Emergent brain dynamics prebirth to adolescence

339 Pages·2018·42.51 MB·English

by  Benasich

April A. Benasich is Elizabeth H. Solomon Professor of neuroscience/cognitive science PE Emergent Brain Dynamics Emergent Brain Dynamics
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Molecular and Behavioral Neuroscience at Rutgers Contributors the Prebirth to Adolescence
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University–Newark, where she is also Director of the Sylvain Baillet, Marina Bedny, Yehezkel Ben-Ari, April A. Benasich, Olivier Bertrand, György tot
Carter Center for Neurocognitive Research. Urs Ribary Buzsáki, Alain Chédotal, Sam M. Doesburg, Gordon Fishell, Adriana Galván, Jennifer N. AB
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is Endowed BC LEEF Leadership Chair in Cognitive Gelinas, Jay Giedd, Pierre Gressens, Ileana L. Hanganu-Opatz, Rowshanak Hashemiyoon, da
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Neuroscience, Director of the Behavioral and Cognitive Takao K. Hensch, Suzana Herculano-Houzel, Mark Hübener, Matthias Kaschube, Michael S. le D
Neuroscience Institute (BCNI), and Professor in Psy- Kobor, Bryan Kolb, Thorsten Kolling, Jean-Philippe Lachaux, Ulman Lindenberger, Heiko scy
chology, Pediatrics, and Psychiatry at Simon Fraser J. Luhmann, Hannah Monyer, Sarah R. Moore, Charles A. Nelson III, Tomáš Paus, Patrick L. enna
University and the University of British Columbia in Purdon, Pasko Rakic, Urs Ribary, Akira Sawa, Terrence J. Sejnowski, Wolf Singer, Cheryl L. cm
Vancouver. Sisk, Nicholas C. Spitzer, Michael P. Stryker, Mriganka Sur, Peter J. Uhlhaas eic
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This volume in the Strüngmann Forum Reports series
explores the complex mechanisms that accompany the
dynamic processes by which the brain evolves and ma-
tures. Integrating perspectives from multiple disciplines,
“This volume of edited chapters by many leaders in this important fi eld of study is the product
the book identifi es knowledge gaps and proposes inno-
of one of the remarkable meetings organized by the Ernst Strüngmann Forum, based on an
vative ways forward for this emerging area of cross-
in-depth symposium examining and debating the details of the fundamentally important
disciplinary study. The contributors examine maturation
question, ‘How do early experiences infl uence brain development to determine who we
of nonlinear brain dynamics across systems from a
become?’ Much important information is provided by this infl uential volume, and essential
developmental perspective and relate these organizing
unresolved questions, problems, and concerns are elucidated, making this an important read
networks to the establishment of normative cognition and
for experts and for those newly introduced to the issues raised therein.”
pathology seen in many neurodevelopmental disorders.
—Fred H. Gage, Adler Professor, Laboratory of Genetics, Salk Institute for Biological Studies
The book looks at key mechanistic questions,
including: What role does dynamic coordination play
in the establishment and maintenance of brain net-
works and structural and functional connectivity? How
are local and global functional networks assembled
and transformed over normative development? To what
degree do oscillatory patterns vary across develop-
ment? What is the impact of critical periods, and which
factors initiate and terminate such periods? It also
aA edited by April A. Benasich and Urs Ribary explores the potential of new technologies and tech-
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dr niques to enhance understanding of normative develo p-
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The MIT Press
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Massachusetts Institute of Technology o
Cambridge, Massachusetts 02142 rs
http://mitpress.mit.edu
978-0-262-03863-8
90000
9 780262038638 ERNST STRÜNGMANN FORUM
Emergent Brain Dynamics
Prebirth to Adolescence
Strüngmann Forum Reports
Julia R. Lupp, series editor
The Ernst Strüngmann Forum is made possible through
the generous support of the Ernst Strüngmann Foundation,
inaugurated by Dr. Andreas and Dr. Thomas Strüngmann.
This Forum was supported by the
Deutsche Forschungsgemeinschaft
Emergent Brain Dynamics
Prebirth to Adolescence
Edited by
April A. Benasich and Urs Ribary
Program Advisory Committee:
Yehezkel Ben-Ari, April A. Benasich, Julia R. Lupp,
Charles A. Nelson III, Urs Ribary, Wolf Singer,
Terrence J. Sejnowski
The MIT Press
Cambridge, Massachusetts
London, England
© 2018 Massachusetts Institute of Technology and
the Frankfurt Institute for Advanced Studies
Series Editor: J. R. Lupp
Editorial Assistance: M. Turner, A. Ducey-Gessner, C. Stephen
Photographs: N. Miguletz
Lektorat: BerlinScienceWorks
All rights reserved. No part of this book may be reproduced in any form
by electronic or mechanical means (including photocopying, recording,
or information storage and retrieval) without permission in writing from
the publisher.
The book was set in TimesNewRoman and Arial.
Printed and bound in the United States of America.
Library of Congress Cataloging-in-Publication Data
Names: Benasich, April, editor. | Ribary, Urs, editor.
Title: Emergent brain dynamics : prebirth to adolescence / edited by April A.
Benasich and Urs Ribary.
Other titles: Strüngmann Forum reports.
Description: Cambridge, MA : The MIT Press, [2018] | Series: Strüngmann
Forum reports | Includes bibliographical references and index.
Identifi ers: LCCN 2018005125 | ISBN 9780262038638 (hardcover : alk.
paper)
Subjects: | MESH: Brain--growth & development | Nervous System
Physiological Phenomena | Neuronal Plasticity
Classifi cation: LCC QP376 | NLM WL 300 | DDC 612.8/2--dc23 LC record
available at https://lccn.loc.gov/2018005125
Ernst Strüngmann Forum (25th: 2017 : Frankfurt am Main, Germany)
10 9 8 7 6 5 4 3 2 1
Contents
The Ernst Strüngmann Forum vii
List of Contributors ix
1 Exploring Emergent Brain Dynamics 1
April A. Benasich and Urs Ribary
2 The Role of Oscillations and Synchrony in the 15
Development of the Nervous System
Wolf Singer
Fetal to Birth
3 Molecular Guidance and Cell-to-Cell Interactions 35
in Intrauterine Brain Construction during
Typical and Atypical Development
Alain Chédotal
4 Fetal to Birth 47
Nicholas C. Spitzer, Terrence J. Sejnowski, Yehezkel Ben-Ari,
Alain Chédotal, Gordon Fishell, Ileana L. Hanganu-Opatz,
Suzana Herculano-Houzel, Heiko J. Luhmann, Hannah Monyer,
and Michael P. Stryker
Early Childhood
5 Factors that Initiate and Terminate Critical Periods 69
Takao K. Hensch
6 Epigenetic Mechanisms and the Developing 81
Brain: Bridging the Nature–Nurture Divide
Sarah R. Moore and Michael S. Kobor
7 Early Childhood 101
Matthias Kaschube, Charles A. Nelson III, April A. Benasich,
Gyorgy Buzsáki, Pierre Gressens, Takao K. Hensch, Mark Hübener,
Michael S. Kobor, Wolf Singer, and Mriganka Sur
Early Adolescence
8 How Do Pubertal Hormones Impact Brain 127
Dynamics and Maturation?
Cheryl L. Sisk
9 Brain Plasticity in the Adolescent Brain 143
Bryan Kolb
10 Anesthesia-Induced Brain Oscillations: A Natural 161
Experiment in Human Neurodevelopment
Patrick L. Purdon
vi Contents
11 Understanding Effects of Experience on Neurocognitive 179
Development through the Lens of Early Adolescence
Marina Bedny, Tomáš Paus, Sam M. Doesburg, Jay Giedd,
Rowshanak Hashemiyoon, Bryan Kolb, Patrick L. Purdon,
Pasko Rakic, and Cheryl L. Sisk
Emerging Adulthood
12 Modifi cations in Brain Coordination and the Emergence 197
of Brain Disorders during Late Adolescence
Peter J. Uhlhaas
13 Plasticity beyond Early Development: 207
Hypotheses and Questions
Ulman Lindenberger
14 What Factors Determine Changes in the Adolescent Brain? 225
Adriana Galván
15 Late Adolescence: Critical Transitions into Adulthood 243
Jennifer N. Gelinas, Sylvain Baillet, Olivier Bertrand,
Adriana Galván, Thorsten Kolling, Jean-Philippe Lachaux,
Ulman Lindenberger, Urs Ribary, Akira Sawa,
and Peter J. Uhlhaas
Bibliography 265
Subject Index 319
The Ernst Strüngmann Forum
Science is a highly specialized enterprise—one that enables areas of enquiry to
be minutely pursued, establishes working paradigms and normative standards,
and supports rigor in experimental research. Some issues, however, do not
fall neatly into the purview of a single disciplinary fi eld and for these areas,
specialization can actually hinder conceptualization and limit the generation
of potential problem-solving approaches. The Ernst Strüngmann Forum was
created to address such topics.
Founded on the tenets of scientifi c independence and the inquisitive nature
of the human mind, the Ernst Strüngmann Forum is dedicated to the continual
expansion of knowledge. Its activities promote interdisciplinary communi-
cation on high-priority issues encountered in basic science. Through its in-
novative communication process, the Ernst Strüngmann Forum provides an
intellectual haven within which experts scrutinize high-priority issues from
multiple vantage points.
This process begins with the identifi cation of themes. By nature, a theme
constitutes a problem area that transcends classic disciplinary boundaries—
a topic of high-priority interest that requires concentrated, multidisciplinary
perusal. Proposals are received from leading scientists active in their fi eld
and reviewed by an independent Scientifi c Advisory Board. Once approved, a
steering committee is convened to refi ne the scientifi c parameters of the pro-
posal and select participants. Approximately one year later, a central gathering,
or Forum, is held to which circa forty experts are invited. Expansive discourse
is employed to address the problem. Often, this necessitates reexamining long-
established ideas and relinquishing previously held perspectives, yet when ac-
complished, novel insights begin to emerge. Resultant ideas and newly gained
perspectives from the entire process are disseminated to the scientifi c commu-
nity for further consideration and implementation.
Preliminary discussion on this theme began in 2015, when April Benasich
approached me with the wish to extend exploration into dynamic brain coor-
dination and synchrony by utilizing a developmental perspective. Urs Ribrary
joined us in preparing the proposal and from April 15–17, 2016, the Program
Advisory Committee (Yehezkel Ben-Ari, April Benasich, Julia Lupp, Charles
Nelson, Urs Ribary, Wolf Singer, and Terry Sejnowski) met to refi ne the sci-
entifi c framework for this Forum, which was held in Frankfurt am Main from
March 5–10, 2017.
This volume synthesizes the resulting discourse that took place between
a diverse group of experts and is comprised of two types of contributions.
Background information is provided on specifi c aspects of the overall theme.
These chapters, drafted before the Forum, initiated the discussion at the
Forum; they have been peer-reviewed and subsequently revised to provide an
viii The Ernst Strüngmann Forum
up-to-date assessment of these topics. In addition, Chapters 4, 7, 11, and 15
provide an overview of the working groups. These chapters are not consensus
documents: their intent was to summarize the discourse, to expose diverging
opinions, and to highlight areas where future enquiry is needed.
An endeavor of this kind creates its own unique group dynamics and puts
demands on everyone who participates. Each invitee played an active role and
for their efforts, I am grateful to all. A special word of thanks goes to the
Program Advisory Committee, to the authors and reviewers of the background
papers, as well as to the moderators of the individual working groups (Terry
Sejnowski, Charles Nelson, Tomáš Paus, and Sylvain Baillet). The rapporteurs
of the working groups (Nick Spitzer, Matthias Kaschube, Marina Bedny, and
Jennifer Gelinas) deserve special recognition, for to draft a report during the
Forum and fi nalize it in the months thereafter is no simple matter. Finally,
I extend my appreciation to April Benasich and Urs Ribary, whose commit-
ment and congenial personalities were essential to this 25th Ernst Strüngmann
Forum.
A communication process of this nature relies on institutional stability and
an environment that encourages free thought. The generous support of the
Ernst Strüngmann Foundation, established by Dr. Andreas and Dr. Thomas
Strüngmann in honor of their father, enables the Ernst Strüngmann Forum
to pursue its work in the service of science. In addition, valuable partner-
ships with the following groups are gratefully acknowledged: the Scientifi c
Advisory Board, which ensures the scientifi c independence of the Forum; the
German Science Foundation, for its supplemental fi nancial support; and the
Frankfurt Institute for Advanced Studies, which shares its intellectual setting
with the Forum. Long-held views are never easy to put aside. Yet, when this
is achieved, when the edges of the unknown begin to appear and the resulting
gaps in knowledge are able to be identifi ed, the act of formulating strategies
to fi ll such gaps becomes a most invigorating activity. On behalf of everyone
involved, I hope this volume will inspire future research focused on under-
standing the mechanisms by which the brain develops into a mature, fully
functioning organ.
Julia R. Lupp, Director
Ernst Strüngmann Forum
Frankfurt Institute for Advanced Studies (FIAS)
Ruth-Moufang-Str. 1, 60438 Frankfurt am Main, Germany
https://esforum.de/
List of Contributors
Baillet, Sylvain Neurology and Neurosurgery, Biomedical Engineering and
Computer Science, Montreal Neurological Institute, McGill University,
Montreal QC H2J 2Z3, Canada
Bedny, Marina Psychological and Brain Sciences, Johns Hopkins
University, Baltimore, MD 21218, U.S.A.
Ben-Ari, Yehezkel Neurochlore, Institut de Neurobiologie de la
Mediterranée (Inmed), 13273 Marseille Cedex 09, France
Benasich, April A. Center for Molecular and Behavioral Neuroscience
(CMBN), Rutgers University, Newark, NJ 07102, U.S.A.
Bertrand, Olivier Lyon Neuroscience Research Center, INSERM, CNRS,
Univ. Lyon 1, 69500 Bron, France
Buzsáki, Gyorgy NYU Neuroscience Institute, New York University,
Langone Medical Center, New York, NY 10016, U.S.A.
Chédotal, Alain Sorbonne Université, INSERM, CNRS, Institut de la
Vision, 75012 Paris, France
Doesburg, Sam M. Biomedical Physiology and Kinesiology, Simon Fraser
University, Burnaby BC V5A 1S6, Canada
Fishell, Gordon NYU Neuroscience Institute, New York University,
Langone Medical Center, New York, NY 10016, U.S.A.
Galván, Adriana Department of Psychology, Brain Research Institute,
University of California, Los Angeles, CA 90095-1563, U.S.A.
Gelinas, Jennifer N. Department of Neurology, Institute for Genomic
Medicine and the Gertrude H. Sergievsky Center, Columbia University
Medical Center, New York, NY, 10032, U.S.A.
Giedd, Jay Division of Child and Adolescent Psychiatry, University of
California, San Diego, La Jolla, CA 92093, U.S.A.
Gressens, Pierre Robert Debre Hospital, INSERM U1141, 75019 Paris,
France
Hanganu-Opatz, Ileana L. Developmental Neurophysiology, Institute of
Neuroanatomy, University Medical Center Hamburg-Eppendorf, 20251
Hamburg, Germany
Hashemiyoon, Rowshanak Stereotactic and Functional Neurosurgery,
University Hospital of Cologne, 50937 Köln, Germany
Hensch, Takao K. Molecular and Cellular Biology, Harvard University,
Cambridge, MA 02138, U.S.A.