BRAIN DEVELOPMEN T This page intentionally left blank BRAIN DEVELOPMEN T NORMAL PROCESSES AND THE EFFECT S O F ALCOHOL AND NICOTIN E EDITED BY Michael W. Miller OXPORD UNIVERSITY PRES S 2006 OXPORD UNIVERSITY PRES S Oxford Universit y Press, Inc., publishes works that furthe r Oxford University' s objective of excellence in research, scholarship, and education . Oxford Ne w Yor k Auckland Cap e Town Da r es Salaam Hon g Kong Karach i Kuala Lumpur Madri d Melbourn e Mexic o Cit y Nairob i New Delhi Shangha i Taipe i Toront o With offices i n Argentina Austri a Brazi l Chil e Czec h Republi c Franc e Greec e Guatemala Hungar y Ital y Japa n Polan d Portuga l Singapor e South Kore a Switzerlan d Thailan d Turke y Ukrain e Vietna m Copyright © 2006 by Oxford Universit y Press, Inc . Published b y Oxford University Press, Inc. 198 Madison Avenue, New York, New York 1001 6 www.oup.com Oxford i s a registered trademark of Oxford University Press All rights reserved. No part of this publication may be reproduced , stored i n a retrieval system, or transmitted, i n any form or by any means , electronic, mechanical, photocopying, recording, or otherwise, without the prior permission of Oxford University Press. Library of Congress Cataloging-in-Publication Data Brain development : normal processes and the effect s o f alcohol an d nicotine / edited by Michael W. Miller. p. ; cm. Includes bibliographical references and index. ISBN-13 978-0-19-518313- 9 ISBN 0-19-518313-4 1. Developmenta l toxicology. 2 . Nenrotoxicology . 3 . Alcohol-Toxicology . 4 . Nicotin e —Toxicology. 5. Alcoholis m i n pregnancy—Pathophysiology. 6 . Pregnan t women—Tobacco use —Physiological effect . [DNLM: 1 . Brain—dru g effects. 2 . Brain—growt h & development. 3 . Ethanol—pharmacology . 4 . Fetus—dru g effects . 5. Neurons-dru g effects. 6 . Nicotin e - pharmacology. WL 300 B8125 2006] I . Miller , Michael W. RA1224.45.B73 2006 616.8'6471-dc22 200501285 4 1 3 5 7 9 8 6 4 2 Printed in the Unite d States of America on acid-free paper Acknowledgments As such, the present volume is the product of decades of work by teams of neuroscientists and developmen - tal biologists . I than k th e name d an d nameles s o f these dedicate d researcher s wh o hav e reache d m e through bot h ora l and/o r writte n communications . This volume builds on the foundation of research de- scribed i n a boo k publishe d 1 3 year s ago, Develop- ment of the Central Nervous System, Effects of Alcohol and Opiates (Miller , 1992). Since that book was pub- lished, our understanding of the mechanism s under - lying norma l brai n developmen t an d th e effect s o f ethanol neurotoxicit y on neura l ontogen y ha s grown exponentially. Interes t i n th e clinica l proble m o f nicotine exposure has also increased. Personally, m y researc h ha s bee n supporte d b y a host of postdoctoral trainees, graduate and undergrad- uate students, and technicians . I am greatl y indebted to them fo r working toward our commo n goa l of un- derstanding th e intricacie s o f brai n development . Some o f my current students (Maria Bruns and Juli e Siegenthaler) an d collaborator s (Sandr a Mooney ) contributed t o the writing of this book. My career has been consistently an d substantively supported b y the federal government , notably the Nationa l Institute of Alcohol Abus e an d Alcoholism an d th e Departmen t of Veterans Affairs. Without the support of these agen - cies I would not have been able to study normal an d abnormal brain development, no r would I have been able t o meet th e peopl e wh o wrot e chapter s fo r this volume. These people hav e brought considerabl e ex- pertise and keen insights to their contributions of out- standing chapters . The dua l sculptors, nature and nurture, have bee n essential factor s in my development as a scientist. M y fascination wit h science—ho w thing s wor k and ho w they fail—wa s fostere d b y m y parent s an d th e post - Sputnik America n culture . I t i s m y grea t hop e tha t children of all ages, boys and girls, retain their wonder as to why things are as they are. This sense of marvel should b e celebrate d an d hel d i n awe by society. My candle was stoked by high school and college teachers (including Willia m Harri s and Willia m Tully , an d vi ACKNOWLEDGMENT S Edward Hodgson an d Edwar d Maly, respectively), re- Finally , I would lik e to thank my family , m y wif e search mentor s (includin g Pedro Pasi k and Ala n Pe - an d thre e children , fo r their continue d suppor t an d ters), and collaborators (notably Richard Nowakowski goo d humor . The y ar e m y sustenance , grounding , and Rober t Rhoades). They encouraged m e t o think an d reason for being, broadly and not to be confined by dogma o r methods. Contents List of Abbreviations i x Contributors xii i 1. Model s o f Neurotoxicity Provide Unique Insight into Normal Development 3 Michael W. Miller Part I. Norma l Developmen t 2. Cel l Proliferatio n 9 Bernhard So ter Pradeep G . Bhide 3. Neurona l Migration 2 7 Huaiyu Hu 4. Neurona l Differentiation: From Axons to Synapses 4 5 C. David Mintz Iddii H. Bekirov Tonya R. Anderson Deanna L. Benson 5. Cel l Death 7 3 Stevens K Rehen Jerold J.M. Chun 6. Intracellula r Pathways of Neuronal Death 9 1 Sandra M. Mooney George I. Henderson 7. Developmenta l Disorder s and Evolutionary Expectations: Mechanism s of Resilience 10 4 Barbara L. Finlay Jeremy C. Yost Desmond T. Cheung vii viii CONTENT S Part IL Ethanol-Affecte d Developmen t 8. Prenata l Alcohol Exposure and Huma n Development 12 3 Claire D. Coles 9. Influenc e of Alcohol on the Structur e of the Developing Human Brain 14 3 Susanna L, Fryer Christie L. McGee Andrea D. Spadoni Edward P. Riley 10. Prenatal Ethanol Exposure and Feta l Programming: Implications for Endocrine and Immune Development an d Long-Term Healt h 15 3 Joanna H, Sliwowska Xingqi Zhang Joanne Weinberg 11. Earl y Exposure to Ethanol Affects th e Proliferation of Neuronal Precursor s 18 2 Michael W. Miller 12. Effect s o f Ethanol on the Regulatio n of Cell Cycle in Neural Stem Cells 19 9 W. Michael Zawada Mita Das 13. Mechanism s of Ethanol-Induced Alterations in Neuronal Migration 21 6 Julie A. Siegenthaler Michael W. Miller 14. Effect s o f Ethanol on Mechanism s Regulating Neuronal Process Outgrowth 23 0 Tara A. Lindsley 15. Neurona l Survival Is Compromised b y Ethanol: Extracellular Mediators 24 5 Michael W. Miller Maria B. Bruns Paula L. Hoffman 16. Intracellular Events in Ethanol-Induce d Neuronal Death 26 7 Sandra M. Mooney Michael W . Miller George I. Henderson 17. Neural Crest and Developmental Exposur e to Ethanol 27 9 Susan M. Smith Katherine A. Debelak-Kragtorp 18. Glial Targets of Developmental Exposur e to Ethanol 29 5 Consuelo Guerri Gemma Rubert Maria Pasqual Part III. Nicotine-Affecte d Developmen t 19. Tobacco use During Pregnancy : Epidemiology and Effects on Offspring 31 5 Jennifer A. Willford Nancy L . Day Marie D. Cornelius 20. Prenata l Nicotine Exposur e and Animal Behavior 32 9 Brenda M. Elliott Neil E. Grunberg 21. Neurona l Receptors for Nicotine: Functiona l Diversity and Developmental Change s 34 1 Huibert D. Mansvelder Loma W. Role 22. Neura l Precursors as Preferential Targets for Dru g Abuse: Long Term Consequence s and Latent Susceptibilit y to Central Nervous System Disorders 36 3 Kurt F. Hauser Nazira El-Hage Shreya Buch Gregory N. Barnes Henrietta S. Bada James R. Pauly 23. Nicotini c Receptor Regulatio n of Developing Catecholamine System s 38 1 Frances M. Leslie Layla Azam Kathy Goliardo Kathryn O'Leary Ryan Franke Shahrdad Lotfipour Index 39 9 List of Abbreviations 5-HT serotoni n 8-OH-DPAT 8-hydroxy-2-(di-n-propylamino)tetrali n ABCG2 ATP-bindin g cassette protein otBgTx a-bungarotoxi n ACh acetylcholin e AChE acetylcholinesteras e ACTH adrenocorticotropi c hormone ADH alcoho l dehydrogenase ADHD attentio n deficit hyperactivity disorder ADNF activity-dependen t neurotrophic factor ADNP activity-dependen t neuroprotective protein ADP adenosin e diphosphate ADX adrenalectom y AHP adul t hippocampal progenitor AIDS acquire d immunodeficiency syndrome AI F apoptosi s inducing factor ALC prenatall y exposed to alcohol, both with and without dysmorphic features AMPA a-amino-B-hydroxy-S-methyM-isoxazole - propionic acid AMPAR a-amino-3-hydroxy - 5-methyl-4-isoxazole propionic acid receptor AP-1 activatin g protein-1 APAF apoptoti c protease activating factor ARIA acetylcholin e receptor-inducin g protei n ARND alcohol-relate d neurodevelopmenta l disorder ASD atria l septic defect ASR acousti c startle reflex Astn astrotacti n ATP adenosin e triphosphate AVP arginin e vasopressin BDNF brain-derive d neurotrophic facto r BEG bloo d ethanol concentratio n ix