Cognitive Neuroscience of Attention 2nd Edition
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Library of Congress Cataloging-in-Publication Data
Cogntive neuroscience of attention / edited by Michael I. Posner. — 2nd ed.
p. cm.
Includes bibliographical references and index.
ISBN 978-1-60918-985-3 (cloth: alk. paper)
1. Attention—Physiological aspects. 2. Cognitive neuroscience. I. Posner,
Michael I.
QP405.C7125 2012
612.8`233—dc23
2011035523
About the Editor
Michael I. Posner, PhD, is Professor Emeritus at the University of Oregon and Adjunct
Professor of Psychology in Psychiatry at the Weill Cornell Medical College in New York,
where he served as founding director of the Sackler Institute for Developmental Psycho-
biology. Dr. Posner is well known for his work with Marcus Raichle on imaging the human
brain during cognitive tasks; the book Images of Mind resulted from that collaboration.
He has worked on the anatomy, circuitry, development, and genetics of three attentional
networks underlying maintaining alertness, orienting to sensory events, and voluntary
control of thoughts and ideas. Dr. Posner’s methods for measuring these networks have
been applied to a wide range of neurological, psychiatric, and developmental disorders.
His research on the training of attention in young children and adults to understand the
interaction of specific experience and genes in shaping attention is described in Educating
the Human Brain, coauthored with Mary K. Rothbart. Dr. Posner has received numerous
awards, including seven honorary degrees, election to the National Academy of Sciences
of the USA, and the 2008 National Medal of Science.
v
Contributors
Søren K. Andersen, PhD, Department of Neurosciences, University of California, San Diego,
La Jolla, California; Institute for Psychology, University of Leipzig, Leipzig, Germany
Mauricio Arcos-Burgos, MD, PhD, Medical Genetics Branch, National Human Genome
Research Institute, National Institutes of Health, Bethesda, Maryland
Katherine M. Armstrong, PhD, Howard Hughes Medical Institute and Department of
Neurobiology, School of Medicine, Stanford University, Stanford, California
Edward Awh, PhD, Department of Psychology and Institute of Neuroscience, University of
Oregon, Eugene, Oregon
Arielle R. Baskin-Sommers, MS, Department of Psychology, University of Wisconsin–Madison,
Madison, Wisconsin
Martha Ann Bell, PhD, Department of Psychology, Virginia Polytechnic Institute and State
University, Blacksburg, Virginia
Andrea Berger, PhD, Department of Psychology, Zlotowski Center for Neuroscience,
Ben-Gurion University of the Negev, Beer-Sheva, Israel
Chananel Buchman, MA, Department of Psychology, Zlotowski Center for Neuroscience,
Ben-Gurion University of the Negev, Beer-Sheva, Israel
Brittany Burrows, PhD, Howard Hughes Medical Institute and Department of Neurobiology,
School of Medicine, Stanford University, Stanford, California
Timothy J. Buschman, PhD, Picower Institute for Learning and Memory, Department of Brain
and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts
George Bush, MD, MMSc, Department of Psychiatry, Harvard Medical School, Cambridge,
Massachusetts; Psychiatric Neuroscience Division, Department of Psychiatry, Benson-Henry
Institute for Mind-Body Medicine, Massachusetts General Hospital, Boston, Massachusetts;
MGH/MIT/HMS Athinoula A. Martinos Center for Biomedical Imaging, Charlestown,
Massachusetts
Susan D. Calkins, PhD, Department of Human Development and Human Studies,
and Department of Psychology, University of North Carolina at Greensboro,
Greensboro, North Carolina
vii
viii Contributors
Cameron S. Carter, MD, Center for Neuroscience, University of California at Davis,
Davis, California
B. J. Casey, PhD, Sackler Institute for Developmental Psychobiology, Weill Cornell Medical
College, New York, New York
Mindy H. Chang, PhD, Howard Hughes Medical Institute and Department of Neurobiology,
School of Medicine, Stanford University, Stanford, California
Qi Chen, PhD, Center for Studies of Psychological Application, South China Normal University,
Guangzhou, China
Maurizio Corbetta, MD, Departments of Radiology, Neurology, and Anatomy
and Neurobiology, Washington University in St. Louis School of Medicine,
St. Louis, Missouri
Kirby Deater-Deckard, PhD, Department of Psychology, Virginia Polytechnic Institute and State
University, Blacksburg, Virginia
Nico U. F. Dosenbach, MD, PhD, Department of Neurology, Washington University in St. Louis
School of Medicine, St. Louis, Missouri
John Duncan, PhD, MRC Cognition and Brain Sciences Unit, Cambridge University,
Cambridge, United Kingdom
Edward F. Ester, MS, Department of Psychology, University of Oregon, Eugene, Oregon
Damien A. Fair, PA-C, PhD, Departments of Behavioral Neuroscience and Psychiatry,
Oregon Health and Science University, Portland, Oregon
Jin Fan, PhD, Department of Psychology, Queens College, City University of New York, and
Mount Sinai School of Medicine, New York, New York
Luis J. Fuentes, PhD, Faculty of Psychology, University of Murcia, Murcia, Spain
Carmen González-Salinas, PhD, Faculty of Psychology, University of Murcia, Murcia, Spain
Tamar Green-Bleier, MA, Department of Psychology, Zlotowski Center for Neuroscience,
Ben-Gurion University of the Negev, Beer-Sheva, Israel
Steven A. Hillyard, PhD, Department of Neurosciences, University of California, San Diego,
La Jolla, California
Liqiang Huang, PhD, Department of Psychology, The Chinese University of Hong Kong,
Hong Kong, People’s Republic of China
Glyn W. Humphreys, PhD, School of Psychology, University of Birmingham,
Birmingham, United Kingdom
Nancy Kanwisher, PhD, McGovern Institute for Brain Research, Massachusetts Institute of
Technology, Cambridge, Massachusetts
Brandon Keehn, PhD, Department of Neurosciences, Joint Doctoral Program in Language
and Communicative Disorders, University of California, San Diego, La Jolla, California
Clifford George Kentros, PhD, Department of Psychology, Institute of Neuroscience,
University of Oregon, Eugene, Oregon
Raymond M. Klein, PhD, Department of Psychology, Dalhousie University, Halifax,
Nova Scotia, Canada
Torkel Klingberg, MD, PhD, Department of Neuroscience, Karolinska Institute,
Stockholm, Sweden
Marie K. Krug, PhD, Department of Psychology, Washington University in St. Louis,
St. Louis, Missouri
Contributors ix
Linda K. Langley, PhD, Department of Psychology, North Dakota State University,
Fargo, North Dakota
Michael A. Lawrence, MsC, Department of Psychology, Dalhousie University, Halifax,
Nova Scotia, Canada
Xun Liu, PhD, Institute of Psychology, Chinese Academy of Sciences, Beijing, People’s Republic
of China; Mount Sinai School of Medicine, New York, New York
Steven J. Luck, PhD, Center for Mind and Brain, Department of Psychology, University of
California, Davis, Davis, California
Tom Manly, PhD, MRC Cognition and Brain Sciences Unit, Cambridge University,
Cambridge, United Kingdom
Eirini Mavritsaki, PhD, School of Psychology, University of Birmingham,
Birmingham, United Kingdom
Bruce D. McCandliss, PhD, Department of Psychology and Human Development,
Vanderbilt University, Nashville, Tennessee
Earl K. Miller, PhD, Picower Institute for Learning and Memory, Department of Brain and
Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts
Tirin Moore, PhD, Howard Hughes Medical Institute and Department of Neurobiology, School
of Medicine, Stanford University, Stanford, California
Maximilian Muenke, MD, Medical Genetics Branch, National Human Genome Research
Institute, National Institutes of Health, Bethesda, Maryland
Matthias M. Müller, PhD, Institute for Psychology, University of Leipzig, Leipzig, Germany
Joseph P. Newman, PhD, Department of Psychology, University of Wisconsin–Madison,
Madison, Wisconsin
Anna C. Nobre, PhD, Brain and Cognition Laboratory, Department of Experimental Psychology,
and Oxford Centre for Human Brain Activity, University of Oxford, Oxford, United Kingdom
Redmond G. O’Connell, PhD, School of Psychology and Trinity College Institute of
Neuroscience, Dublin, Ireland
Harold Pashler, PhD, Department of Psychology, University of California, San Diego,
La Jolla, California
Steven E. Petersen, PhD, Departments of Radiology, Anatomy and Neurobiology, Pediatrics,
and Psychology, Washington University in St. Louis School of Medicine, St. Louis, Missouri
Michael I. Posner, PhD, Department of Psychology, University of Oregon, Eugene, Oregon;
Department of Psychology, Weill Cornell Medical College, New York, New York
Leila Reddy, PhD, University of Toulouse, UPS, Research Center on Brain and Cognition,
Toulouse, France
K. Richard Ridderinkhof, PhD, Amsterdam Center for the Study of Adaptive Control in
Brain and Behavior, Department of Psychology, and Cognitive Science Center, University of
Amsterdam, Amsterdam, The Netherlands
Megan Riddle, MD, Sackler Institute for Developmental Psychobiology, Weill Cornell Medical
College, New York, New York
Ian H. Robertson, PhD, School of Psychology and Trinity College Institute of Neuroscience,
Dublin, Ireland
Gustavo Rohenkohl, PhD, Brain and Cognition Laboratory, Department of Experimental
Psychology, and Oxford Centre for Human Brain Activity, University of Oxford,
Oxford, United Kingdom
x Contributors
David Clayton Rowland, MS, Department of Biology, Institute of Neuroscience, University of
Oregon, Eugene, Oregon
Robert J. Schafer, PhD, Department of Brain and Cognitive Sciences and McGovern Institute of
Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts
Jeffrey D. Schall, PhD, Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision
Research Center, and Department of Psychology, Vanderbilt University, Nashville, Tennessee
Bradley L. Schlaggar, MD, PhD, Departments of Radiology, Anatomy and Neurobiology,
Pediatrics, and Psychology, Washington University in St. Louis School of Medicine,
St. Louis, Missouri
Charles E. Schroeder, PhD, Nathan S. Kline Institute for Psychiatric Research,
Orangeburg, New York
Gordon L. Shulman, PhD, Department of Neurology, Washington University in St. Louis
School of Medicine, St. Louis, Missouri
Tony J. Simon, PhD, MIND Institute and Department of Psychiatry and Behavioral Sciences,
University of California, Davis, Davis, California
Mark G. Stokes, PhD, Brain and Cognition Laboratory, Department of Experimental
Psychology, and Oxford Centre for Human Brain Activity, University of Oxford,
Oxford, United Kingdom
Kirk G. Thompson, PhD, Laboratory of Sensorimotor Research, National Eye Institute,
National Institutes of Health, Bethesda, Maryland
Jeanne Townsend, PhD, Department of Neurosciences, University of California, San Diego,
La Jolla, California
Ana B. Vivas, PhD, City College, International Faculty of the University of Sheffield,
Thessaloniki, Greece
Edward K. Vogel, PhD, Department of Psychology and Institute of Neuroscience,
University of Oregon, Eugene, Oregon
Hongbin Wang, PhD, School of Biomedical Informatics, University of Texas Health Science
Center at Houston, Houston, Texas
Zhe Wang, MS, Department of Psychology, Virginia Polytechnic Institute and State University,
Blacksburg, Virginia
Marissa Westerfield, PhD, Department of Neurosciences, University of California, San Diego,
La Jolla, California
Wery P. M. van den Wildenberg, PhD, Amsterdam Center for the Study of Adaptive
Control in Brain and Behavior, Department of Psychology, University of Amsterdam,
Amsterdam, The Netherlands
Geoffrey F. Woodman, PhD, Vanderbilt Vision Research Center, Vanderbilt University,
Nashville, Tennessee
Scott A. Wylie, PhD, Department of Neurology, University of Virginia Health System,
Charlottesville, Virginia
Contents
1. Progress in Attention Research 2004–2011 1
Michael I. Posner
I. COGNITIVE SCIENCE
2. On the Modes and Domains of Attention 11
Raymond M. Klein and Michael A. Lawrence
3. Boolean Map Approach to Visual Attention 29
Liqiang Huang and Harold Pashler
4. Symbolic and Connectionist Models of Attention 47
Hongbin Wang, Xun Liu, and Jin Fan
5. Models of Visual Search: From Abstract Function 57
to Biological Constraint
Glyn W. Humphreys and Eirini Mavritsaki
6. Inhibitory Mechanisms in the Attentional Network: 76
A Multidisciplinary Approach
Luis J. Fuentes, Ana B. Vivas, Linda K. Langley, Qi Chen,
and Carmen González-Salinas
7. Dynamic Cognitive Control and Frontal–Cingulate Interactions 89
Cameron S. Carter and Marie K. Krug
xi
xii Contents
8. Discrete Resource Limits in Attention and Working Memory 99
Edward F. Ester, Edward K. Vogel, and Edward Awh
II. IMAGING
9. Two Attentional Networks: Identification and Function 113
within a Larger Cognitive Architecture
Gordon L. Shulman and Maurizio Corbetta
10. Clutter and Attention in Multivoxel Functional 129
Magnetic Resonance Imaging Representations
Leila Reddy and Nancy Kanwisher
11. A Frontoparietal Attention System in Human 143
and Monkey Brain: Constructing and Assembling
the Fragments of Thought and Behavior
John Duncan and Tom Manly
12. Nervous Anticipation: Top-Down Biasing across Space and Time 159
Anna C. Nobre, Gustavo Rohenkohl, and Mark G. Stokes
13. Microstructural Properties of White Matter Tracts Are Linked 187
to the Efficiency of Specific Attention Networks
Bruce D. McCandliss
14. Tracking the Allocation of Attention in Visual Scenes 197
with Steady-State Evoked Potentials
Søren K. Andersen, Matthias M. Müller, and Steven A. Hillyard
III. NEUROSCIENCE
15. Using Nonhuman Primates to Study the Micro- and 219
Macrodynamics of Neural Mechanisms of Attention
Geoffrey F. Woodman and Charles E. Schroeder
16. Top-Down Control of Attention by Rhythmic 229
Neural Computations
Earl K. Miller and Timothy J. Buschman
17. Neural Mechanisms of Saccade Target Selection: 242
Evidence for a Stage Theory of Attention and Action
Jeffrey D. Schall and Kirk G. Thompson
18. Neural Circuits Controlling Visual Attention 257
Tirin Moore, Brittany Burrows, Katherine M. Armstrong, Robert J. Schafer,
and Mindy H. Chang
Contents xiii
19. Attentional Modulation of the Firing Patterns 277
of Hippocampal Neurons
David Clayton Rowland and Clifford George Kentros
IV. DEVELOPMENT
20. Resting-State Studies on the Development of Control Systems 291
Damien A. Fair, Nico U. F. Dosenbach, Steven E. Petersen,
and Bradley L. Schlaggar
21. Development of Error Detection 312
Andrea Berger, Chananel Buchman, and Tamar Green-Bleier
22. Attentional Control and Emotion Regulation 322
in Early Development
Martha Ann Bell and Susan D. Calkins
23. Development of Temperament and Attention: 331
Behavioral Genetic Approaches
Kirby Deater-Deckard and Zhe Wang
V. DEFICITS AND INTERVENTIONS
24. Typical and Atypical Development of Attention 345
B. J. Casey and Megan Riddle
25. “Abstraction of Mind”: Attention in Autism 357
Jeanne Townsend, Brandon Keehn, and Marissa Westerfield
26. Cingulate–Frontal–Parietal Function in Health and Disease 374
George Bush
27. Understanding Attention through Evolutionary 388
and Epidemiological Genetics: Attention-Deficit/Hyperactivity
Disorder as an Extreme Phenotypic Variant
Mauricio Arcos-Burgos and Maximilian Muenke
28. Action Control in Times of Conflict: Analysis of Reaction Time 409
Distributions in Healthy and Clinical Populations
K. Richard Ridderinkhof, Wery P. M. van den Wildenberg,
and Scott A. Wylie
29. Early Selective Attention Abnormalities in Psychopathy: 421
Implications for Self-Regulation
Joseph P. Newman and Arielle R. Baskin-Sommers
xiv Contents
30. Attentional Impairments in Children with Chromosome 22q11.2 441
Deletion Syndrome
Tony J. Simon and Steven J. Luck
31. Training the Brain: Nonpharmacological Approaches 454
to Stimulating Cognitive Plasticity
Redmond G. O’Connell and Ian H. Robertson
32. Training of Working Memory and Attention 475
Torkel Klingberg
Author Index 487
Subject Index 505
CHAPTER 1
Progress in Attention Research
2004–2011
Michael I. Posner
T he pace of attention research has accelerated since the previous edition of this vol-
ume was published in 2004. Among the major trends are (1) further integration of
research in which behavioral, imaging, cellular, and genetic methods are combined; (2)
important breakthroughs in imaging the developing brain; (3) new applications of atten-
tional theory to illuminate psychopathology; (4) proposed interventions to improve poor
attention and normal aging.
I have continued to group the chapters under the general headings of Cognitive Sci-
ence, Imaging, Neuroscience, Development, and Deficits and Interventions, but it becomes
increasingly difficult to keep them in place as methods are combined and developmental
or evolutionary perspectives are applied to adult studies. For each of these topics I have
tried to indicate places where advances have occurred and the new research opportunities
they offer.
Cognitive Science
A major trend in cognitive studies is to develop explicit models that can be used to sum-
marize previous findings and to predict new ones. These models often focus on individual
tasks, but hopefully in the future they will be applied more generally to encompass the
whole of attention. Modeling usually begins by trying to define the domain to which the
model applies. Klein and Lawrence (Chapter 2) develop a taxonomy of attention tasks by
considering attention to space and time separately for exogenous and endogenous cues.
The type of endogenous cue is quite specific in this chapter, usually involving the use
of an arrow or a verbal instruction, but the problem of how an internal “goal tree” of
1
2 1. Progress in Attention Research
current concerns operates to bias attention toward relevant environmental events remains
for future studies.
Chapter 3, by Huang and Pashler, describes a Boolean model for a set of tasks that
involves both exogenous and endogenous attention to spatial locations or object features.
The Boolean map provides a method of access that is richer than a spatial location and
provides a theoretical framework for the idea of salience maps that have been developed
in primate studies (e.g., Bisley & Goldberg, 2010).
Frequently, models are designed to mirror performance in a single cognitive task.
One task that is used in several chapters is the Attention Network Test (ANT). This test
is designed to provide measures of different attention networks and is discussed further
in Chapters 6, 9, 13, 20, 21, 25, and 31. In Chapter 4, Wang, Lin, and Fan present both
symbolic and connectionist models of the task. The task purports to provide a somewhat
independent measure of the efficiency of three attentional networks, but how these net-
works function together in a coordinated fashion during the complex natural tasks of
daily life is still largely a mystery.
In Chapter 5, Humphreys and Mavritsaki expand the model-building effort by
explicit use of neuroimaging data in the study of visual search. They argue persuasively
that using a combination of behavioral and imaging input to build models is needed to
further develop a cognitive neuroscience of attention. Interestingly, their imaging data
point to the key role of the right temporal parietal junction, a brain area already identi-
fied as a unique contributor to the disengaging of attention (see also Chapter 9).
While the early chapters in Part I deal mainly with orienting to sensory events, where
the field has advanced the most, the last few chapters raise higher-level issues of executive
control. The areas of executive control and self-regulation (see the Development section)
are crucial ones for the future of the field. In Chapter 6, Fuentes and colleagues begin
this discussion by pointing out some of the similarities between orienting to sensory
events and to semantic memory. Both of these functions seem to involve similar compo-
nent operations, such as engaging and disengaging the focus of attention. As Carter and
Krug (Chapter 7) point out, conflict between responses is ubiquitous, because the brain
computes many simultaneous functions, the output of which could conflict with current
goals. When the brain is viewed in terms of its many simultaneously active networks,
the problem of regulating output with respect to current goals becomes a central issue.
Carter and Krug argue that a brain network involving the anterior cingulate is involved
in monitoring this conflict and in working with other brain areas to prevent conflicting
behaviors. It is this aspect of executive control that links this part with Parts II and IV on
Imaging and on Development and represents an important future for attention studies.
The link between attention and working memory for spatial locations is the topic
of Chapter 8 by Ester, Vogel, and Awh. Close links between attention and memory have
been proposed from some of the earliest papers on working memory (e.g., Baddeley &
Hitch, 1974). In the current chapter, a correlation is reported between the number of
items that can be tracked by attention and the number held in store during working
memory tasks. As stated by the authors of Chapter 8, “we propose that a common dis-
crete resource mediates both the selection and storage of visual information. This discrete
resource enables the simultaneous selection or storage of a limited number of individu-
ated object representations.” This chapter points the way to important research linking
attention to individual and group differences, and these differences are discussed further
in Part IV on Development and Part V on Deficits.
1. Progress in Attention Research 3
Imaging
Imaging has opened a distinct level of analysis in terms of brain networks, somewhere
between the behavioral models of cognitive science and the cellular and genetic orien-
tation of neuroscience. The idea of brain networks underlying cognition has probably
been most advanced in the study of attention. In most of the chapters in Part II the form
of attention studied involves orienting to sensory (usually visual) objects, often during
search for a target. However, Chapters 11 and 13 point toward imaging studies of other
forms of attention.
As Shulman and Corbetta say in Chapter 9, “Single-unit, event-related potential,
transcranial magnetic stimulation, and neuroimaging studies have investigated the
detailed characteristics of the frontal and parietal components of this system.” Shulman
and Corbetta highlight the dorsal and ventral attention networks that are active during
orienting to sensory events; however, these same regions remain connected during rest
(see Fair et al., Chapter 20). The right temporal–parietal junction (TPJ) appears to be a
very specialized region that plays a role in reorienting away from an attended location,
irrespective of the direction of new stimuli. The TPJ also appears to be the most fre-
quently damaged brain area in patients who exhibit neglect.
The visual system can extract objects from cluttered visual scenes. The orienting sys-
tem described by Shulman and Corbetta influences the visual system’s response to objects
within scenes but exactly how strong an influence is possible? Reddy and Kanwisher, in
Chaper 10, review studies of multivoxel pattern recognition routines to quantify this
influence. The method of combining voxels from different regions illustrates the use of
magnetic resonance imaging (MRI) to peer into the microcircuitry of visual recognition.
The influence of many visual areas on the recognition of an individual pattern in a
cluttered field suggests that even relatively localized processes such as visual recognition
may involve multiple areas working together. As we move forward in the brain to frontal
areas, this principle becomes even more important, as Duncan and Manly point out in
Chapter 11. The function of a frontal area depends on the task structure. As the person
attends to different aspects of the task, many frontal areas become activated in accord
with task demands. Duncan and Manly also propose to account for individual differ-
ences in the ability to solve problems by identifying a set of areas, including prefrontal
and cingulate areas, involved in many tasks that load upon the general (g) factor of intel-
ligence tests.
Attention allows the anticipation of where a target will occur and also when it will
occur, as discussed by Nobre and colleagues in Chapter 12. They report that temporal
anticipation does not amplify the early P1 wave of the event-related potential (ERP),
which is normally enhanced by attending to locations. This may be because a warning
signal does not change processing along the ventral (“what” pathway) but acts to enhance
the speed at which that information can be attended (Posner, 2008). This relatively late
influence could reflect the distribution of norepinepherine input, which is strong in the
parietal lobe but does not directly modulate the ventral pathway (Morrison & Foote,
1986). Nobre et al. argue that oscillatory activity may serve as one mechanism by which
temporal information influences processing in remote brain regions.
A major development of work with MRI is the measurement of white matter both
by functional connectivity (correlations in the blood-oxygenation-level-dependent
[BOLD] signal between brain areas) and diffusion tensor imaging (DTI). In Chapter 13,
