The Visual Brain in Action

320 Pages·2006·2.39 MB·English

by  A. David Milner, Melvyn A. Goodale

THE VISUAL BRAIN IN ACTION
Second edition
OXFORD PSYCHOLOGY SERIES
Editors
Mark D’Esposito Daniel Schacter
Jon Driver Anne Treisman
Trevor Robbins Lawrence Weiskrantz
1. The neuropsychology of anxiety: an enquiry 22. Classification and cognition
into the functions of the septohippocampal W. Estes
system 23. Vowel perception and production
J.A. Gray B. S. Rosner and J. B. Pickering
2. Elements of episodic memory 24. Visual stress
E. Tulving A. Wilkins
3. Conditioning and associative learning 25. Electrophysiology of mind
N. J. Mackintosh Edited by M. Rugg and M. Coles
4. Visual Masking: an integrative approach 26. Attention and memory: an integrated
B. G. Breitmeyer framework
5. The musical mind: the cognitive psychology N. Cowan
of music 27. The visual brain in action
J. Sloboda A. D. Milner and M. A. Goodale
6. Elements of psychophysical theory 28. Perceptual consequences of cochlear damage
J.C. Falmagne B. C. J. Moore
7. Animal intelligence 29. Binocular vision and stereopsis
Edited by L. Weiskrantz I. P. Howard
8. Response times: their role in inferring 30. The measurement of sensation
elementary mental organization D. Laming
R. D. Luce 31. Conditioned taste aversion
9. Mental representations: a dual coding J. Bures, F Bermúdez-Rattoni, and
approach T. Yamamoto
A. Paivio 32. The developing visual brain
10. Memory, imprinting, and the brain J. Atkinson
G. Horn 33. Neuropsychology of anxiety 2e
11. Working memory J. A. Gray and N. McNaughton
A. Baddeley 34. Looking down on human intelligence: from
12. Blindsight: a case study and psychometrics to the brain
implications I. J. Deary
L. Weiskrantz 35. From conditioning to conscious
13. Profile analysis ecollection: memory systems of the brain
D. M. Green H. Eichenbaum and N. J. Cohen
14. Spatial vision 36. Understanding figurative language: from
R. L. DeValois and K. K. DeValois metaphors to idioms
15. The neural and behavioural organization S. Glucksberg
of goal-directed movements 37. Active vision
M. Jeannerod J. M. Findlay and I. D. Gilchrist
16. Visual pattern analyzers 38. False memory
N. V. Graham C.J. Brainerd and V.F. Reyna
17. Cognitive foundations of musical pitch 39. Seeing black and white
C. L. Krumhansl A. Gilchrist
18. Perceptual and associative learning 40. The case for mental imagery
G. Hall S. Kosslyn
19. Implicit learning and tacit knowledge 41. Visual masking: time slices through
A. S. Reber conscious and unconscious vision
20. Neuromotor mechanisms in human B. G. Breitmeyer and H. Ögmen
communication 42. Motor cognition: what actions tell the self
D. Kimura M. Jeannerod
21. The frontal lobes and voluntary action 43. The visual brain in action 2e
R. E. Passingham A.D. Milner and M.A. Goodale
The Visual Brain
in Action
Second edition
A. David Milner
Professor of Cognitive Neuroscience,
University of Durham, UK
Melvyn A. Goodale
Canada Research Chair in Visual Neuroscience,
University of Western Ontario, Canada
1
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Data available
Library of Congress Cataloging in Publication Data
Milner, A. D. (A. David)
The Visual brain in action / A. David Milner, Melvyn A. Goodale.
2nd ed. p. ; cm. (Oxford psychology series; no 43)
Includes bibliographical references and index.
ISBN-13: 978–0–19–852472–4 (alk. paper)
ISBN-10: 0–19–852472–2 (alk. paper)
1. Visual cortex. 2. Visual pathways—Evolution. I. Goodale Melvyn A.
II. Title. III. Series.
[DNLM: 1. Visual Cortex. 2. Visual Pathways. 3. Visual Perception.
WL 307 M659v 2006]
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10 9 8 7 6 5 4 3 2 1
To Christine and Joan
The great end of life is not knowledge but action
T.H. Huxley, 1825–1895; from A Technical Education, 1877.
Preface to the Second Edition
Twelve years have passed since we wrote the first edition of The Visual Brain in
Action. In the book, we put forward a model for an understanding of visual
processing for perception and action that has provoked considerable interest
and debate. In this new edition, we have made a deliberate decision not to
change the body of the text, which we believe still stands as a coherent state-
ment of our position. Instead, we have added an Epilogue at the end of the
book, in which we review some of the key developments that support or chal-
lenge the views that we put forward in the first edition.
Research on the neural substrates of vision and visuomotor control contin-
ues to expand, although the methodologies have changed considerably. The
biggest single area of development has been that of functional neuroimaging,
allowing investigators for the first time to plot the patterns of activity within
the brains of behaving and thinking humans. When we were writing the first
edition of the book, in 1994, there were only a small number of relevant
neuroimaging studies. These studies, several of which we cited, made use of
positron emission tomography (PET) technology. Only a small number of
laboratories were able to exploit this kind of methodology, and its limitations,
including health risks and expense, have meant that it has never been very
widely used. Functional magnetic resonance imaging (fMRI) was virtually
unknown when we wrote the book, but has now left PET well behind in the
number of published studies. FMRI has the advantages of better spatial and
temporal resolution, as well as safety and relative cheapness. There are now
literally thousands of fMRI studies of visual processing in the human cerebral
cortex, and they are increasing rapidly all the time.
The development of fMRI, had it occurred 10 years earlier, would have dra-
matically affected the way we constructed our case in the book. In the absence
of such data, we relied to a great extent on nonhuman primate evidence and
therefore had to make a major (cross-species) theoretical leap. The demon-
stration that there were two cortical visual streams of processing was based
entirely on work with monkeys, as was the physiological and behavioural
evidence for how the two streams might operate. In contrast, virtually nothing
was known about the organization of visual pathways in the human brain
beyond primary visual cortex (V1). Although we were able to cite evidence
from neurological patients to support our interpretations, these were
viii PREFACE TO THE SECOND EDITION
necessarily highly conjectural in the absence of firm knowledge of the anatomy
and function of human visual areas beyond V1.
The pioneering work of Tootell and his group provided the first major
breakthrough. His use of fMRI showed for the first time that, in broad-brush
terms at least, the visual areas in the human cerebral cortex were laid out in a
remarkably similar fashion to those of the macaque monkey. As this work pro-
gressed it became clear that the notion of two visual streams of processing
applies not only to the monkey but to the human brain as well. In other words
fMRI has now confirmed the fundamental assumption in our book that the
organization of the monkey visual system provides a good model for under-
standing the neural substrates of vision in humans. But more importantly, the
advent of fMRI has allowed investigators to characterize differences in the pat-
terns of brain activation during the performance of different kinds of visual
tasks, including important differences in the processing of visual information
by the dorsal and ventral streams. We attempt to integrate some of these new
studies within the framework of our model in the Epilogue.
One particularly exciting new avenue of research is the use of fMRI in mon-
keys. This work allows investigators to go beyond the inferences that can be
made from single neuronal responses alone towards an understanding of the
whole pattern of brain activation involved in particular perceptual or behav-
ioural tasks. It also allows a closer comparison to be made between monkey
and human brain during similar perceptual processing tasks. We survey the
current state of both human and nonhuman fMRI research in the Epilogue.
We argue not only that they confirm the existence of human homologues of
the ventral and dorsal visual streams, but that they also shed new light on the
function of the various areas that comprise the two streams. Primate work has
become more sophisticated in other ways as well, notably in the behavioural
paradigms that have been developed to explore more fully the perceptual
experience of the monkey during particular experimental tasks. This increased
sophistication is well exemplified by the work of Cowey and colleagues in
exploring ‘blindsight’ in monkeys and that of Logothetis and colleagues in the
understanding of how neuronal activity in the ventral stream is correlated
with the animal’s awareness of the visual stimulus.
A major implication of our model is the counterintuitive idea that people’s
perception of the visual world does not always follow the same rules as their
behavioural interactions with that world. One example of this dissociation,
one which captured the attention of researchers in perception and psycho-
physics, was the surprising demonstration that a compelling illusion of visual
size did not influence the way in which people picked up the misperceived
stimulus. In other words, the grasping movements were calibrated to the real,
PREFACE TO THE SECOND EDITION ix
not the perceived, size of the target object. Since we described this result in the
first edition of the book, more than 100 studies, either supporting or challeng-
ing this finding, have appeared. Some investigators have concluded that our
model must be wrong since in some situations actions can be affected by per-
ceptual illusions. But, as we argue in the Epilogue, several factors have to be
taken into account in interpreting the results of these various studies—and
there are indeed some circumstances where our model would specifically
predict an effect of perceptual illusions on action.
One of the most important developments in our own research since we first
published The Visual Brain in Action has been a study in which we were able to
examine the patterns of fMRI activation to be seen in the brain of patient D.F.,
whose visual abilities and disabilities formed much of the stimulus for writing
the book in the first place. This study enabled us to make direct tests of our
previously indirect inferences concerning the cortical mechanisms underlying
her visual life. In the Epilogue, we review the main findings of the neuroimag-
ing work on D.F. and relate those findings to the new data that are emerging
about the functional organization of the dorsal and ventral streams in the nor-
mal brain. We use the Epilogue, however, not only to review the range of new
empirical findings, but also to clarify and refine our ideas as set out in the
unchanged main body of the book.
Our ideas have been sharpened over the intervening years thanks to the
practical collaboration and intellectual stimulation provided by many col-
leagues, past and present, including Salvatore Aglioti, Steve Arnott, Liana
Brown, Jonathan Cant, David Carey, Cristiana Cavina Pratesi, Erik Chang,
Jason Connolly, Jody Culham, James Danckert, Chris Dijkerman, Richard
Dyde, Susanne Ferber, Tzvi Ganel, Joe Gati, Herb Goltz, Claudia Gonzalez,
Angela Haffenden, Monika Harvey, Charles Heywood, Yaoping Hu, Keith
Humphrey, Lorna Jakobson, Karin Harman James, Tom James, Bob Kentridge,
Grzegorz Króliczak, Jonathan Marotta, Robert McIntosh, Ravi Menon, Mark
Mon-Williams, Kelly Murphy, Sukhvinder Obhi, Marie-Thérèse Perenin,
David Perrett, Nichola Rice, Yves Rossetti, Thomas Schenk, Igor Schindler,
Philip Servos, Jennifer Steeves, Chris Thomas, Kenneth Valyear, Lynne
Mitchell, Tutis Vilis, David Westwood, David Whitney, and Haitao Yang. We
would particularly like to thank Robert McIntosh, Kenneth Valyear, and David
Westwood, for their insightful comments on an earlier draft of the Epilogue,
and Kenneth Valyear and Grzegorz Króliczak for their assistance in preparing
the figures and illustrations.
University of Durham A.D.M.
University of Western Ontario M.A.G.