Unilateral Neglect: Clinical and Experimental Studies
edited by Ian H. Robertson and John C. Marshall
Robin Walker
Department of Psychology
University of Durham
Durham
DH1 3LE
UK
robin.walker@durham.ac.uk
Copyright (c) Robin Walker 1994
PSYCHE, 1(8), August 1994
Previously hled: http://psyche.cs.monash.edu.au/v1/psyche-1-8-walker.html
Keywords: awareness, neuropsychology, representation, unilateral neglect,
visual attention
1.1 Unilateral Neglect: Clinical and Experimental Studies is a recent
title in the series published by Lawrence Erlbaum on the theme of brain
damage, behaviour and cognition, which reflects the recent growth of
interest in the area of neuropsychology. Unilateral neglect is a
condition which has generated a great deal of interest in the past
decade, as it reveals a vast amount of often bewildering behavioural
manifestations. Given the explosion of papers on the subject a
coherent, well-written book is long overdue and also something of a
formidable undertaking. Ian Robertson and John Marshall have managed to
edit an excellent and comprehensive volume containing 15 well-written
chapters from 22 contributors (see appendix). The book manages to
combine the different approaches to the study of neglect in three
separate sections, providing an overview of the models; it also
discusses the rehabilitation of this perplexing neurological disorder.
If you are a student, postgraduate researcher, or lecturer interested in
visual attention or visual neglect, you will want to buy this book.
Clinicians and people working with neglect patients will also find it
invaluable as a reference and as a guide to the rehabilitation
techniques that may help patients overcome their deficits.
1.2 Neglect most typically occurs following a stroke in the region of the
right hemisphere of the brain and results in patients failing to respond
to stimuli, objects and even people located to their left (contralesional)
side. The failure to respond to and report left-sided stimuli is not due
to a primary visual field defect such as a left hemianopia (loss of vision
for the contralesional visual field). Some patients can be shown to have
intact visual fields (Walker et al., 1991) and yet still show profound
neglect on a wide range of tasks. Neglect is not related to any loss of
intellectual functioning in the patient. The first chapter from Ian
Robertson and John Marshall sets the scene by clearly stating that neglect
should be regarded as a ``cognitive inability'' to respond to contralesional
stimuli.
1.3 Before reviewing the book it may be worth considering what
neuropsychology is and what its aims are. Neuropsychology is the area
of psychology which aims to find out how the brain performs certain
cognitive functions by studying the range of deficits that patients show
following brain damage. One of the important assumptions of
neuropsychology is that the brain contains various specialised modules
for processing information. An example of this modularity is the
existence of two separate cortical visual pathways, one being
responsible for object recognition and one for spatial analysis
(Ungerleider and Mishkin, 1982; Milner and Goodale, 1993). Damage to
one of these pathways can leave the patient unable to recognise `WHAT'
an object is (object agnosia), while damage to the other pathway gives
rise to a problem of `WHERE' the object is located in space. This kind
of dissociation following localised brain damage can enable cognitive
scientists to learn more about the way these independent modules
contribute to the cognitive process of visual perception. A good
example of this technique has been the study of patients who exhibit a
phenomenon known as `blindsight' (Weiskrantz et al., 1974). Blindsight
patients have damage to their primary visual cortex and a genuine visual
field deficit, but can still make accurate pointing responses to stimuli
presented in the `blind' regions. The interesting question is: if the
patients can `see' the stimulus well enough to point to it, why aren't
they consciously aware of it? Unilateral neglect is, in a sense, the
opposite side of this coin. A patient with neglect fails to respond and
report objects and stimuli presented in the region opposite to the
lesion site, but has an otherwise intact visual field. It has been
demonstrated that the `neglected' stimulus is processed covertly, to a
high level outside of conscious awareness (Marshall and Halligan,
1988). Why is the patient no longer consciously aware of something which
falls into an otherwise intact sensory field, and what can this help to
show us about the nature of brain functioning?
1.4 One of the unresolved issues in neglect concerns the two different
explanations commonly used to account for the phenomenon. These
accounts can be summarised as follows: neglect results from damage to
the attentional orienting system; alternatively, neglect is also
attributed to the failure to construct a complete mental representation
of contralesional space. The attentional theories of neglect suggest
that patients fail to shift their attention to the left side of space
and also have a tendency to automatically shift their attention to the
right side of space. This reluctance to shift attention to the left,
coupled with a strong tendency to orient attention to the right, results
in the patient being unaware of left-sided stimuli. The
representational view has received strong support from Italian workers
who have demonstrated that neglect can occur for the left side of a
mental image. Bisiach et al., (1979) demonstrated that neglect patients
failed to report the left-sided differences of pairs of cloud-like
patterns, when viewed behind a narrow central slot. This presentation
enabled the patients to view all of the pattern in central vision, but
patients still failed to notice differences in the left sides of these
patterns, which appears to provide strong support for the
representational hypothesis. The status of these different hypotheses
may become clearer as we look in detail at some of the chapters.
1.5 The book is made up of three sections entitled: `What is neglect?';
'The neuropsychological processes underlying neglect'; and `The
rehabilitation of neglect.'
1.6 The first section contains two chapters. The first by Halligan and
Marshall provides a historical overview of neglect, while in the second
Vallar has examined the `anatomical basis of neglect in humans'. Vallar
confirms that the posterior region of the inferior parietal lobe in the
right hemisphere is the region most commonly associated with neglect.
Cases of neglect have also been reported following damage to subcortical
structures such as: the thalamus, the basal ganglia circuit and lesions
to the white matter. Neglect following thalamic damage may be related
to damage to the pulvinar, while basal ganglia damage could also involve
damage to the substantia nigra. The parietal lobe, pulvinar region of
the thalamus and basal ganglion are all interconnected. Vallar's
interpretation is that neglect results from damage to these cortical and
subcortical structures because they form part of a neural circuit which
is involved in spatial representation and conscious awareness. Damage
to selective parts of this circuit could have an influence on other
structures which may help explain the distinctions between neglect for
near and far space and the dissociable perceptual and motor aspects of
neglect. Vallar has applied his knowledge of functional anatomy to
support the representational view of neglect. However, as a proponent
of the attentional view, I would suggest a different functional role of
this circuit. The inferior parietal lobe, the posterior regions of the
thalamus (pulvinar) and the substantia nigra (part of the basal ganglia
circuit) are all structures that are involved in the production of fast
eye movements (saccades). The parietal cortex receives input from the
pulvinar and has efferent connections to the superior colliculus, one of
whose functions is thought to be the translation of the sensory input
into a motor output. Activity in the colliculus is subject to
inhibition from, amongst other regions, the substantia nigra. Theories
of how visual attention may be oriented have hypothesised a link between
the neural systems involved in saccade generation (e.g. Rizzolatti et
al., 1987; Shepherd et al., 1986). The argument is that a shift of
visual attention may be performed by the same system that is required to
program a saccadic eye movement. Damage to part of the system involved
in producing a saccade would impair the patients' ability to shift their
eyes and attention to the contralesional side of space. The lack of an
attentional shift could then result in the failure of neglect patients
becoming aware of the stimulus presented there.
1.7 The second part of the book, `Neuropsychological processes
underlying neglect,' contains ten chapters, covering both the
attentional and representational theories of neglect. All of the
chapters are good, but I will consider only a few of them. Kinsbourne's
chapter reviews the development of his opponent processor model of
neglect. Kinsbourne's model is based on the notion that the left
hemisphere of the brain controls attentional shifts towards the right
and the right hemisphere controls attentional shifts towards the left.
The processes involved in producing the orienting responses are thought
to be reciprocally connected, which results in crossed inhibition. An
active left hemisphere processor inhibits the right hemisphere processor
and an active right hemisphere will inhibit the left. Damage to the
right hemisphere will leave the left hemisphere orienting system
'over-activated' resulting in a tendency for neglect patients to bias
their attention to the right. Indeed, neglect patients have been shown
to make faster manual responses to visual stimuli presented further away
from the fovea (further rightwards) than to stimuli presented near to
the fovea. Kinsbourne's view is that the brain damage associated with
neglect results in an attentional gradient present in both hemispaces,
which results in attention being directed to the right regardless of the
'absolute location' of the stimulus. This idea is useful in explaining
why neglect can occur for the left side of a stimulus presented briefly
(tachistoscopically) entirely within the right hemifield. Kinsbourne's
view of an attentional gradient biased to the right of the entire visual
field is consistent with the performance of many patients who show a
strong bias to attend to the right side of a stimulus wherever it
appears in space.
1.8 The representational/attentional debate continues in the notable
chapter by Rizzolatti and Berti. From the beginning they state that
neglect can best be thought of as a disorder of `spatial awareness.'
Spatial awareness is thought to be derived from ``joint activity of
several cortical and subcortical areas, each of which has its own neural
space representation.'' These areas are also involved in controlling
motor responses, so damage to the representation would also result in
impaired motor activity. Finally, they state that ``attentional deficits
which may accompany neglect are a secondary consequence of the lesion of
space representations.'' Rizzolatti supports his argument first by
reviewing models of attention and considering what the term `attention'
actually means. There is no one single accepted definition of
attention. It has been regarded as a filtering process, as a spotlight
to enhance perception and as a mechanism responsible for the selection
of action. The spotlight view of attention is that it operates as a
selection procedure to allow a stimulus to be identified and reach
conscious awareness. Damage to the patient's ability to orient this
spotlight impairs his or her conscious awareness of stimuli. Rizzolatti
points out that according to this view the patient would have a lack of
awareness of any type of stimulus in any part of space. A single
attentional centre cannot account for the many dissociations shown in
neglect. Rizzolatti also gives a good account of the `selection for
action' view of attention. According to this theory attention is seen
as a modular function operating within several independent neural
networks concerned with producing a motor response to a sensory
stimulus. The facilitation of perception due to attentional mechanisms
is accounted for by the activation of the relevant motor circuit. This
is a most convincing model of attention. It fits with Rizzolatti's own
pre-motor theory of attention (Rizzolatti et al., 1987) and also fits
with recent work on patients with parietal lobe damage (Milner and
Goodale, 1993).
1.9 Rizzolatti, however, proposes that activity in several brain centres
forms a representation of space and is responsible for our conscious
space awareness. Space is coded in a viewer-centred co-ordinate system,
damage to this system results in neglect. The multiple spatial
representations are also involved in the control of motor
programmes. Any attentional deficit is thought to be a secondary
consequence of damage to the representation involved in producing a
motor response. Rizzolatti does not state whether this representation of
space is topographically organised in the same way that the primary
visual cortex provides a retinotopic map of our visual fields. Although
it is convenient to think of the brain as containing a topographical map
of space, as this confirms our subjective impression of having a map of
object spatial location, Stein (1992) has recently argued that our
representation of external space cannot be topographically organised.
Stein proposed that the role for the posterior parietal cortex is in
forming part of a network concerned with transforming sensory inputs
into motor coordinates; attention plays a part in mediating this
transformation process. The multiple brain circuit approach advocated
by Rizzolatti is useful in providing a way of explaining the
dissociations shown in neglect (such as: neglect for near or far space,
neglect for left sided objects or neglect for the left side of an
object). This multiple spatial representational view is also very
similar to the multiple attentional channels view already described. The
important issue seems to be to determine what is necessary for the
conscious awareness of stimuli; an intact representation of viewer
centred space, or the attentional selection of a stimulus under the
control of a spatial representation.
1.10 Some of the next chapters in the `neuropsychological processes'
section have taken into account the theories about normal visual
functioning and related these to the findings from neglect. Like all
good neuropsychology the implications from neglect are used to help
model how the system may function in the intact brain. Farah's
contribution takes into account the notion of parallel visual channels
(WHAT and WHERE) thought to be responsible for object perception and
spatial location. She examines the nature of the representation to
which attention is allocated; i.e., is it allocated to an object centred
representation, or to a spatial representation? Farah reviews the
evidence to show that the impairment of attentional allocation in
neglect can occur both in location-based and in object-based
co-ordinates. She uses the example of `neglect dyslexia' shown when
patients make reading errors to the left side of single words. It has
been demonstrated that neglect patients omit fewer left- sided letters
from real words, than from non-words. In Farah's view this is not
because the word's representation facilitates word recognition (top-down
processing), but is due to attention being deployed on an object-based
reference frame. The result is that attention is allocated further to
the left of a real word than a non-word, which reduces left-sided letter
omissions made to real words. Some support for this view comes from the
finding that left-sided neglect is reduced in line bisection to a
greater extent when a real word is above the line, than when a non-word
is above the line. Farah holds that ``attention operates on
representations of spatial location,'' and also that ``attention has
considerable object knowledge.'' Farah's view of attention seems to be
consistent with the `zoom lens' metaphor often used to describe
attentional deployment. There is, however, good evidence for attention
being allocated in either object-based or spatial reference frames, and
this is important for the view of distinct attentional modules needed
for appropriate motor responses. The main weakness of this chapter is
the lack of any discussion about what attention is.
1.11 The chapters by Humphreys and Riddoch and by Lynn Robertson and
Eglin examine the performance of neglect patients on visual search
tasks. Both of these chapters provide support for the attentional
models of neglect. Humphreys and Riddoch emphasise in their model that
attention is oriented on the basis of low-level features. Once
attention is oriented to a location, feedback into the separate object
recognition system can enhance the processing of the object
description. Robertson and Eglin show that neglect patients have three
attentional deficits on visual search tasks: patients show a directional
bias when scanning the right side of a display; they are generally
impaired at searching anywhere in the display; and they also appear to
have problems `disengaging' attention from the right side to move
attention into the left side of the display. The right-sided bias of
attention shown in neglect may reflect a rightward attentional bias
found in normals (cf. Kinsbourne).
1.12 The remaining chapters in this section consider the spatial
dimensions of neglect (Ladavas), the reference frames involved in
neglect (Werth), and neglect and visual language (Ellis, Young and
Flude). Ellis et al. examine neglect- dyslexia reading errors, and the
problems in spelling and writing shown by neglect patients. Along with
a variety of neglect patients who make left-sided reading errors, they
also review the findings from one intriguing patient, N.G., who when
reading, writing and spelling made errors for the letters at the right
end of the words. They also provide a good account of the implications
that can be drawn from neglect for the language process. Neglect could
affect the encoding of the low-level representation of the left-sided
letters in a `stimulus centred letter shape map.' The resulting
(partial) representation activates the wrong entry in the orthographic
lexicon, the structure that contains the memory representation of
familiar words. N.G.'s performance suggests that the same disrupted
representation may be involved in reading, spelling and writing. This
chapter provides a good illustration of how we can learn more about the
functioning of the cognitive system from the study of patients with
neurological impairments.
1.13 The final chapter in this section is by Ian Robertson and
highlights a further attentional deficit that may be important in
neglect. Robertson argues that neglect results not only from an
impairment in the orienting and disengagement of visual attention, but
also from damage to an alerting or vigilance system which is located in
the right hemisphere. This vigilance component is non spatial and plays
a role in increasing the rate to which attention can respond to a
stimuli. Damage to the right hemisphere would cause low levels of
vigilance that would result in profound and sustained left-sided
neglect. Patients with left hemisphere damage typically show a quick
recovery from signs of right neglect. According to Robertson the left
brain damage leaves the vigilance component intact enabling them to
learn to compensate from their deficits of attentional orienting and
disengagement.
1.14 The third section of the book contains two chapters on the
rehabilitation of neglect (Ian Robertson, Halligan and Marshall; Diller
and Riley). Robertson et al. considers the study of rehabilitation to
be important in providing informative practical and theoretical insights
into the condition. Studies that have tried to train neglect patients
to scan the left side have had rather limited success in reducing the
patients neglect. Two techniques have been shown to reduce neglect;
namely, activation of the affected limb in the neglected hemispace and
vestibular stimulation by the injection of iced water into the left
ear. The effectiveness of voluntary limb activation supports the view
that neglect could be caused by an impairment from modular circuits
involved in programming motor actions. The mechanism behind vestibular
stimulation is less clear. Theories of attentional orienting have
suggested a link between the neural systems involved in shifting the
eyes and those involved in shifting attention. The vestibular system is
linked to the eye movement system, so vestibular stimulation may perhaps
induce an attentional shift via this mechanism.
1.15 As an overview I find that this book is extremely informative and
provides excellent discussions of the theories of visual neglect and
also reflects on the implications for models of normal cognitive
functioning. One criticism is the frequent use of the term `attention'
without stating exactly what the author means by the term. At times,
attention becomes like an all-encompassing homunculus that guides our of
perceptions and actions and leads to conscious awareness. It is
described as a spotlight, or zoom lens, that can be oriented and moved
around, thus facilitating our perception of stimuli. Attention is also
used to solve the problem of how activity in columns of single cells can
be combined to form a representation of a single object when more than
one object is present at nearby retinal locations (the `binding
problem'). Attention may also be involved in programming motor
responses depending on the stimulus and the required motor output. A
quote from Allport (1993) illustrates the difficulties associated with
the term: ``there can be no simple `theory of attention', any more than
there can be a simple `theory of thought'. A humbler but also more
ambitious task will be to characterise, in cognitive neurobiological
terms, as much as is possible of this diversity of attentional
functions.'' In the last chapter Marshall, Halligan and Ian Robertson
consider this problem and argue that there is no single entity of
neglect and that there could be whole range of attentional and
representational deficits hiding behind this term. They emphasise the
modular approach to the study of selective attention, and the need to
further fractionate the neglect syndrome in terms of information
processing models of spatial cognition. This book provides an
informative review of the issues involved in the study of visual
neglect, while acknowledging that, as in the case of blindsight, some of
the most interesting questions still remain to be answered.
References
Allport, A. (1993). Attention and control: have we been asking the wrong
question? Tutorial review in D.E. Meyers and S. Kornblum (Eds.),
Attention and Performance, 14,183-219.
Bisiach, E., Luzzatti, C., & Perani, D. (1979). Unilateral neglect,
representational schema and consciousness. Brain, 102, 609-618.
Marshall, J. C., & Halligan, P. W. (1988). Blindsight and insight in
visuo-spatial neglect. Nature, 336(22/29), 766-767.
Milner, D. A., & Goodale, M. A. (1993). Visual pathways to perception
and action. In T. P. Hicks, S. Molotchnikoff, & T. Ono (Eds.),
Progress in Brain Research Vol. 95 (pp. 317 - 337). Elsevier Science
Publishers.
Rizzolatti, G., Riggio, L., Dascola, I., & Umilta, C. (1987).
Reorienting attention across the horizontal and vertical meridians:
Evidence in favour of a premotor theory of attention. Neuropsychologia,
25(1A), 31-40.
Shepherd, M., Findlay, J. M., & Hockey, R. J. (1986). The relationship
between eye movements and spatial attention. Quarterly Journal of
Experimental Psychology, 38, 475-491.
Stein, J. F. (1992). The representation of egocentric space in the
posterior parietal cortex. Behavioral and Brain Sciences, 15,
691-700.
Ungerleider, L. G. and Mishkin, M. (1982). Two cortical visual systems.
In D.J. Ingle, M.A. Goodale and R.J.W. Mansfield (Eds.), Analysis of
visual behavior (pp. 549 - 587). Cambridge, Mass.: MIT press.
Walker, R., Findlay, J. M., Young, A. W., & Welch, J. (1991).
Disentangling neglect and hemianopia. Neuropsychologia, 29(10),
1019-1027.
Weiskrantz, L., Warrington, E. K., Sanders, M. D., & Marshall, J.
(1974). Visual capacity in the hemianopic field following a restricted
occipital ablation. Brain, 97, 709-728.
Appendix 1
Contents of: Unilateral Neglect: Clinical and Experimental Studies
edited by Ian H. Robertson and John C. Marshall
Part 1. What is neglect?
[Ch. 1.] The history and clinical presentation of neglect.
Halligan, P.W. and Marshall, J.C.
[Ch. 2.] The anatomical basis of spatial hemineglect in humans.
Vallar, G.
Part 2. Neuropsychological processes underlying neglect.
[Ch. 3.] Orientational bias model of unilateral neglect: Evidence from
attentional gradients within hemispace. Kinsbourne, M.
[Ch. 4.] Neural mechanisms of spatial neglect. Rizzolatti, G. and Berti, A.
[Ch. 5.] The role of spontaneous eye movements in orienting attention and in unilateral neglect. Gainotti, G.
[Ch. 6.] `What' and `Where' in visual attention: Evidence from the neglect
syndrome. Farah, M.J., Wallace, M.A., Vecera, S.P.
[Ch. 7.] Interactive attentional systems and unilateral visual neglect.
[Ch. 8.] Attentional search in unilateral visual neglect. Robertson,
Lynn C. and Eglin, M.
[Ch. 9.] Spatial dimensions of automatic and voluntary orienting
components of attention. Ladavas, E.
[Ch. 10.] Shifts and omissions in spatial reference in unilateral
neglect. Werth, R.
[Ch. 11.] Neglect and visual language. Ellis, A.W., Young, A.W. and
Flude, B. M.
[Ch. 12.] The relationship between lateralised and non-lateralised
attentional deficits in unilateral neglect. Robertson, Ian H.
Part 3. Rehabilitation of unilateral neglect.
[Ch. 13.] Prospects for the rehabilitation of unilateral neglect.
Robertson, I.H., Halligan, P.W. and Marshall, J.C.
[Ch. 14.] The behavioural management of neglect.
Diller, L. and Riley, E.
Coda
[Ch. 15.] Contemporary theories of unilatera
