To my parents, Krystyna Dobraczynska and James Johnson, who provided both my nature and my nurture

This third edition first published 2011
© 2011 Mark H. Johnson

Edition history: Blackwell Publishers Ltd (1e, 1997); Blackwell Publishing Ltd (2e, 2005)

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Library of Congress Cataloging-in-Publication Data

Johnson, Mark H. (Mark Henry), 1960–
Developmental cognitive neuroscience : an introduction / Mark H. Johnson ; with Michelle de
Haan. – 3rd ed.
p. ; cm.
Includes bibliographical references and index.
ISBN 978-1-4443-3085-4 (hb : alk. paper) – ISBN 978-1-4443-3086-1 (pb : alk. paper)
1. Cognitive neuroscience. 2. Developmental neurobiology. I. De Haan, Michelle, 1969– II.
Title.
[DNLM: 1. Neuropsychology. 2. Brain–physiology. 3. Cognition. 4. Human Development.
WL 103.5 J68d 2011]
QP360.5.J64 2011
612.8’233–dc22

2010011925

List of Figures

Figures listed below without a page number appear in the color plate section. The color plate section appears between pages 138 and 139.

1.1 Seventeenth-century “spermist” drawing

1.2 Simple three-layered connectionist neural network

1.3 The epigenetic landscape of Waddington (1975)

2.1 An illustration of the relative strengths and weaknesses of different functional brain imaging methods used with infants and children (color plate)

2.2 An infant wearing a high-density ERP/EEG system (EGI Geodesic Sensor Net) during a study on the “mirror neuron system” (color plate)

2.3 An infant engaged in an optical imaging (NIRS) study (color plate)

2.4 The expansion of myelinated fibers over early postnatal development as revealed by a new structural MRI technique (color plate)

3.1 (a) The basic double helix structure of DNA (b) Detail showing how the two strands are linked by chemical bonds between the bases of neucleotides

3.2 The complex causal pathway between a genetic level defect and its consequences for behaviour from Fragile-X syndrome

4.1 Simplified schematic diagram showing cerebral cortex as a thin sheet composed of six layers

4.2 A typical cortical pyramidal cell

4.3 Embryonic and fetal development of the human brain

4.4 MRI structural scans of a 4-month-old infant (top) and a 12-year-old adolescent (below)

4.5 Cellular structure of the human visual cortex based on Golgi stain preparations

4.6 The sequence of axon myelination by an oligodendrocyte

4.7 Resting state networks in a single representative infant (color plate)

4.8 An approximate timeline for some of the most important changes in human brain development (color plate)

4.9 The development of density of synapses in human primary visual cortex

4.10 A colour-coded map of changes in cortical gray matter with development (color plate)

4.11 Trajectories of cortical development in “superior” and “average” intelligence groups (color plate)

4.12 Cytoarchitectural map of the cerebral cortex

4.13 The radial unit model of Rakic (1987)

4.14 Patterning of areal units in the somatosensory cortex

4.15 Developmental changes in local cerebral metabolic rates for glucose (ICMRGlc) in the normal human infant

5.1 Diagram of the developmental sequence of visual behavior and ventral- and dorsal-stream neural systems contributing to this

5.2 Simplified schematic diagram illustrating how projections from the two eyes form ocular dominance columns in the visual cortex

5.3 (a) Afferents from both eyes synapse on the same cells in layer 4 (b) Afferents are segregated on the basis of eye origin

5.4 Diagram representing some of the main neural pathways and structures involved in visual orienting and attention

5.5 The oculomotor delayed response task as designed for use with infants

5.6 Grand-average saccade-locked potentials at Pz in 6-month-old infants, 12-month-old infants, and adults

5.7 Three types of saccades made by young infants in response to two targets briefly flashed as shown

5.8 Heart-rate-defined phases of sustained attention

6.1 Major routes whereby retinal input reaches the dorsal and ventral streams

6.2 A diagram showing the object processing model of Mareschal et al. (1999)

6.3 Gamma-band EEG activity recorded from infants in the Kaufman et al. (2003) experiment (color plate)

7.1 Some of the regions involved in the human social brain network

7.2 Data showing the extent of newbornsߣ head and eye turns in following a schematic face, a scrambled face, and a blank (unpatterned) stimulus

7.3 Human newborn and model responses to schematic images

7.4 Outline sagittal view of the chick brain showing the main visual pathway to IMM

7.5 Schematic illustration of the stimuli that might be optimal for eliciting a face-related preference in human newborns

7.6 Selective activation to face, object and building stimuli across different age groups (color plate)

7.7 Example of the edited video image illustrating the stimulus for Experiment 1 in Farroni et al. (2000)

7.8 Results of the preferential looking study with newborns

8.1 The medial temporal lobe memory system

8.2 (a) Example of a sequence to be imitated (b) Production of actions by 20-month-old infants in a baseline period, at immediate recall after the sequence is demonstrated, and after a two-week delay (color plate)

8.3 Memory performance for Beth, Jon and Kate on the Rey-Osterrieh Complex Figure

9.1 Some of the key structures involved in language processing

9.2 Cortical areas showing increases in blood oxygenation on fMRI when normal hearing adults read English sentences, when congenitally deaf native signers read English sentences, and when congenitally deaf native signers view sentences in their native sign language (American Sign Language)

9.3 Covert language task: group average fMRI activation in the unaffected and affected members of the KE family (color plate)

10.1 A summary of the superior frontal-intraparietal network involved in the development of visuo-spatial working memory (color plate)

10.2 Interaction between wakefulness and the linguistic nature of the stimuli (color plate)

10.3 Summary of the sequence and anatomical distribution of the coherence patterns reported by Thatcher (1992)

10.4 (a) Rate of growth of EEC coherence between frontal and posterior lobes during middle childhood (F 7–P 3; Thatcher, 1992) (b) Rate of growth of working memory (counting span and spatial span) during the same age range

11.1 A summary diagram of the model proposed by Geschwind, Behan, and Galaburda

12.1 The formation of representations in the cortical matrix model under two different architectural conditions

12.2 An illustration of different kinds of brain connectivity

12.3 Developmental changes in interregional functional connectivity (color plate)

List of Tables

1.1 Levels of interaction between genes and their environment

2.1 A thumbnail sketch of some of the major developmental disorders

5.1 Summary of the relation between developing oculomotor pathways and behavior

5.2 Marker tasks for the development of visual orienting and attention

7.1 Stimulus-dependent effects of neurophysiological manipulations

12.1 Three viewpoints on human functional brain development

Preface to the Third Edition

In the 13 years since publication of the first edition of this book, the field of developmental cognitive neuroscience has expanded enormously, and the number of researchers active in the field, and the papers they produce, has increased by at least an order of magnitude. Accompanying this growth has been a plethora of conferences, edited volumes and monographs. This dramatic expansion has made the challenge of selecting what new material to include in this third edition somewhat daunting. As in previous editions, the selection of material reflects my own biases, but with a focus on domains in which there are clear examples of the developmental cognitive neuroscience approach. This inevitably means that there are topics in cognitive development or developmental neuroscience that are not addressed. The quantity of new work in the field also makes it increasingly difficult for one person to cover all areas. Therefore, I am very grateful that Michelle de Haan agreed to update and revise Chapters 8, 9 and 10 (previously 6, 7 and 8).

Like any introduction to a new interdisciplinary field, students and researchers come from different parent disciplines and, therefore, will bring different background expertise with them to reading this book. Thus, in order to improve the progression of build-up of knowledge for the reader, this edition includes two new background foundation chapters (2 and 3). The first of these introduces the established and new methods and paradigms that are critical for advances in the field, and also gives an overview of the different populations and developmental disorders that have been studied. The second new chapter reflects a major new trend in the field for the integration of molecular and population genetics with studies of brain development and function. Anticipating the increasing importance of this approach, the new Chapter 3 introduces the reader to the basics of genetics as relevant to developmental psychology and neuroscience.

Other significant revisions to several chapters of the book includes a greater focus on mid-childhood and adolescence, on practical applications of basic research, and on the emergence of functional networks of brain regions. In line with changes in the field, there is also increased discussion of data from different structural and functional imaging methods. Additionally, to assist the teacher there are now “key discussion points” provided at the end of each chapter, which can be used along with the website associated with the book (www.wiley.com/go/johnson/dcn) that has essay, short answer, and multiple choice test questions as well as downloadable figures. As with previous editions, this basic introduction serves as a “feeder” into more detailed and comprehensive edited volumes. Specifically, this third edition recommends many further readings from Nelson and Luciana’s excellent 2008 Handbook of Developmental Cognitive Neuroscience (2nd edn), and some readers may wish to use the two volumes together.

As with the previous editions, I am indebted to colleagues and collaborators for educating and informing me on a variety of topics in the field. My colleagues at the Centre for Brain and Cognitive Development, and our distinguished visitors to London, continue to keep me abreast of current developments in a variety of topics. I also continue to be indebted to those who have commented on chapters in this and previous editions of the book including Rick Gilmore, Michelle de Haan, Annette Karmiloff-Smith, Denis Mareschal, Gaia Scerif and Cert Westermann. Sarah Lloyd-Fox, Kim Davies, Amy Profères, Helena Ribeiro, and Leslie Tucker all contributed invaluably to the production of this edition.

Preface to the Second Edition

In the eight years since publication of the first edition of this book, developmental cognitive neuroscience has grown from newborn to toddler: still uncertain on its feet, but just beginning to put together fragments of knowledge. While the first edition was described by one leading figure as “a clarion call for a new way of doing both developmental psychology and cognitive neuroscience,” the present edition puts more emphasis on making sense of the data already in hand.

Since the last edition a number of trends have become apparent in the field. First, the field has actually settled on the phrase “developmental cognitive neuroscience” as the name that best describes it. While it could be said that the first edition was the book that gave the field its name, it is my hope that its most important contribution was in attracting new researchers to the topic. Another trend of note is that some of the more heated debates about both behavioral and neuroscience evidence are becoming resolved as more evidence from different sources and methods becomes available. A surprising amount of agreement is breaking out in the field, with many issues turning out to be not black or white, but a subtle and interesting shade of grey. A third trend in the field is the recent flurry of books and review chapters. This made me question whether or not there was still a need for this book. On reflection, however, I have convinced myself that a basic introduction that serves as a “feeder” into more detailed and comprehensive edited volumes is still valuable. In fact, teachers should note that this second edition is specifically designed to be used with one or more of three current edited volumes (Nelson & Luciana, 2001; Johnson, Munakata, & Gilmore, 2002; de Haan & Johnson, 2003), and specific recommendations for further reading from these volumes are highlighted throughout the text. Since our young field can often feel somewhat fragmented to the student, I continue to believe that the single voice and unified perspective presented in this book are important.

Because this book is intended as an introduction, its coverage is necessarily selective. While this was challenging for the first edition, the massive increase in data over the past years made the prospect of choosing what to exclude even more daunting. As in the first edition, my choices were guided by focusing on areas where the developmental cognitive neuroscience approach has been most avidly pursued, rather than topics dominated by a developmental psychology or an adult cognitive neuroscience approach. Needless to say, my own particular interests and biases are evident throughout.

As with the first edition, I am indebted to colleagues and collaborators for educating and informing me on a variety of topics. I was privileged to chair a panel to review the current state of our knowledge on the development of Perception, Attention, and Memory (funded by the McDonnell and Sackler foundations). The discussions and presentations at these meetings brought me up to date, and particularly helped with the new chapter on Objects and Number. My colleagues at the Centre for Brain and Cognitive Development, particularly Gergely Csibra and Denis Mareschal, kept me abreast of current developments in a variety of fields. Rick Gilmore, Gaia Scerif, and Gert Westermann kindly provided their comments on a draft of the revisions to the book. Michelle de Haan, Brian Hopkins, and Annette Karmiloff-Smith gave me comments on specific chapters. From Blackwell, Sarah Bird persuaded me to undertake the second edition, and Jennie Brown, Justin Dyer, Roberta Herrick, Katie Menssen, Leslie Tucker, and Agnes Volein all contributed invaluably to the production.

Teachers may wish to note that a website accompanies this book with teaching aids: www.wiley.com/go/johnson/dcn

Preface to the First Edition

In the first chapter of this book I describe some of the factors responsible for the recent emergence of a subdiscipline at the interface between developmental psychology and cognitive neuroscience. I have chosen to refer to this new field as “developmental cognitive neuroscience,” though it has been known under a number of other terms such as “developmental neurocognition” (de Boysson-Bardies, de Schonen, Jusczyck, McNeilage, & Morton, 1993). Though a series of edited volumes on the topic has recently appeared, like most newly emerging disciplines there is a time lag before the first books suitable for teaching appear. This book and the Reader which I edited in 1993 (Johnson, 1993) are initial attempts to fill the gap. While some may believe these efforts to be premature, my own view is that the lifeblood of any new discipline is in the students and postdocs recruited to the cause. And the sooner they are recruited, the better.

Is developmental cognitive neuroscience really significantly different from other fields that have a more extended history, such as developmental neuropsychology or cognitive development? Clearly, it would be unwise to rigidly demarcate developmental cognitive neuroscience from related, and mutually informative, fields. However, it is my belief that the emerging field has a number of characteristics that makes it distinctive. First, while there is some disagreement about exact definitions, the fields of developmental neuropsychology and developmental psychopathology focus on atypical development, while commonly comparing them to normal developmental trajectories. In contrast, cognitive neuroscience (including the developmental variant outlined in this book) focuses on normal cognitive functioning, but uses information from deviant functioning and development as “nature’s experiments” which can shed light on the neural basis of normal cognition. This book is therefore not intended as an introduction to the neuropsychology of developmental disorders. For such information the reader is referred to the excellent introductions by Cicchetti and Cohen (1995) and Spreen, Risser, and Edgell (1995).

Second, unlike many in cognitive development, this book adopts the premise that information from brain development is more than just a useful additional source of evidence for supporting particular cognitive theories. Rather, information about brain development is viewed as both changing and originating theories at the cognitive level. Third, developmental cognitive neuroscience restricts itself to issues at the neural, cognitive, and immediate environmental levels. In my view it is a hazard of some interdisciplinary fields that the focus of interest is diffused across many different levels of explanation. This is not to deny the importance of these other levels, but a mechanistic interdisciplinary science needs to restrict both the domains (in this case aspects of cognitive processing) and levels of explanation with which it is concerned. Finally, developmental cognitive neuroscience is specifically concerned with understanding the relation between neural and cognitive phenomena. For this reason, I have not discussed evidence from the related field of developmental behavior genetics. In general, developmental behavior genetics tends to be concerned with correlations between the molecular level (genetics) and gross behavioral measures such as IQ. With some notable exceptions, little effort is made to specifically relate these two levels of explanation via the intermediate neural and cognitive levels. Having pointed out the different focus of developmental cognitive neuroscience, my hope is that this book is written to be both accessible and informative to those in related and overlapping disciplines.

The above comments go some way to explaining the choice of material that I have presented in the book. However, I have no doubt that there is a substantive amount of excellent experimentation and theorizing that could have been included but was not. Since this is intended as a brief introduction to the field, I have chosen to focus on a few particular issues in some detail. Of course, the choice of material also reflects my own biases and knowledge since the book is intended as an introductory survey of the field as viewed from my own perspective. I apologize in advance for the inevitable omissions and errors.

The book is aimed at the advanced-level student and assumes some introductory knowledge of both neuroscience and cognitive development. Students without this background will probably need to refer to more introductory textbooks in the appropriate areas. I also hope that the book will attract developmentalists with an interest in learning more about the brain, and cognitive neuroscientists curious as to how developmental data can help constrain their theories about adult functioning. But most of all I hope that the book inspires readers to find out more about the field, and to consider a developmental cognitive neuroscience approach to their own topic.

Acknowledgments

The author and publishers gratefully acknowledge the following for permission to reproduce copyright material:

Figure 2.1 from S. Lloyd-Fox, A. Blasi and C.E. Elwell (2010) Illuminating the developing brain: The past, present and future of functional near infrared spectroscopy. Neuroscience and Biobehavioural Reviews. Reprinted with permission from Elsevier.

Figure 2.2 reprinted by permission of Michael Crabtree.

Figure 2.3 reprinted by permission of Sarah Lloyd-Fox.

Figure 2.4 images courtesy of Dr Sean Deoni, King’s College London and Brown University.

Figure 3.1 from J. Stiles (2008) The fundamentals of brain development: Integrating nature and nurture. Cambridge, MA: Harvard University Press. Copyright © 2008 by the President and Fellows of Harvard College. Reprinted by permission of the publisher.

Figure 3.2 from K.M. Cornish, J. Turk, J. Wilding, V. Sudhalter, F. Munir, F. Kooy, and R. Hagerman (2004) Annotation: Deconstructing the attention in fragile X syndrome: A developmental neuropsychological approach. Journal of Child Psychology and Psychiatry, 45, 1042–1053. Reprinted by permission of Wiley-Blackwell.

Figure 4.4 images courtesy of the Centre for NeuroImaging Sciences, King’s College London and the Birkbeck-UCL Centre for NeuroImaging.

Figure 4.5 from J. LeRoy Conel (1939–1967) The postnatal development of the human cerebral cortex, vols. I–VIII. Cambridge, MA: Harvard University Press, Copyright © 1939, 1941, 1947, 1951, 1955, 1959, 1963, 1967 by the President and Fellows of Harvard College. Reprinted by permission of the publisher.

Figure 4.6 from J. Stiles (2008) The fundamentals of brain development: Integrating nature and nurture. Cambridge, MA: Harvard University Press. Copyright © 2008 by the President and Fellows of Harvard College. Reprinted by permission of the publisher.

Figure 4.7 from P. Fransson, B. Skiöld, S. Horsch, A. Nordell, M. Blennow, H. Lagercrantz, and U. Aden (2007) Resting-state networks in the infant brain. Proceedings of the National Academy of Sciences, USA, 104, 15531– 15536. Copyright © 2007 National Academy of Sciences, USA. Reprinted by permission of the publisher.

Figure 4.8 from B. J. Casey, N. Tottenham, C. Liston, and S. Durston (2005) Imaging the developing brain: What have we learned about cognitive development? Trends in Cognitive Sciences, 9,104–110. Which is a modified version of a figure from R. A. Thompson and C. A. Nelson (2001) Developmental science and the media: Early brain development. American Psychologist, 56, 5–15. Copyright © 2005 Elsevier Ltd. Reprinted by permission of the publisher.

Figure 4.10 from A. W. Toga, P. M. Thompson, and E. R. Sowell (2006) Mapping brain maturation. Trends in Neuroscience, 29, 148–158. Reprinted by permission of Dr Arthur W. Toga and Dr Paul M. Thompson, Laboratory of Neuro Imaging at UCLA.

Figure 4.11 from P. Shaw, D. Greenstein, J. Lerch, L. Clasen, R. Lenroot, N. Gogtay, A. Evans, J. Rapaport, and J. Giedd (2006) Intellectual ability and cortical development in children and adolescents. Nature, 440, 676–679. Reprinted by permission of Nature Publishing Group.

Figure 7.5 from M. H. Johnson (2005) Sub-cortical face processing. Nature Reviews Neuroscience, 6, 766–774. Reprinted by permission of Nature Publishing Group.

Figure 7.6 from K. S. Scherf, M. Behrmann, K. Humphreys, and B. Luna (2007) Visual category-selectivity for faces, places and objects emerges along different developmental trajectories. Developmental Science, 10, F15–F30. Reprinted by permission of Wiley-Blackwell.

Figure 8.1 from F. Bloom, C. A. Nelson, and A. Lazerson (2001) Brain, mind, and behavior (3rd ed.), New York: Worth Publishers. Reprinted by permission of Worth Publishers.

Figure 8.2 from P. J. Bauer (2006) Constructing a past in infancy: A neuro-developmental account. Trends in Cognitive Sciences, 10, 175–181. Reprinted by permission of Elsevier Ltd.

Figure 8.3 from F. Vargha-Khadem, D. G. Gadian, K. E. Watkins, A. Connelly, W. van Paesschen and M. Mishkin (1997) Differential effects of early hippocampal pathology on episodic and semantic memory. Science, 277, 376–380. Reprinted by permission of AAAS.

Figure 10.1 from T. Klingberg (2006) Development of a superior frontal-intraparietal network for visuo-spatial working memory. Neuropsychologia, 44, 2171–2177. Copyright © 2006 with permission from Elsevier.

Figure 12.2 adapted from a figure by M. K. Belmonte, G. Allen, A. Beckel-Mitchener, L. M. Boulanger, R. A. Carper and S. J. Webb (2004) Autism and abnormal development of brain connectivity. The Journal of Neuroscience, 24, 9228–9231.

Figure 12.3 from K. Supekar, M. Musen, and V. Menon (2009) Development of large-scale functional brain networks in children. PLoS Biology, 7, el000157. Reprinted by permission of the authors and of Public Library of Science, Biology.

Abbreviations

ADHD

attention deficit/hyperactivity disorder

ASL

American Sign Language

CANTAB

Cambridge Neuropsychological Testing Automated Battery

DLPFC

dorsolateral prefrontal cortex

DNMS

delayed non-match to sample

EEG

electroencephalography

ERP

event-related potential

FEF

frontal eye fields

FFA

fusiform face area

fMRI

functional magnetic resonance imaging

GABA

Gamma-aminobutyric acid

HD-ERPs

high-density event-related potentials

IMHV

intermediate and medial part of the hyperstriatum ventrale

IS

interactive specialization

ISI

inter-stimulus interval

LGN

lateral geniculate nucleus

MGN

medial geniculate nucleus

MRI

magnetic resonance imaging

Nc

negative component

NIRS

near infra-red spectroscopy

PET

positron emission tomography

PFC

prefrontal cortex

PKU

phenylketonuria

PN

projection neuron

SLI

specific language impairment

SOA

stimulus onset asynchrony

SP

spike potential

STS

superior temporal sulcus

WS

Williams syndrome

1

The Biology of Change

In this introductory chapter I discuss a number of background issues for developmental cognitive neuroscience, beginning with historical approaches to the nature-nurture debate. Constructivism, in which biological forms are an emergent product of complex dynamic interactions between genes and environment, is presented as an approach to development that is superior to accounts that seek to identify pre-existing information in the genes or external environment. However, if we are to abandon existing ways of analyzing development in terms of “innate” and “acquired” components, this raises the question of how we should best understand developmental processes. One scheme is proposed for taking account of the various levels of interaction between genes and environment. In addition, a dissociation is introduced between innate representations and architectural constraints on the emergence of representations within neural networks. Following this, a number of factors are discussed that demonstrate the importance of the cognitive neuroscience approach to development, including the increasing availability of brain imaging and molecular approaches. Conversely, the importance of development for analyzing the relation between brain structure and cognition is reviewed. In examining the ways in which development and cognitive neuroscience can be combined, three different perspectives on human functional brain development are discussed: a maturational view, a skill learning view, and an “interactive specialization” framework. Finally, the contents of the rest of the book are outlined.

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