Cognitive Electrophysiology of Attention. Signals of the Mind

292 Pages·2014·30.442 MB·English

by  George R. Mangun (Eds.)

COGNITIVE
ELECTROPHYSIOLOGY
OF ATTENTION
Signals of the Mind
GEORGE R. MANGUN
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Dedication
This book is dedicated to Tamara, Alex, and Nick, as well as to all the loved ones of the authors. It is written in honor
of Steven A. Hillyard, scientist, scholar, teacher, and friend, as well as loving husband, father and grandfather.
Preface
The Cognitive Electrophysiology of Attention: Signals of Society annual meeting. There, many of the authors of
the Mind was a labor of love, for all of the contributors. this volume presented their latest work to honor the
First, all are passionate about their work and wanted to mentor, colleague, and friend who taught them how to
provide concise reviews and cutting edge data and mod- turn their curiosity into science. The conference gave life
els. Second, however, and more importantly, the book is to this volume, but the current authors include several
a tribute to the life, work and accomplishments of Pro- of Professor Hillyard’s students, trainees, and colleagues
fessor Steven A. Hillyard, one of the founding fathers of who were unable to attend the conference, providing a
cognitive neuroscience, who helped lead the charge to current view of the cognitive neuroscience of attention
study human higher mental function using physiological and related higher mental functions.
methods. In his case, this largely means the methods of The book includes much of the most current elec-
cognitive electrophysiology, which are recordings of the trophysiology, but also includes studies using fMRI
electroencephalogram (EEG) and event-related poten- and other modern methods. The quality of the papers
tials (ERPs), but has also included studies in patients presented not only attests to the scientific impact that
with focal brain damage and remarkable medical cases Professor Hillyard has had through his training and
such as split-brain patients, as well as the futuristic mentoring of generations of scholars, but also to the love
(to us from the last generation) neuroimaging methods they have for him personally, and the respect they have
like functional magnetic resonance imaging (fMRI). for his immense intellectual contributions to cognitive
The book follows, but is not wholly derivative of the neuroscience.
2011 conference in Professor Hillyard’s honor, which George R. Mangun
was held in San Francisco, California in April, 2011, as Davis, California, USA
a satellite symposium of the Cognitive Neuroscience 2013
ix
Foreword
The history of cognitive neuroscience is replete with relays while a cat was quietly resting or being attracted
examples of scientific insights that led to paradigm-shift- by mice in a jar. They reported that the auditory
ing new knowledge and the birth of new models and the- responses to clicks were larger in amplitude in the cat’s
ories. One such story is the struggle to understand how cochlear nucleus when the animal was passively listen-
attention influences our perceptions of the world, and ing than when distracted to pay attention to the mice.
hence, shapes our experience. It was indeed a struggle, Hernández-Peón and colleagues suggested that this was
because two strongly and dogmatically opposed theo- evidence that attention could affect early subcortical
retical positions were vigorously advocated by teams sensory processing via inhibition of unattended signals.
of scholars lining up to defend their faith, with data and At about the same time, Robert Galambos, David
experiment, of course. What was the nature of this battle Hubel, and their colleagues working at the Walter Reed
for understanding? In its simplest form it was the ques- Army Institute for Research in Washington D.C., were
tion of whether or not focused selective attention could also interested in the effects of attention, but this time on
alter early sensory processes. Although we all now cortical activity. They recorded from auditory cortex neu-
know the answer, for decades this question was hotly rons in a cat that was awake. They found that neurons
contested. Some argued that it was inopportune for the that could not be reliably driven to respond by clicks,
nervous system to alter sensory inputs until those inputs tones, or speaker noise would respond when the stimuli
were fully analyzed, whereupon attentional processes were more interesting, such as a human voice, a tap on the
could begin to filter the relevant from the irrelevant. Oth- table, and so on. They concluded that these neurons were
ers took the position that simple sensory cues could be putative ‘attention’ neurons, in that they only responded
used to bias the processing of incoming information in when the sounds were relevant to the animals. In sum-
favor of relevant information, thereby preventing infor- ming up, they also made the observation that: “Unfortu-
mation overload, and possibly analytic failures at higher nately, attention is an elusive variable that no one has yet been
decision stages. Straightforward question, complicated able to quantify” (Hubel et al., Science, 1959).
answer. This type of evidence seemed at the time to very clearly
This so-called “early versus late selection debate” was indicate that attention affected sensory processing.
foreshadowed in the thinking and writing of late 19th But a theoretical problem was soon recognized, which
century scholars. William James, the great American led to the appreciation of some important experimental
psychologist and philosopher, extensively wrote about con cerns with these early studies. It was understood that the
attention in his seminal Principles of Psychology (1890). study of attention was confounded with general behav-
James believed that attention was multifaceted, and ioral arousal. That is, a cat presented with mice is in a dif-
that top-down effects of attention could be directed to ferent aroused state than one resting quietly. Although
different types of information, including sensory infor- it is interesting to understand how arousal might affect
mation and information stored in memory. For James, neural processing, it is subtly but importantly different
attention was a high-level mental operation. His con- from understanding the nature of selective attention:
temporary, Hermann Von Helmholtz, the inspirational attending to one source of inputs while simultaneously
physicist and a forefather of psychophysics, speculated ignoring other distracting ones. This theoretical dis-
that attention might involve interactions with sensory tinction was made clear in influential writings by Risto
processes (Von Helmholtz, 1909–1911). Neither James Näätänen, the distinguished Finnish psychologist and
nor Von Helmholtz could really test different models of psychophysiologist (e.g., Näätänen, 1975). Näätänen
the attention mechanisms: that was to come later with clearly articulated the distinction between arousal and
refinements in psychophysics, experimental psychology, selective attention and argued for key experimental
and physiology. controls that would be necessary to demonstrate selec-
In the 1950s, physiologists like Raul Hernández-Peón, tive attention while controlling nonspecific behavioral
the Mexican physiologist, and his colleagues hypoth- arousal.
esized that attention might influence early sensory These arguments were not lost on his colleagues,
processing (Hernández-Peón et al., Science, 1956). Work- and in 1973, Steven A. Hillyard (a former student of
ing at UCLA, they recorded from subcortical auditory Robert Galambos) and his coworkers at UC San Diego
xi
xii FOREWORD
performed a seminal study that warmed the hearts of The authors draw on work from single neuron record-
not only Finns, but all researchers interested in atten- ing, ERPs, and functional imaging to tell the tale, review-
tion. Recording from electrodes on the scalp of healthy ing some of their own elegant work.
humans, they both controlled for nonspecific arousal Finally, in the third section, Robert Knight and his col-
and sensory signal intensity, in a study of auditory selec- leagues, Boaz Sadeh and Sara Szczepanski, take us on
tive attention (Hillyard et al., Science, 1973). The finding a tour of some new work in the basic neurophysiology
was that a cortical-evoked response, gleaned from the of cognition. Their chapter describes cross-frequency
ongoing EEG by signal averaging methods, was larger coupling of neuronal oscillations, an area of heightened
in amplitude for attended than ignored stimuli, convinc- interest in recent years. They recount the evidence from
ingly demonstrating for the first time that selective atten- multiple sources, including their fascinating work in
tion modulated sensory processing. This volume, edited human intracranial recordings, where Knight’s team
by George R. Mangun (one of Hillyard’s many students recently discovered high-frequency signals that provide
and colleagues), now carries us into the present with a a new view of neural function.
series of chapters presenting detailed information about The foregoing are merely a taste of some of the many
what has happened in studies of human attention in the interesting chapters in this book, including some by
ensuing 40 years. Hillyard and his colleagues, which I chose not to men-
The book is organized into three sections that cover tion in order to highlight the work of his former students
topics in spatial attention, feature and object attention, and colleagues, but are nonetheless impressive contribu-
and higher-order aspects of attention. The authors are tions and worth the read.
the students and colleagues of Hillyard, as well as their In closing, let me place this history and current book in
students and trainees. One of the first things to appreci- its place in the science of the mind. Over the past 50 years,
ate is the tremendous impact of Hillyard’s contributions we have seen the growth of a new field known as cogni-
as reflected in the who’s who of authors. From his lab, a tive neuroscience. The work of Steven A. H illyard and his
spectacular array of leading scholars has continuously many students and colleagues have played a major role
emerged, and they provide concise and cutting edge in the development of the field, and studies of attention
information about the state of studies of attention and are among the clearest examples of how neuroscience
cognition. It is beyond the scope of the foreword to give and psychology have come together to solve basic ques-
an exhaustive summary of the works contained herein, tions about how the brain gives rise to the mind.
but I would point to some highlights.
In the first section, the chapter by Risa Sawaki and Michael S. Gazzaniga
Steven J. Luck presents a model for how the brain pre- Santa Barbara
vents orienting to irrelevant events. They describe an 2013
event-related potential (ERP) that they have shown to
be part of an active suppression mechanism. The idea is
References
that preventing unwanted shifts of attention involves, in
part, inhibiting information from salient events at irrel-
Von Helmholtz, H. (1909–1911). Handbuch der Physiologischen Optik [Trea-
evant spatial locations. This is a critical elaboration on tise on Physiological Optics]. Leipzig, Germany: L. Vos. (Trans lated in
attention models because rather than focusing on the Warren R. M. & Warren R. P., Helmholtz on Perception: Its Physiol-
differential facilitation versus inhibition for relevant and ogy and Development. New York: Wiley, 1968.).
Hernández-Peón, R., Scherrer, H., & Jouvet, M. (1956). Modification of
irrelevant events, respectively, the model includes a sep-
electrical activity in cochlear nucleus during attention in unanes-
arate mechanism to avert unwanted shifts of attention.
thetized cats. Science, 123, 331–2.
In the second section on feature and object attention, Hillyard, S. A., Hink, R. F., Schwent, V. L., & Picton, T. W. (1973). Electrical
the chapter by Ariel Schoenfeld and Christian Stoppel signs of selective attention in the human brain. Science, 182,177–80.
is a scholarly and comprehensive review of the neural Hubel, D. H., Henson, C. O., Rupert, A., & Galambos, R. (1959). Atten-
tion units in the auditory cortex. Science, 129, 1279–80.
mechanisms of feature attention. They incorporate work
James, W. (1890). Principles of Psychology. New York: Holt.
in animals and humans to lay out a view of how atten-
Näätänen, R. (1975). Selective attention and evoked potentials in
tion to stimulus features is managed in the human brain. humans: a critical review. Biological Psychology, 2, 237–307.
Contributors
David E. Anderson Department of Psychology, University of Steven A. Hillyard Department of Neurosciences, University
Oregon, Eugene, OR, USA of California, San Diego, La Jolla, CA, USA
Antonio Arjona Human Psychobiology Lab, Experimental Jens-Max Hopf Leibniz Institute for Neurobiology, Magdeburg,
Psychology Department, University of Seville, Seville, Spain Germany; Department of Neurology, Otto-von-Guericke
Edward Awh Department of Psychology, University of University, Magdeburg, Germany
Oregon, Eugene, OR, USA Jorge Iglesias Cuban Center for Neuroscience, Havana, Cuba
David L. Barack Center for Cognitive Neuroscience, Duke Vicente J. Iragui Department of Neurosciences, University
University, Durham, NC, USA; Department of Psychology of California, San Diego, La Jolla, CA, USA
& Neuroscience, Duke University, Durham, NC, USA;
Robert T. Knight Helen Wills Neuroscience Institute,
Department of Philosophy, Duke University, Durham, NC,
University of California, Berkeley, Berkeley, CA, USA;
USA
Department of Psychology, University of California, Berkeley,
Carsten N. Boehler Department of Experimental Psychology, Berkeley, CA, USA
Ghent University, Ghent, Belgium
Marta Kutas Department of Neurosciences, University
Vincent P. Clark Department of Psychology, University of of California, San Diego, La Jolla, CA, USA; Department of
New Mexico, Albuquerque, NM, USA; Psychology Clinical Cognitive Science, University of California, San Diego, La Jolla,
Neuroscience Center, University of New Mexico, Albuquerque, CA, USA
NM, USA; Mind Research Network and LBERI, Albuquerque,
Steven J. Luck Department of Psychology and Center for
NM, USA
Mind and Brain, University of California, Davis, Davis, CA, USA
Brian A. Coffman Department of Psychology, University of
George R. Mangun Departments of Psychology and
New Mexico, Albuquerque, NM, USA; Psychology Clinical
Neurology and Center for Mind and Brain, University of
Neuroscience Center, University of New Mexico, Albuquerque,
California, Davis, Davis, CA, USA
NM, USA; Mind Research Network and LBERI, Albuquerque,
NM, USA Antígona Martínez Department of Neurosciences, School
of Medicine, University of California, San Diego, La Jolla,
Tanya J. D'Avanzo Department of Psychology, Rehabilitation
CA, USA; Nathan Kline Institute for Psychiatric Research,
Hospital of the Pacific, Honolulu, HI, USA
Orangeburg, NY, USA
Francesco Di Russo Department of Human Movement,
Hiroaki Masaki Waseda University, Tokyo, Japan
Social and Health Sciences, University of Rome “Foro Italico”,
Rome, Italy; Neuropsychological Unit, Santa Lucia Foundation John J. McDonald Department of Psychology, Simon Fraser
IRCCS, Rome, Italy University, Burnaby, BC, Canada
Sean P. Fannon Department of Psychology, Folsom Lake Alex R. McMahon Center for Cognitive Neuroscience, Duke
College, Folsom, CA, USA University, Durham, NC, USA
Adam Gazzaley Department of Neurology, Physiology Katsumi Minakata North Dakota State University, Fargo,
and Psychiatry, Sandler Neurosciences Center, University of ND, USA
California, San Francisco, San Francisco, CA, USA
Jyoti Mishra Department of Neurology, Physiology and
Carlos M. Gómez Human Psychobiology Lab, Experimental Psychiatry, Sandler Neurosciences Center, University of
Psychology Department, University of Seville, Seville, Spain California, San Francisco, San Francisco, CA, USA
Marcia Grabowecky Department of Psychology and Stephen R. Mitroff Center for Cognitive Neuroscience, Duke
Interdepartmental Neuroscience Program, Northwestern University, Durham, NC, USA; Department of Psychology &
University, Evanston, IL, USA Neuroscience, Duke University, Durham, NC, USA
Steven A. Hackley University of Missouri, Columbia, MO, USA Matthias M. Müller Department of Psychology, University
Joseph A. Harris Center for Cognitive Neuroscience, Duke of Leipzig, Germany
University, Durham, NC, USA; Department of Psychology & Yu-Qiong Niu Department of Neurology, University of
Neuroscience, Duke University, Durham, NC, USA California, Davis, Sacramento, CA, USA; Center for Mind and
Karen Hebert University of Missouri, Columbia, MO, USA Brain, University of California, Davis, Davis, CA, USA
Hans-Jochen Heinze Leibniz Institute for Neurobiology, John M. Olichney Department of Neurology, University of
Magdeburg, Germany; Department of Neurology, Otto- California, Davis, Sacramento, CA, USA; Center for Mind and
von-Guericke University, Magdeburg, Germany Brain, University of California, Davis, Davis, CA, USA
xiii
xiv CONTRIBUTORS
Ken A. Paller Department of Psychology and Interdepartmental Nelson Trujillo-Barreto Neuroinformatics Department,
Neuroscience Program, Northwestern University, Evanston, Cuban Center for Neuroscience, Havana, Cuba
IL, USA
Michael C.S. Trumbo Department of Psychology, University
Michael A. Pitts Department of Psychology, Reed College, of New Mexico, Albuquerque, NM, USA; Psychology Clinical
Portland, OR, USA Neuroscience Center, University of New Mexico, Albuquerque,
Sabrina Pitzalis Department of Human Movement, Social NM, USA
and Health Sciences, University of Rome “Foro Italico”, Rome, Mitchell Valdes-Sosa Cuban Center for Neuroscience,
Italy; Neuropsychological Unit, Santa Lucia Foundation Havana, Cuba
IRCCS, Rome, Italy
Fernando Valle-Inclán University of La Coruña, La Coruña,
Boaz Sadeh Helen Wills Neuroscience Institute, University Spain
of California, Berkeley, Berkeley, CA, USA; Department of
Cyma Van Petten Department of Psychology, Binghamton
Psychology, University of California, Berkeley, Berkeley, CA, USA
University, State University of New York, Binghamton, NY, USA
David P. Salmon Department of Neurosciences, University
Edward K. Vogel Department of Psychology, University of
of California, San Diego, La Jolla, CA, USA
Oregon, Eugene, OR, USA
Risa Sawaki Department of Psychology and Center for Mind
Ashley R. Wegele Department of Psychology, University of
and Brain, University of California, Davis, Davis, CA, USA
New Mexico, Albuquerque, NM, USA; Ronald E. McNair Post-
Mircea Ariel Schoenfeld Department of Neurology, Otto- Baccalaureate Achievement & Research Opportunity Program,
von-Guericke-University, Magdeburg, Germany; Leibniz- University of New Mexico, Albuquerque, NM, USA
Institute for Neurobiology, Magdeburg, Germany; Kliniken
Jennifer C. Whitman Department of Psychology, Simon
Schmieder, Allensbach, Germany
Fraser University, Burnaby, BC, Canada
Christian Michael Stoppel Department of Neurology, Otto-
Marty G. Woldorff Center for Cognitive Neuroscience, Duke
von-Guericke-University, Magdeburg, Germany
University, Durham, NC, USA; Department of Psychology &
Viola S. Störmer Harvard University, Vision Sciences Neuroscience, Duke University, Durham, NC, USA;
Laboratory, Cambridge, MA, USA Department of Psychiatry, Duke University, Durham, NC,
Satoru Suzuki Department of Psychology and USA; Department of Neurobiology, Duke University, Durham,
Interdepartmental Neuroscience Program, Northwestern NC, USA
University, Evanston, IL, USA Jin-Chen Yang Department of Neurology, University of
Sara M. Szczepanski Helen Wills Neuroscience Institute, California, Davis, Sacramento, CA, USA; Center for Mind and
University of California, Berkeley, Berkeley, CA, USA; Brain, University of California, Davis, Davis, CA, USA
Department of Psychology, University of California, Berkeley,
Lin Zhang Department of Neurology, University of California
Berkeley, CA, USA
Davis, Sacramento, CA, USA
Wolfgang A. Teder 41114th street south, Moorhead, MN, USA
Marla Zinni Department of Neurosciences, University of
Rosario Torres Neurodevelopment Department, Cuban California, San Diego, La Jolla, CA, USA
Center for Neuroscience, Havana, Cuba
Acknowledgments
My love and thanks to my wife Tamara Swaab and our boys Alexander and Nicholas for their support and encour-
agement of this volume. My editorial assistant, Molly Allison-Baker, was invaluable in completing this project in a
timely fashion. One could not ask for a better colleague. The contributors to this volume also deserve my thanks for
working on a tight timeline and meeting all the deadlines to produce such a lovely set of chapters to honor Steven
A. Hillyard. Deep gratitude also goes to my students and scientific colleagues who have contributed directly and
indirectly to the research presented in this book. I would like to acknowledge the National Institute of Mental Health,
National Science Foundation, and the University of California, Davis, for their support. Mica Haley, my publisher at
Elsevier, has been a great source of encouragement and advice, and I truly enjoyed working with her on this project.
I would also like to acknowledge her staff, especially April Graham. They were just fantastic, and I cannot thank
them enough. Lastly, I want to express my deep, sincere, and heartfelt thanks to Steven A. Hillyard, who has been
my teacher, mentor, and friend.
xv
S E C T I O N I
SPATIAL ATTENTION
Quick over here.
Don’t turn your head, don’t look.
Just look with your mind’s eye or ear
get ready to see or hear or feel, more -
sensitivity galore.
Just focus that attentional spotlight
brightly in your head and use it instead
of any observable movement of the behavioral kind.
Trust your mind – don’t peek.
Seek to fixate from behind that pate from within.
Use those various and sundry
distributed frontal and parietal nooks
and you’ll be able to know
everybody’s biz like they were open books
that you need not confess that you actually ever read.
By Marta Kutas