno P (2003) Psychological influences on yawning in children. Curr Psychol Lett Behav Brain Cogn 11, vol 2, pp 1 7 28. Schmuckler MA, Jewell DT (2007) Infant’s visual proprio ceptive intermodal perception with imperfect contingency information. Dev Psychobiol 4:387 398 29. Jacoboni M (2008) Mirroring people: the new science of how we connect with others. Farrar, Straus and Giroux, New York 30. Trevarthen C, Aitken KJ, Papoudi D, Robarts JZ (1996) Chil dren with autism: diagnosis and interventions to meet their needs. Jessica Kingsley, London

Rest-Activity Cycles, Clusters and the Ontogeny of Sleep

8

With the assistance of Luisa Bocconi, Chiara Boschetto, Florinda Ceriani, Alessandra Kustermann and Cinzia Zoppini

Keywords REM • Electro-oculogram • EEG • Children • Polysomnographic recordings • Active sleep • Quiet sleep • Fetal heart rate • Central nervous system • Wakefulness

Sleep is a very widespread, almost ubiquitous phenomenon. Mammals, birds, most reptiles, amphibians, and fishes sleep. Sleep has different characteristics throughout the animal kingdom [1, 2], but common ground can be found in the near-total inactivity, the decreased capacity to react to environmental stimuli, and the cyclic quality of sleep. Even insects and molluscs display prolonged sleep-like periods of inactivity. Given its widespread and peculiar nature, sleep has always fascinated, puzzled, and disquieted mankind. In antiquity sleep was considered a double-faceted phenomenon. On the one hand, it was regarded as a sweet merging with the realm of oblivion from which one reemerged to a new life, restored and reborn each new day. On the other hand, it was viewed as a plunge into a condition akin to death, the darkness and unconsciousness of the eternal sleep. The Greeks captured well this dual nature in their mythology as Hypnos, the god of sleep and the son of Night and Darkness, was the twin brother of Thanatos, the god of death. Dreams were not considered to be creations of those who dreamt them, but emanations visiting the dreamer from above, direct revelations radiating from the gods. As such, dreams were considered important for their predictive, prophetic qualities. All dreamt, but only a few could be dream interpreters, and only particular dreams were enlightening. Down the centuries sleep was largely disregarded for its restorative qualities, and considered almost solely as a container of enlightening dreams [3]. In 1900 Freud threw a whole new light on dreams, which he considered products of the individual psyche. A. Piontelli, Development of Normal Fetal Movements. © Springer Verlag Italia 2010

Dreams no longer came from the gods, but were psychological phenomena pertaining to the single individual. Dreams contained residues of our daily lives, and vestiges of our past, but especially unconscious, repressed thoughts. According to Freud, repressed wishes were mainly sexual in their content, and their meaning, being abhorrent to the waking mind, had to be uncovered and interpreted. Dreams were thus the ‘royal road’ to the unconscious, the main avenue to unveiling our repressed wishes. Sleep was almost entirely considered by Freud as the ‘guardian’ of dreams [4]. Sleep research devoid of dream interpretation properly began with the pioneering work of Aserinsky and Kleitman in Chicago. Interestingly, it was while observing sleeping infants that Aserinsky noticed periods of sleep characterized by bursts of eye movements. Following these preliminary observations the research was extended to adults. In 1955 two different states of sleep in the adult, one with eye movements (rapid eye movement or REM sleep) and one without (Non-REM or N-REM sleep) were described [5]. Alongside eye electrodes (the electro-oculogram, or EOG), William C. Dement, a student in the Kleitman laboratory, placed electrodes on the scalp of his subjects (the electroencephalogram, or EEG), which included infants, and discovered that during REM periods the brain displayed an intense activity similar to wakefulness, hence the name ‘paradoxical sleep’ [6]. Until then sleep had been regarded essentially as state of quiescence of the central nervous system. Other towering figures of early sleep research during

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the 1950s and the 1960s were Giuseppe Moruzzi in Italy and William C. Magoun in the USA, who observed the effects of lesions and stimulation at various levels in the brainstem, and Michel Jouvet in Marseille, who studied sleep predominantly in animal preparations [7, 8]. Following the golden era of the 1950s and the 1960s sleep research became widespread and pursued by many investigators. However, despite innumerable researches and many hypotheses, the full function of dreams still eludes our knowledge.

8.1 Sleep in Children For a long while children, especially young, pre-verbal children, were somewhat ignored by mainstream research. It is only fairly recently that so-called behavioural states in the neonate have been fully recognized and described using mixed criteria both by direct observation of neonates and by analysis of polysomnographic recordings, the joint recording of the EEG, EOG, muscular activity (electromyography, or EMG), electrocardiogram (or ECG), and various other parameters such as oxygen saturation and air flow [9]. The term ‘behavioural state’, signifying various sleeping and waking states, is currently used to indicate ‘clearly distinguishable and relatively stable functioning conditions of the organism periodically and predictably recurring over time’ [10, 11]. These functioning conditions comprise the presence or lack of bodily motions and ocular movements, the type of breathing, and specific characteristics of the EEG and of the EMG recorded at the level of the chin. Two basic types of sleep have been distinguished in the neonate. Some confusion has been created by the various names they have been given. One is active sleep, also called state 1, irregular, paradoxical, or REM sleep. The other is quiet sleep, also called state 2, or regular, or N-REM sleep. For reasons of clarity and simplicity only the terms active and quiet sleep will be used in this book. This terminology is also better suited to describing fetal phenomena pertaining to the first 25 weeks of pregnancy. During active sleep cardiac and breathing rhythms are irregular, breathing is paradoxical, apnoeas are possible, rapid eye movements are present, and so is intense and turbulent bodily motion, muscular tone is elevated, and the infant displays a variety of facial expressions. During quiet sleep all activities which come under the

8 Rest-Activity Cycles, Clusters and the Ontogeny of Sleep

control of the neuro-vegetative system are much more regular. Hence cardiac and breathing rhythms are regular, less accelerated and non-paradoxical. No rapid eye movements can be noted, muscular tone ‘falls’ and the overall motility is greatly reduced, being almost exclusively represented by startles and short, occasional local movements. At birth, active sleep is largely prevalent, but soon quiet sleep becomes increasingly predominant [12]. The concept of behavioural states is currently widely used and taken into account during the assessment of individual infants. Neonatologists wait until the infant is in a favourable state, neither fretting restlessly nor sound asleep, before examining it. Increasingly, parents who ask for a consultation about their children’s sleeping problems are helped to distinguish various states and to no longer regard some of these as distressing conditions, but as a predictable chain of naturally occurring events.

8.2 Behavioural States in Premature Infants and Mature Fetuses Behavioural states have been thoroughly investigated in the premature infant. Severely premature infants are continuously asleep and their eyes are kept almost constantly closed. However, they basically alternate between active and quiet sleep. During quiet sleep they are immobile and respiration, although generally assisted, is regular. Active sleep is characterized by more or less pronounced unrest, presence of startles, intermittent eye movements and irregular breathing with frequent apnoeas [13]. At 24 weeks the EEG is mostly silent, with some brief (