SPACE, TIME AND NUMBER IN THE BRAIN SEARCHING FOR THE FOUNDATIONS OF MATHEMATICAL THOUGHT SPACE, TIME AND NUMBER IN THE BRAIN SEARCHING FOR THE FOUNDATIONS OF MATHEMATICAL THOUGHT AN ATTENTION AND PERFORMANCE SERIES VOLUME Edited by Stanislas Dehaene and Elizabeth M. Brannon AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK• OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA Copyright © 2011 Elsevier Inc. 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Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN : 978-0-12-385948-8 For information on all Academic Press publications visit our website at elsevierdirect.com Typeset by MPS Limited, a Macmillan Company, Chennai, India www.macmillansolutions.com Printed and bound in Canada 10 11 12 13 14 15 10 9 8 7 6 5 4 3 2 1 Contents Contributors vii 11. Neglect "Around the Clock": Dissociating Foreword ix Number and Spatial Neglect in Right Brain Damage 149 12. Saccades Compress Space, Time, and I Number 175 MENTAL MAGNITUDES IV AND THEIR TRANSFORMATIONS ORIGINS OF PROTO- MATHEMATICAL 1. Mental Magnitudes 3 2. Objects, Sets, and Ensembles 13 INTUITIONS 3. Attention Mechanisms for Counting in Stabilized and in Dynamic Displays 23 13. Origins of Spatial, Temporal, and Numerical Cognition: Insights from Comparative Psychology 191 II 14. Evolutionary Foundations of the Approximate Number System 207 NEURAL CODES FOR SPACE, 15. Origins and Development of Generalized TIME AND NUMBER Magnitude Representation 225 4. A Manifold of Spatial Maps in the Brain 41 V 5. Temporal Neuronal Oscillations can Produce Spatial Phase Codes 59 REPRESENTATIONAL 6. Population Clocks: Motor Timing with Neural Dynamics 71 CHANGE AND 7. Discrete Neuroanatomical Substrates EDUCATION for Generating and Updating Temporal Expectations 87 16. Foundational Numerical Capacities and the 8. The Neural Code for Number 103 Origins of Dyscalculia 249 17. Neurocognitive Start-Up Tools for Symbolic III Number Representations 267 18. Natural Number and Natural Geometry 287 SHARED MECHANISMS FOR 19. Geometry as a Universal Mental Construction 319 SPACE, TIME AND NUMBER? 20. How Languages Construct Time 333 21. Improving Low-Income Children's Number 9. Synesthesia: Gluing Together Time, Number, Sense 343 and Space 123 10. How is Number Associated with Space? Index 355 The Role of Working Memory 133 v Contributors Marilena Aiello Dipartimento di Psicologia, Uni- Jennifer T. Coull Laboratoire de Neurobiologie versità degli Studi “La Sapienza”, Roma, Italy & de la Cognition, CNRS—Université de Provence, Fondazione Santa Lucia IRCCS, Roma, Italy Marseille, France Paola Binda Istituto di Neuroscienze del CNR, Stanislas Dehaene Collège de France, Paris, Pisa, Italy & Italian Institute of Technology, France & INSERM, Cognitive Neuro imaging Genova, Italy Unit, NeuroSpin center, Saclay, France Lera Boroditsky Psychology Department, Stan- Dori Derdikman Department of Physiology, ford University, Stanford, CA Faculty of Medicine, Technion, Haifa, Israel Elizabeth M. Brannon Center for Cognitive Neu- Jean-Philippe van Dijck Department of Experi- roscience, Duke University, Durham, NC mental Psychology, Ghent University, Belgium Claudio Brozzoli ImpAct, Centre des Neuro- Fabrizio Doricchi Dipartimento di Psicologia, sciences de Lyon, Institut National de la Santé Università degli Studi “La Sapienza”, Roma, Italy et de la Recherche Médicale, Université Claude & Fondazione Santa Lucia IRCCS, Roma, Italy Bernard Lyon, Bron, France Lisa Feigenson Department of Psychological Dean V. Buonomano Departments of Neuro - and Brain Sciences, Johns Hopkins University, biology and Psychology, UCLA, Los Angeles, CA Baltimore, MD Christopher Burgess UCL Institute of Cognitive Wim Fias Department of Experimental Psy- Neuroscience and UCL Institute of Neurology, chology, Ghent University, Belgium University College London, UK C. R. Gallistel Department of Psychology and Neil Burgess UCL Institute of Cognitive Neu- Rutgers Center for Cognitive Science, Rutgers roscience and UCL Institute of Neurology, University, New Brunswick, NJ University College London, UK Limor Gertner Department of Psychology, and David Burr Istituto di Neuroscienze del CNR, Zlotowski Center for Neuroscience, Ben-Gurion Pisa, Italy & Department of Psychology, Uni- University of the Negev, Beer-Sheva, Israel versitá Degli Studi di Firenze, Firenze, Italy Wim Gevers Unité de Recherches en Neuro- Brian Butterworth Institute of Cognitive Neuro- sciences Cognitives, Université Libre de science & Department of Psychology, University Bruxelles, Belgium College London, UK Daniel Haun Max Planck Institute for Evoluti- Patrick Cavanagh Laboratoire Psychologie de la onary Anthropology, Leipzig, Germany, & Perception, Université Paris Descartes, France Max Planck Institute for Psycholinguistics, Nijmegen, The Netherlands, & University of Nicky Clayton Department of Experimental Psy- Portsmouth, UK chology, University of Cambridge, UK Sheng He Department of Psychology, University Roi Cohen Kadosh Department of Experimental of Minnesota, Minneapolis, MN Psychology and Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Danielle Hinchey Department of Psychology, University of Oxford, UK Harvard University, Cambridge, MA vii viii Contributors Masami Ishihara Department of Health Pro- Andreas Nieder Animal Physiology Institute motion Sciences, Tokyo Metropolitan University, of Neurobiology, University of Tübingen, Japan Germany Véronique Izard Laboratoire Psychologie de la Manuela Piazza INSERM, U562, Cognitive Neu- Perception, Université Paris Descartes, Paris, roimaging Unit, CEA/SAC/DSV/DRM/Neu- France & CNRS UMR 8158, Paris France & rospin center, Gif-sur-Yvette, France, & Center for Department of Psychology, Harvard University, Mind/Brain Sciences and Dipar timento di Scienze Cambridge, MA della Cognizione e della Formazione University of Sophie Jacquin-Courtois ImpAct, Centre des Trento, Italy Neurosciences de Lyon, Institut National de la Pierre Pica “Formal Structure of Language”, Santé et de la Recherche Médicale, Université CNRS and Université Paris 8, Paris, France Claude Bernard Lyon, Bron, France, & Mouvement et Handicap, Hôpital Henry Gabrielle, Hospices Geetha B. Ramani Department of Human Devel- Civils de Lyon, St Genis Laval, France opment, University of Maryland, College Park, Fiona Jordan Max Planck Institute for MD Psycholinguistics, Nijmegen, The Netherlands John Ross Department of Psychology Uni- R. Laje Departments of Neurobiology and versity of Western Australia, Nedlands, Perth, Psychology, UCLA, Los Angeles, CA, & Depart- Western Australia ment of Science and Technology, University of Quilmes, Argentina Yves Rossetti ImpAct, Centre des Neurosciences de Lyon, Institut National de la Santé et de la Matthew R. Longo Department of Psychological Recherche Médicale, Université Claude Bernard Sciences, Birbeck, University of London, UK Lyon, Bron, France, & Mouvement et Handicap, Stella F. Lourenco Department of Psychology, Hôpital Henry Gabrielle, Hospices Civils de Emory University, Atlanta, GA Lyon, St Genis Laval, France Dustin J. Merritt Center for Cognitive Neuro- science, Duke University, Duke University, Nicolas W. Schuck Department of Psychology, Durham, NC Humboldt Universität zu Berlin, Germany Concetta Morrone Department of Physiological Robert S. Siegler Department of Psychology, Sciences, University of Pisa & Scientific Carnegie Mellon University, Pittsburgh, PA Institute Stella Maris, Pisa, Italy Elizabeth S. Spelke Department of Psychology, Edvard I. Moser Kavli Institute for Systems Harvard University, Cambridge, MA Neuroscience and the Centre for the Biology of Memory, Norwegian University of Science and Giorgio Vallortigara Centre for Mind/Brain Technology, Trondheim, Norway Sciences, University of Trento, Rovereto, Italy Foreword by Stanislas Dehaene and Elizabeth M. Brannon The knowledge of first principles, as space, evolutionary processes and neural mecha- time, motion, number, is as sure as any of those nisms which may universally give rise to which we get from reasoning. And reason must Kantian intuitions. trust these intuitions of the heart, and must base But a second issue motivates our present on them every argument. Blaise Pascal, Pensées focus on the representations of space, time (translated by W. F. Trotter) and number: they all raise deep computational issues for cognitive neuroscience. In all three What do the representations of space, domains, the nervous system must encode time and number have in common that jus- and compute with quantities. Behavioral evi- tifies our dedicating an entire book to them? dence suggests that these computations can In his Critique of Pure Reason, Immanuel Kant be remarkably accurate, even in miniature famously argued that they provide “a priori organisms such as desert ants or in imma- intuitions” that precede and structure how ture systems such as the infant brain. Animal we experience our environment. Indeed, spatial navigation implies the mental stor- these concepts are so basic to our understand- age of spatial coordinates and their updating ing of the external world that we find it hard through path integration [1]. Temporal deci- to imagine how any animal species could sions imply that memorized representations survive without possessing mechanisms for of time are subjected to operations analogous spatial navigation, temporal orienting (e.g., to addition, subtraction and comparison [3]. time-stamped memories), and elementary In the number domain, human infants as well numerical computations (e.g., choosing the as other animal species readily anticipate the food patch with the largest expected return) outcome of analogs of arithmetic operations [1]. In the course of their evolution, humans performed with concrete sets of objects [4]. and many other animal species have internal- Does this mean that a common set of coding ized basic codes and operations isomorphic to and computation mechanisms underlies quan- the physical and arithmetic laws that govern tity manipulations in all three domains? Do the interaction of objects in the external world these systems share similar brain circuitry? An [2]. Indeed, there is now considerable evi- exciting research program consists of mapping dence that space, time and number are part of the range of the possible implementations of the essential toolkit that adult humans share quantitative operations in the nervous system, with infants and with many other nonhu- and testing whether evolution has arrived at man animals. One of the main purposes of the the same computational solutions in distinct present book is therefore to review this work organisms or for distinct domains. in detail. From grid cells to number neurons, The 24th Attention & Performance meet- the richness and variety of the mechanisms ing on “Space, Time, and Number: Cerebral used by animals and humans, including Foundations of Mathematical Intuitions”, held infants, to represent the dimensions of space, from July 6 to 10, 2010, in Vaux de Cernay near time and number is bewildering and suggests Paris, was organized with this goal in mind: to ix