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Attention in Action
Advances from Cognitive Neuroscience

Edited by
Glyn W. Humphreys and
M. Jane Riddoch
First published 2005
by Psychology Press
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Simultaneously published in the USA and Canada
by Psychology Press
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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
Attention in action : advances from cognitive neuroscience / edited by
Glyn Humphreys and Jane Riddoch.
p. cm. – (Advances in behavioural brain science)
Includes bibliographical references and index.
ISBN 1-84169-354-5 (hardcover)
1. Attention. 2. Clinical neuropsychology. 3. Cognitive
therapy. 4. Psychology, Pathological. I. Humphreys, Glyn W.
II. Riddoch, M. Jane. III. Series.
RC455 4.A85A885 2004
616.8–dc22
2003021537
ISBN 0-203-44922-3 Master e-book ISBN

ISBN 0-203-67704-8 (Adobe eReader Format)

ISBN 1-84169-354-5 (Print edition)
Contents

List of contributors vii

Preface xi

PART I
Functional processes 1

1 Attending to what you are doing: Neuropsychological and

experimental evidence for interactions between
perception and action 3
G. W. HUMPHREYS, M. J. RIDDOCH, K. L. LINNELL, D. J. PUNT,
M. G. EDWARDS AND A. M. WING

2 Hierarchical systems of attention and action 27

A. COHEN AND H. MAGEN

3 Attentional selection in sequential manual movements,

movements around an obstacle and in grasping 69
H. DEUBEL AND W. X. SCHNEIDER

4 Intention in action 93
W. PRINZ, S. DE MAEGHT AND L. KNUF

5 Intention and reactivity 109

T. ASTOR-JACK AND P. HAGGARD

6 Selective attention for action: New evidence from visual

search studies 131
A. HANNUS, S. F. W. NEGGERS, F. W. CORNELISSEN AND
H. BEKKERING
vi Contents
7 Attention and inaction: Mechanisms for preventing
distractor responses 151
N. LAVIE

8 Object- and location-based inhibition in goal-directed

action: inhibition of return reveals behavioural and
anatomical associations and interactions with memory
processes 171
S. GRISON, K. KESSLER, M. A. PAUL, H. JORDAN AND S. P. TIPPER

PART II
Neural processes 209

9 A map of complex movements in motor cortex of primates 211

M. S. A. GRAZIANO, C. S. R. TAYLOR, D. F. COOKE AND T. MOORE

10 Spatial representations and attentional systems for action

in the parietal cortex 233
M. F. S. RUSHWORTH AND A. ELLISON

11 Prefrontal cortex and attention to action 263

R. E. PASSINGHAM, J. B. ROWE AND K. SAKAI

12 A neuroimaging study of selection-for-action: a reach-to-

grasp study 287
H. CHAPMAN, M. GAVRILESCU, M. KEAN, G. EGAN AND
U. CASTIELLO

13 Action binding and the parietal lobes: some new

perspectives on optic ataxia 303
S. R. JACKSON, R. NEWPORT, D. MORT, M. HUSAIN, G. M. JACKSON,
R. SWAINSON, S. PEARS AND B. WILSON

14 Selective attention and response control following damage

to the human pulvinar 325
R. WARD AND S. DANZIGER

Index 351
Contributors

Tamsin Astor-Jack, Institute of Cognitive Neurosciences, University

College London, Alexandra House, 17 Queen Square, London WC1N
3AR, UK
Harold Bekkering, Department of Experimental Psychology, Nijmegen
Institute for Cognition and Information (NICI), University of Nijmegen,
PO Box 9104, 6500 HE Nijmegen, The Netherlands
Umberto Castiello, Department of Psychology, Royal Holloway and Bedford
New College, University of London, Egham Hill, Egham, Surrey, UK
Heidi Chapman, Howard Florey Institute, Centre for Neuroscience,
University of Melbourne, Melbourne 3010, Australia
Asher Cohen, Department of Psychology, The Hebrew University, Jerusa-
lem 91905, Israel
Dylan F. Cooke, Department of Psychology, Princeton University,
Princeton, NJ 08544, USA
Frans W. Cornelissen, Laboratory of Experimental Ophthalmology, School
for Behavioral and Cognitive Neurosciences (BCN), University of
Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands
Shai Danziger, Department of Psychology, Ben Gurion University of the
Negev, 84105 Beer Sheva, Israel
Sarah de Maeght, Department of Cognition and Action, Max Planck Insti-
tute for Psychological Research, Amalienstrasse 33, 80799 Munich,
Germany
Heiner Deubel, Department of Psychology, Ludwig-Maximilians-
Universität, Leopoldstrasse 13, 80802 München, Germany
Martin G. Edwards, Behavioural Brain Sciences, School of Psychology,
University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
Gary Egan, Howard Florey Institute, Centre for Neuroscience, University of
Melbourne, Melbourne 3010, Australia
viii Contributors
Amanda Ellison, Department of Psychology, University of Durham,
Stockton Campus, Stockton-on-Tees TS17 6BH, UK
Maria Gavrilescu, Howard Florey Institute, Centre for Neuroscience, Uni-
versity of Melbourne, Melbourne 3010, Australia
Michael S.A. Graziano, Department of Psychology, Princeton University,
Princeton, NJ 08544, USA
Sarah Grison, Beckman Institute, University of Illinois at Urbana-
Champaign, 405 North Mathews Avenue, Urbana, IL 61801, USA
Patrick Haggard, Institute of Cognitive Neurosciences, University College
London, Alexandra House, 17 Queen Square, London WC1N 3AR, UK
Aave Hannus, Department of Experimental Psychology, Nijmegen Institute
for Cognition and Information (NICI), University of Nijmegen, PO Box
9104, 6500 HE Nijmegen, The Netherlands
Glyn W. Humphreys, Behavioural Brain Sciences, School of Psychology,
University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
Masud Husain, Division of Neuroscience and Psychological Medicine,
Imperial College, University of London, London W6 8RF, UK
Georgina M. Jackson, Institute of Neuroscience, School of Psychology, The
University of Nottingham, University Park, Nottingham NG7 2RD, UK
Stephen R. Jackson, Institute of Neuroscience, School of Psychology, The
University of Nottingham, University Park, Nottingham NG7 2RD, UK
Heather Jordan, Department of Experimental Psychology, Oxford
University, South Parks Road, Oxford OX1 3UD, UK
Michael Kean, Howard Florey Institute, Centre for Neuroscience,
University of Melbourne, Melbourne 3010, Australia
Klaus Kessler, Department of Neurology, University of Düsseldorf,
D-40225 Düsseldorf, Germany
Lothar Knuf, Department of Cognition and Action, Max Planck Institute
for Psychological Research, Amalienstrasse 33, 80799 Munich, Germany
Nilli Lavie, Department of Psychology, University College London, Gower
Street, London WC1E 6BT, UK
Karina J. Linnell, Department of Psychology, Goldsmiths College,
University of London, New Cross, London SE14 6NW, UK
Hagit Magen, Department of Psychology, The Hebrew University, Jerusalem
91905, Israel
Tirin Moore, Department of Psychology, Princeton University, Princeton,
NJ 08544, USA
 Contributors ix
Dominic Mort, Division of Neuroscience and Psychological Medicine,
Imperial College, University of London, London W6 8RF, UK
Sebastian F.W. Neggers, Helmholtz Research Institute, Utrecht University,
Psychonomics Division, Heidelberglaan 2, 3584 CS Utrecht, The
Netherlands
Roger Newport, Institute of Neuroscience, School of Psychology, The
University of Nottingham, University Park, Nottingham NG7 2RD, UK
Richard E. Passingham, Department of Experimental Psychology,
University of Oxford, South Parks Road, Oxford OX1 3UD, UK
Matthew A. Paul, Department of Psychology, University of Wales Bangor,
Bangor, Gwynedd LL57 2PX, UK
Sally Pears, Institute of Neuroscience, School of Psychology, The
University of Nottingham, University Park, Nottingham NG7 2RD, UK
Wolfgang Prinz, Department of Cognition and Action, Max Planck Insti-
tute for Psychological Research, Amalienstrasse 33, 80799 Munich,
Germany
David J. Punt, Behavioural Brain Sciences, School of Psychology,
University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
M. Jane Riddoch, Behavioural Brain Sciences, School of Psychology, Uni-
versity of Birmingham, Edgbaston, Birmingham B15 2TT, UK
James B. Rowe, Wellcome Department of Imaging Neuroscience, Institute
of Neurology, University College London, London WC1E 6BT, UK
Matthew F.S. Rushworth, Department of Experimental Psychology and
Centre for Functional Magnetic Resonance Imaging of the Brain
(FMRIB), University of Oxford, Oxford OX3 1UD, UK
Katz Sakai, Wellcome Department of Imaging Neuroscience, Institute of
Neurology, University College London, London WC1E 6BT, UK
Werner X. Schneider, Department of Psychology, Ludwig-Maximilians-
Universität, Leopoldstrasse 13, 80802 München, Germany
Rachel Swainson, Institute of Neuroscience, School of Psychology, The
University of Nottingham, University Park, Nottingham NG7 2RD, UK
Charlotte S.R. Taylor, Department of Psychology, Princeton University,
Princeton, NJ 08544, USA
Steven P. Tipper, Department of Psychology, University of Wales Bangor,
Bangor, Gwynedd LL57 2PX, UK
Robert Ward, Centre for Cognitive Neuroscience, School of Psychology,
University of Wales Bangor, Bangor, Gwynedd LL57 2PX, UK
x Contributors
Barbara Wilson, MRC Cognition and Brain Sciences Unit, Cambridge CB2
2QQ, UK
Alan M. Wing, Behavioural Brain Sciences, School of Psychology,
University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
Preface

The external world is a complex place, full of many objects, and we have
only a limited number of effectors with which we can make actions. Because
of these constraints, we must limit our processing of stimuli and our plan-
ning of actions, so that we behave efficiently to meet our behavioural goals.
Some of the constraints on stimulus processing may be influenced directly
by our actions, so that, for example, processing is enhanced at locations and
for stimulus dimensions that are relevant to a given movement (see Chapters 1,
3 and 6). Similarly, some of the ways that perception is organized can influ-
ence the programming and selection of actions to objects (see Chapters 1 and
13). There may be independent processes concerned with selecting stimuli
for action and selecting the appropriate actions to make to stimuli (see
Chapters 2, 7 and 10), and between the processes leading to internally and
externally driven actions (see Chapters 4 and 5). Furthermore, there may be
interactions between different action systems, and direct coding of complex
actions based on the goal of the action (see Chapter 9), which, in turn, can
influence how we attend to stimuli (see Chapter 13). The processes involved
in the selection of action to objects not only operate over the short term,
determining momentary priorities of stimuli and actions, but also over the
longer term, modulated by (among other things) long-term inhibition of
episodic memories (see Chapter 8).
Traditionally, the study of attention has tended to emphasize the processes
involved in selecting stimuli for action. In contrast, the processes and brain
mechanisms involved in selecting the appropriate action to objects, and the
interactions between selective perception and action, have been somewhat
neglected. Recently, however, this has changed. This change comes partially
through the development of new procedures for measuring actions accur-
ately, and for measuring the relations between attention and action (three-
dimensional kinematic analysis, saccadic contingent display changes). The
change has also been facilitated by the use of new brain imaging procedures
that enable us to assess the relations between activation in neural areas con-
cerned with perception and action (see Chapters 11 and 12), and by interven-
tion techniques that allow us to assess the consequences of directly altering
neuronal activation (see Chapters 9 and 10). These new procedures both
xii Preface
support and extend more traditional approaches to analysing the relations
between brain function and behaviour, through neuropsychological analyses
of patients. Nevertheless, such neuropsychological studies can often provide
the starting place for convergent work, since they can indicate counterintui-
tive ways in which performance fractionates when attentional coupling
between perception and action is disrupted (or, indeed, left intact, when
other attentional functions are disturbed; see Chapters 1 and 14).
In this book, we have brought together contributions from leading
researchers in the field that highlight the relations between attention and
action (in both perceptual selection and action selection). The chapters are
built around the first Behavioural Brain Sciences Symposium, held at
the Behavioural Brain Sciences Centre, University of Birmingham, UK, in
September 2002. We were delighted to host such a distinguished set of con-
tributors and we hope both the meeting and the chapters that have emerged
will help advance our understanding of the interactions between attention
and action—a topic central to the psychology of both perception and action.
We have divided the 14 chapters according to whether they deal with the
functional relations between attention and action or whether they deal with
the underlying brain mechanisms. In the first chapter in Part I, Humphreys
et al. use experimental studies with both normal and neuropsychological
individuals to evaluate how action and attention interact. We summarize
recent neuropsychological and experimental evidence indicating that there is
a close coupling between action and attention. This coupling can be affected
by the placement of objects in potent positions for action, with the pos-
itional relations between objects affecting both visual selection and action
selection. In addition, new evidence is presented demonstrating that the
effects of object-relations interact with the effects of action towards an
object, and that action towards an object can modulate “object-based” selec-
tion—making a part represented as the target object for selection or
emphasizing spatial selection at the expense of the selection of whole
objects.
In Chapter 2, Cohen and Magen examine the proposal that there are two
distinct attentional networks, one “executive” network dealing with action-
related selection and another specialized for visual attention (dedicated to
selection among input stimuli). They further propose that the systems are
hierarchically related. The lower-level network (e.g. visual attention) operates
to resolve online conflicts, at both the input and output ends of processing,
with a limited set of selection cues (e.g. location or feature-enhancement).
The higher-level network is recruited for selection primarily when these
lower-level cues are not available.
Some of the experiments reported in the chapter by Humphreys et al.
examine the effects of movement on the deployment of visual attention,
showing a strong coupling between movement and attention. The paradigm
used in these studies was invented by Deubel and Schneider and, in Chapter 3,
they investigate covert selective attention in more complex movement
 Preface xiii
situations, as when sequential eye and hand movements are directed to two
targets, when we make reaching movements around an obstacle, when
movements are delayed and when we grasp an object. Similar to the results
reported in Humphreys et al., Deubel and Schneider find that visual atten-
tion is largely confined to the action-relevant parts of the object—that is,
those parts that will be grasped. They argue for the existence of covert senso-
rimotor selection processes (influenced by both visual and motor stimuli),
which occur before complex open movements are initiated.
In Chapter 4, Prinz et al. examine the relations between the effects of
intending to make an action and the effects of perceptually cueing a so-called
“ideomotor action”, made in response to another action (e.g. yawning in
response to someone else yawning). They develop a new paradigm in which
participants see a ball going towards or away from a target. Participants can
alter the trajectory of the ball’s movement through a mouse, but only for a
certain period of time (the instrumental period), after which their move-
ments are not effective (the induction period). Movements made during the
induction period can then be assessed to determine whether they are driven
by the ball (“perceptual induction”) or by the intended action (“intentional
induction”). Prinz et al. report that intentional induction is weaker, and per-
ceptual induction stronger, with other-generated than with self-generated
actions. This work, then, begins to unpick the nature of ideomotor actions,
to understand the extent to which they are induced by intention or simply by
observing an event.
Astor-Jack and Haggard also focus on the interactions between internally
generated actions and externally triggered actions in Chapter 5. They, too,
use a novel experimental procedure (the “truncation procedure”) in which
participants have to prepare an intentional action but which can be truncated
so that they make the same action but to a perceptual event. They find a
substantial cost of truncation relative to when participants make the same
response just to the perceptual event, and this is attributed to the need to
switch from the control of action by an intentional system to control by a
reactive response system. In this case, there are attentional constraints on
selecting the same response through different “action control” systems.
In Chapter 6, Hannus and colleagues examine the effects of the intended
response on the selection of perceptual events. They discuss evidence sug-
gesting that the constraints of a task can sensitize visual selection to proper-
ties of the world relevant to the particular action (e.g. making a grasp
response heightens our sensitivity to orientation information). They argue
that the perception of specific object features and the planning of an action
to interact with an object are to some extent tapping into the same mechanism.
Again, action affects perceptual selection.
In Chapter 7, Lavie deals not just with how we select a particular target
(and an action to that target), but also how we prevent responses to dis-
tractors. She argues that responses to distractors are prevented either
through reduced distractor perception or through active inhibition of
xiv Preface
responses to irrelevant distractors, depending on factors such as the
perceptual load of a task. The results from several new experiments are
reported, which show reduced distractor perception under conditions of
high perceptual load and also the involvement of active response inhibition
when distractors are rejected under low load conditions. Here specific
attentional processes may be recruited for the control of action.
In the last chapter in Part 1, Grison et al. discuss the role of inhibition of
return (IOR) in the control of action. They review imaging and neuro-
psychological evidence distinguishing between IOR of spatial locations and
IOR of objects, and they provide novel evidence for long-lasting object-
based IOR, operating over at least 20 minutes. This new evidence suggests
that there can be inhibition of episodic memory traces, affecting behaviour
over the long term. This object-based IOR provides a flexible mechanism for
selecting objects for action.
In Part II, the chapters deal more specifically with the neural underpin-
nings of attention in action. In Chapter 9, Graziano et al. discuss recent
studies from their laboratory in which they examined motor responses
elicited by prolonged stimulation of motor cortex and surrounding regions.
In contrast to previous work, Graziano et al. demonstrate that complex, goal-
directed movements can be evoked from stimulation. Stimulation of pri-
mary motor cortex generates actions in central space, where monkeys most
often manipulate objects with their fingers. Stimulation in premotor cortex
evoked a variety of other responses, including apparent defensive move-
ments (e.g. to defend the head). These striking findings contradict the view
that actions are constructed in a hierarchical fashion, suggesting instead that
the motor cortex may include a topographic map of postures that are of
behavioural relevance to individuals.
In the Chapter 10, Rushworth and Ellison differentiate between parietal
areas concerned with attention to movement and those concerned with
visuospatial attention. Thus lesions and transcranial magnetic stimulation
(TMS) of posterior parietal cortex affect the redirecting of visuospatial
attention from one location to another, while lesions and TMS of left
anterior parietal cortex interfere with the redirecting of motor attention
from one movement to another. Hence at a neural level, some distinction is
possible between attentional circuits involved in the control of action and
visuospatial attention, even if these processes interact at a functional level
(see also Chapters 1 and 3).
In Chapter 11, Passingham et al. discuss fMRI studies for the learning of
motor sequences. They demonstrate activity in the dorsal prefrontal cortex
during initial learning, which subsequently reduces to baseline levels. How-
ever, the dorsal prefrontal cortex is reactivated when participants are asked to
attend to their actions. They argue that, during attention to action, there are
top-down interactions between the prefrontal and premotor areas, with the
prefrontal cortex serving to integrate information about the external context
and the individual’s goals.
 Preface xv
Chapman et al., in Chapter 12, attempt to identify the neural correlates
underlying selective reaching and grasping when multiple objects are present.
When targets appeared at predictable locations, activations in the left pari-
eto-occipital sulcus and the right intraparietal sulcus were found; however,
when the distractors were visible at all times, reducing the need for selection,
only the right occipital cortex was found to be more activated when the
distractors were present relative to when they were absent. Chapman et al.
suggest that the left parieto-occipital sulcus and the right intraparietal sulcus
specifically mediate the selection of objects for action.
In Chapter 13, Jackson et al. present neuropsychological evidence on
action control and planning. They document data from two patients with
optic ataxia (a deficit in misreaching to visual information) following damage
to parietal cortex. Traditionally, optic ataxia has been conceptualized as a
problem in integrating spatially congruent eye and hand movements, due to
damage to parietal systems that code and transform visual information for
action. Jackson et al., however, argue for a different interpretation, suggesting
instead that there is a problem in representing simultaneously two “visuo-
motor objects”, in different frames of reference, for different actions (hand
and eye movements). The parietal lobe may be crucially important for
maintaining these “visuomotor objects” for independent actions.
In the final chapter, Ward and Danziger discuss the role of a subcortical
structure, the pulvinar, in relation to the control of action. They question
theories that the pulvinar is critical for the spatial filtering of stimuli on the
contralesional side of space, arguing instead that the pulvinar is involved in
modulating the activation of responses to such stimuli, especially under
conditions of response competition. They suggest that the pulvinar appears
to be involved both in binding a stimulus representation to a response, and in
binding visual features to coherent representations of visual objects.
Taken together, the work reported here helps to provide new constraints
on our understanding of the relations between attention and action, paving
the way for the development of detailed accounts of perceptuo-motor func-
tion. We very much look forward to these developments, not least because
of the prospect of generating theoretically informed therapies for patients
with perceptuo-motor dysfunction.
We are very grateful to several organizations and individuals who made
both the conference and this book possible. We thank the Experimental
Psychology Society, whose workshop fund supported the conference,
together with the Medical Research Council, Wellcome Trust and Stroke
Association (UK), who fund our research. The running of the meeting was
helped by Marietta Remoundou and Eun Young Yoon, and most especially
by Elaine Fox. Thanks to you all.

Glyn W. Humphreys
M. Jane Riddoch
June 2003
Part I

Functional processes