Content uploaded by Andy Simmons
Author content
All content in this area was uploaded by Andy Simmons on Dec 20, 2013
Content may be subject to copyright.
Psychological Medicine, 2000, 30, 873–883. Printed in the United Kingdom
"2000 Cambridge University Press
Imaging attentional and attributional bias: an fMRI
approach to the paranoid delusion
N. J. BLACKWOOD,"R. J. HOWARD, D. H. ffYTCHE, A. SIMMONS, R. P. BENTALL
R. M. MURRAY
From the Departments of Psychological Medicine and Neuroimaging Research,Institute of Psychiatry,
London; and Department of Clinical Psychology,University of Manchester
ABSTRACT
Background. The pathophysiology of auditory hallucinations and delusions of control has been
elucidated using functional imaging. Despite their clinical importance, there have been few similar
attempts to investigate paranoid delusions. We have examined two components of social cognition
(attentional and attributional biases) that contribute to the formation and maintenance of paranoid
delusions, using functional magnetic resonance imaging (fMRI).
Method. Normal subjects performed tasks requiring attentional and attributional judgements. We
investigated the neural response particularly associated with attention to threatening material
relevant to self and with the ‘self-serving ’ attributional bias.
Results. The determination of relevance to self of verbal statements of differing emotional valence
involved left ventrolateral prefrontal cortex (left inferior frontal gyrus, BA 47), right caudate and
right cingulate gyrus (BA 24). Attention to threatening material relevant to self differentially
activated a more dorsal region of the left inferior frontal gyrus (BA 44). Internal attributions of
events, where the self was viewed as an active intentional agent, involved left precentral gyrus (BA 6)
and left middle temporal gyrus (BA 39). Attribution of events in a non ‘self-serving’ manner
required activation of the left precentral gyrus (BA 6).
Conclusions. Anomalous activity or connectivity within these defined regions may account for the
attentional or attributional biases subserving paranoid delusion formation. This provides a simple
model for paranoid delusion formation that can be tested in patients.
INTRODUCTION
Classical definitions of delusions maintained
that they were qualitatively different from
normal beliefs and attitudes (Jaspers, 1912) but
more recent phenomenological studies support
the idea that delusions lie at the extreme end of
a ‘belief continuum ’ (Kendler et al. 1983 ;
Spitzer, 1990; Chadwick, 1992; Peters et al.
1998; Verdoux et al. 1998). Models that seek to
explain paranoid delusions in terms of specific
neuropsychological or reasoning deficits have
had only limited explanatory success (Winters
& Neale, 1983; Maher, 1988; McKenna, 1997 ;
"Address for correspondence: Dr Nigel J. Blackwood, De-
partment of Psychological Medicine, Institute of Psychiatry, De
Crespigny Park, London SE5 8AF.
Simpson et al. 1998). Thus, no specific neuro-
psychological deficits, for example in mnemonic
(McKenna et al. 1990; Saykin et al. 1994) or
executive function (Goldberg et al. 1987, 1990),
consistently correlate with measures of paranoid
delusions (Shallice et al. 1991; Mortimer et al.
1996; Elliot et al. 1998). Deluded patients
experience difficulties in probabilistic (Huq et al.
1988; Garety et al. 1991 ; Fear & Healy, 1997 ;
Dudley et al. 1997; Young & Bentall, 1997),
inductive (John & Dodgson, 1994) and in-
ferential reasoning tasks (Kemp et al. 1996), but
paranoid delusions often emerge as misinter-
pretations of social interactions and events
rather than of neutral or impersonal events. It
seems likely that in social situations where
complex inferences are required, special purpose
873
874 N. J. Blackwood and others
cognitive modules rather than conscious reason-
ing processes are used (Brothers, 1990 ; Brothers
& Ring, 1992; Deakin, 1994).
Paranoid delusions may thus represent a
disturbance of the psychological processes me-
diating the formation and maintenance of
normal social beliefs. Two of the putative
components of processing in the social cognitive
domain have been investigated using measures
of attentional (Bentall & Kaney, 1989) and
attributional biases (Bentall, 1994). Selective
attention to self-referential or threatening in-
formation may lead an individual to form
conclusions about the environment that appear
delusional to others (Ullman & Krasner, 1969).
This attentional bias has been consistently
demonstrated in people with paranoid delusions
(Bentall & Kaney, 1989 ; Kaney et al. 1992 ;
Bentall et al. 1995; Fear et al. 1996 ; Leafhead et
al. 1996). In addition, patients with paranoid
delusions show an exaggeration of the ‘ self-
serving’ attributional bias found in normal
subjects (that is, the tendency to take credit for
success and to deny responsibility for failure),
which may have a role in maintaining self-
esteem. They excessively attribute hypothetical
positive events to internal (self), global (likely to
affect other areas of life) and stable (unchange-
able) causes and hypothetical negative events to
external (circumstances or other people), global
and stable causes (Kaney & Bentall, 1989;
Candido & Romney, 1990; Lyon et al. 1994 ;
Fear et al. 1996; Sharp et al. 1997). Paranoid
patients are additionally abnormal in that
negative events are attributed to active mal-
evolence on the part of the other (external
personal attribution) rather than to the play of
circumstances or chance (external situational
attribution) (Kinderman & Bentall, 1997). It has
been argued that this bias is a proximal cause of
patients’ delusional content, and partly reflects a
theory of mind deficit (that is, an inability to
understand the mental states of others) observed
in paranoid patients by other researchers
(Corcoran et al. 1995, 1997; Frith & Corcoran,
1996; Langdon et al. 1997 ; Sarfati et al. 1997 ;
Doody et al. 1998; Kinderman et al. 1998).
A cognitive neuropsychiatric approach to
paranoid delusions seeks to develop an ex-
planatory model in terms of these underlying
cognitive abnormalities that can in turn be
mapped onto structural and functional neuro-
pathology. Such an approach has been successful
in developing models for auditory hallucinations
and delusions of control (Frith et al. 1992 ;
Liddle et al. 1992; McGuire et al. 1995, 1996;
Silbersweig et al. 1995; Spence et al. 1997).
However, despite their clinical importance, few
attempts have been made to characterize para-
noid delusions in functional imaging terms. All
the imaging studies to date have examined either
the reality distortion symptom cluster (delusions
and hallucinations) (Liddle, 1987; Thompson &
Meltzer, 1993) or ‘delusions ’ as a single entity.
In an early PET study, Liddle and colleagues
(1992) attempted to correlate symptomatic pat-
terns with regional cerebral blood flow (rCBF)
in patients with chronic schizophrenia. Signif-
icant positive correlations were demonstrated
between the reality distortion dimension and
regional cerebral blood flow in left temporal (left
superior temporal pole (BA 22) ; left parahippo-
campal area (BA 27\30)), frontal (left lateral
prefrontal cortex) and ventral striatal areas.
These findings accorded with these authors’ a
priori hypothesis of left temporal lobe dys-
function in reality distortion driven by evidence
that the psychosis associated with left-sided
temporal lobe epilepsy is characterized by
delusions and hallucinations. This finding was
partially corroborated by a PET study of never
treated schizophrenics (Kaplan et al. 1993),
where the reality distortion dimension was
positively associated with left-sided temporal
activity. The salience of these areas was further
demonstrated by two SPECT studies of never
treated schizophrenics (Ebmeier et al. 1993;
Sabri et al. 1997), which found strong negative
correlations between delusion scores and left
frontal, cingulate, left temporal and left thalamic
rCBF. Spence and colleagues (1998) documented
hypoactivation of the left pre-frontal cortex
when patients who were symptomatically de-
luded performed a motor task; such regional
hypoactivation remitted with clinical improve-
ment in the delusions.
Little is known, however, of the brain regions
whose activity supports the attentional and
attributional components of social cognition.
We therefore examined normal volunteer sub-
jects while they were making attentional and
attributional judgements of the kind that are
Imaging attentional and attributional bias 875
most likely to be implicated in the formation
and maintenance of the paranoid delusions of
schizophrenic subjects.
METHOD
Subjects
Five normal male volunteers were recruited
from medical staff at the Maudsley Hospital for
this study. Their ages ranged between 28 and
36 years. All were right-handed as assessed by
the Annett handedness questionnaire and none
had any significant medical or psychiatric his-
tory. All gave informed consent. The study
design was approved by the Bethlem and
Maudsley ethics committee.
Cognitive activation paradigms
Attentional bias
The tasks were visually presented and consisted
of alternating 30 s conditions in an A(target
condition) B(reference condition) design, re-
peated five times, giving a total scan time of
5 min.
Experiment 1 – Neutral statements
The target condition consisted of potentially
self-referent neutral material (e.g. ‘he is eating’ ;
see Appendix 1 for complete list). The reference
condition consisted of other-referential neutral
material (e.g. ‘Graeme is eating’; names used
were different to those of the subjects). Within
each condition, four statements were each
presented for 7n5 s. The subject’s task during the
scan was to indicate by a button press whether
each statement referred to themselves or not.
Immediately after the scanning session, sub-
jects were debriefed and re-presented with the
experimental sentences rating each question on
a 5-point scale (where 1 l‘ This statement
definitely does not apply to me’ to 5 l‘This
statement definitely does apply to me’).
Experiment 2 – Threatening statements
The target condition consisted of potentially
self-referent threatening material (e.g. ‘he is
bugged’). The reference condition was other-
referential threatening material (e.g. ‘Brain is
bugged’). As for condition 1, both epochs con-
tained four statements, each presented for 7n5s.
Key response and debriefing were as before.
Attributional bias
Ten statements taken from the Internal, Personal
and Situational Attributions Questionnaire
(IPSAQ: Kinderman & Bentall, 1996) were each
presented visually for 30 s.
Experiment 3 – Attributions of positive events
A complete list of positive events (e.g. ‘A friend
said that she liked you’) is given in Appendix 2.
Subjects were asked to imagine vividly the event
happening to them and to decide internally the
main cause of the event, whether internal (was it
something about you?), external personal (was
it something about your friend?) or external
situational (was it something about the situation
(circumstances or chance)?) attribution. No
response was required in the scanner but
immediately after the scanning session, subjects
were debriefed and represented with the ex-
perimental sentences and asked to indicate their
attributional decision. Test–retest reliability re-
sults on the extended IPSAQ indicate that the
responses recorded after scanning are reliable
indicators of the responses formulated in the
scanner (R. Bentall, personal communication).
We specifically decided not to employ a key
press response during this experiment because
behavioural data acquired during the construc-
tion of the IPSAQ indicated that provision of
forced choice indicators led to a ‘bypassing’ of
internal envisioning of the event requiring an
attributional judgement.
Experiment 4 – Attributions of negative events
A complete list of negative events (e.g. ‘ A friend
talked about you behind your back) is given in
Appendix 2. Subjects were asked to imagine the
event vividly and were debriefed as before.
Functional magnetic resonance imaging
Gradient echo echoplanar (EPI) data was
acquired on a 1.5 Tesla GE Signa system fitted
with Advanced NMR hardware and software in
the Department of Neuroimaging at the Maud-
sley Hospital. One hundred T#*-weighted images
depicting blood oxygenation level dependent
(BOLD) (Kwong et al. 1992) contrast were
acquired with an in-plane resolution of 3 mm
(TR l3s;TEl40 ms) at each of 14 near-axial
non-contiguous 7 mm thick slices to include the
876 N. J. Blackwood and others
Sagittal Coronal Transverse(a)
Sagittal Coronal Transverse(b)
F. 1. Statistical parametric maps of the comparison : (a) attention to self attention to other for neutral and threatening
statements, thresholded at P0n05 (corrected) : (b) attention to self attention to other for threatening neutral statements,
thresholded at P0n05 (corrected).
Table 1. Coordinates of maximally significant foci in attention to self attention to other.
Coordinates (in millimetres)refer to the location in stereotaxic space of Talairach and Tournoux of
the voxels with the peak Zscore within a particular activated region (P 0n05 corrected )
Region
Coordinates
Zvaluexyz
(a) Neutral and threatening statements
Left inferior frontal gyrus (BA 47) k46 28 k44n38
Right caudate nucleus 10 k220 4n82
Right cingulate gyrus (BA 24) 20 k12 38 3n99
(b) Threatening statements Neutral statements
Left inferior frontal gyrus (BA 44) k58 8 24 4n68
whole brain (slice gap l0n7 mm). During the
same imaging session, a high contrast, high
resolution inversion recovery EPI dataset
(TE l74 ms ; TI l180 ms ; TR l1600 ms;
NEX l8) with an in-plane resolution of 1n5mm
and 3 mm slice thickness was acquired.
Image analysis
Image pre-processing and statistical analysis
were performed in SPM96 (http:\\www.
fil.ion.ucl.ac.uk\spm). Images were realigned,
normalized and smoothed with a 10 mm full-
width at half-maximum filter using standard
methods. Data from the attentional and attrib-
utional bias experiments were analysed in sep-
arate design matrices. For the attentional bias
experiments, data from all 10 experiments were
included in a single matrix (5 subjectsineutral
and threatening statement conditions) allowing
a factorial analysis of main and interaction
effects. For the attributional bias experiments,
two of the 10 data sets were excluded as post-
scan ratings of the statements presented were all
given a single value (see below). While the
factorial designs of both experiments allow us to
test for a number of effects (eight in each
Imaging attentional and attributional bias 877
experiment), we restrict ourselves here to those
that have direct relevance to the models of
paranoid delusion formation presented above.
For the attentional experiments the com-
parisons of interest are : (i) the main effect of
attention to self v. other (main effect of attention
to self); and, (ii) the influence of threat on this
activity (interaction effect).
For the attributional experiments the com-
parisons of interest are : (i) the main effect of
internal v. external attributions (main effect of
internal attribution); (ii) the conjoint effect of
internal attribution of negative events and
external attribution of positive events (con-
junction of task pair differences), representing
non-self-serving attributions; and (iii) the con-
joint effect of internal attribution of positive
events and external attribution of negative events
(conjunction of task pair differences), repre-
senting self-serving attributions.
Significance was based on Zscore and
threshold at P0n05 corrected for multiple
comparisons.
RESULTS
Neural correlates of attentional bias
Post-scan ratings of potential reference to self
and other were significantly different in the
target and control conditions for both neutral
(chi-squared test : Pearson l59n74, P0n001)
and threatening conditions (chi-squared test:
Pearson l27n27, P0n001). Attention to self
compared with other for neutral and threatening
statements (the main effect of self) was associated
with increased activity in left inferior frontal
gyrus, right caudate nucleus and right cingulate
gyrus (Fig. 1(a) and Table 1 (a)). Attention to
self compared with other for threatening state-
Sagittal Coronal Transverse
F. 2. Statistical parametric maps of the comparison : internal external (personal and situational) attributions for positive and
negative events, thresholded at P0n05 (corrected).
ments, but not for neutral statements (the
interaction effect), was associated with increased
activity in left inferior frontal gyrus (Fig. 1(b)
and Table 1(b)).
Neural correlates of attributional bias
In the post-scan ratings of internal, external
personal and external situational attributions,
some subjects reported that they had not
attributed any events to external situational
causes when in the scanner. We therefore
collapsed the three catagories (internal, external
personal and external situational) into two
(internal and external). Two subjects reported
all their attributions of negative events as
external and are therefore excluded from the
negative attribution analysis.
Attribution to internal causes compared with
external causes for positive and negative events
(the main effect of internal attribution) was
associated with increased activity in left middle
temporal gyrus and left precentral gyrus (Fig. 2
and Table 2).
Attribution to internal causes of negative
Table 2. Coordinates of maximally significant
foci in internal external (personal and sit-
uational)attributions.Coordinates (in milli-
metres)refer to the location in stereotaxic space
of Talairach and Tournoux of the voxels with the
peak Zscore within a particular activated region
(P 0n05 corrected )
Region
Coordinates
Zvaluexyz
Positive and negative events
Left precentral gyrus (BA 6) k52 k438 5n00
Left middle temporal gyrus (BA 39) k46 k50 12 4n47
878 N. J. Blackwood and others
Sagittal Coronal Transverse
F. 3. Statistical parametric maps of the conjoint effect of internal attribution of negative events and external attribution of
positive events, representing non-self-serving attributions, thresholded at P0n05 (corrected).
Table 3. Coordinates of maximally significant
foci in the internal attribution of negative events
and external attribution of positive events,repre-
senting non-self-serving attributions.Coordinates
(in millimetres)refer to the location in stereotaxic
space of Talairach and Tournoux of the voxels
with the peak Zscore within a particular activated
region (P 0n05 corrected )
Region
Coordinates
Zvaluexyz
Left precentral gyrus (BA 6) k40 k10 36 4n69
events and to external causes of positive events
(conjunction of task pair differences: non self-
serving attributions) was associated with in-
creased activity in left precentral gyrus (Fig. 3
and Table 3).
Attribution to internal causes of positive
events and to external causes of negative events
(conjunction of task pair differences: self-serving
attributions) was associated with activity in the
left superior temporal gyrus (BA 38) (xlk42,
yl4, zlk8), which only reached an un-
corrected threshold of significance (Zl4n37,
P0n001). This result will therefore not be
considered further.
DISCUSSION
Attentional bias
The adaptive behaviour of humans in the
environment relies on rapid monitoring of
potentially salient cues (typically of a high
emotional valence e.g. threatening stimuli). We
have demonstrated a neural substrate for the
determination of the relevance to self of en-
vironmental stimuli (verbal statements of differ-
ing emotional valence) in our normal volunteer
subjects, involving ventrolateral prefrontal cor-
tex (extending into lateral orbitofrontal cortex),
striatum and anterior cingulate.
Determination of self-relevance involves sem-
antic encoding of self-relevant statements and
retrieval of information from the self-schema.
Such encoding would be expected to involve
more elaborate semantic processing operations
(for example, implications for self and subject’s
intentions with respect to the stimulus) than the
encoding of other-relevant statements, and this
is reflected in left ventrolateral prefrontal cortex
activation (Kapur et al. 1994; Demb et al. 1995;
Wagner et al. 1998). This ‘deeper ’ level of
semantic processing would, in turn, be expected
to yield improved episodic memory for the self-
relevant statements in comparison to other-
relevant statements (Wagner et al. 1998). We
suggest that left ventrolateral prefrontal cortex
activation is in part responsible for the well
documented mnemonic superiority arising from
relating material to the self: the ‘self-referential’
memory effect (Symons & Johnson, 1997).
The activation within the left inferior gyrus
extends into the lateral orbitofrontal cortex.
Orbitofrontal cortex has historically been felt to
be important in the broad domain of behavioural
adaptation, encompassing social judgement,
self-regulation and self-awareness. It has been
implicated in the interface between affect and
cognition by brain imaging (Pardo et al. 1993 ;
Baker et al. 1997; Blair et al. 1999 ; Dougherty et
al. 1999), lesion (Damasio, 1996 ; Dias et al.
1996) and neurophysiology (Rolls, 1999) studies.
Neuronal cells in the orbitofrontal cortex re-
spond to information about reward or pun-
ishment, such that damage to the area is
associated with diminished ability in social
Imaging attentional and attributional bias 879
decision making and the detection of emotional
clues. In the context of this paradigm, it is likely
to be critical in both the determination of the
self-salience and the emotional significance of
the verbal statements.
One set of output pathways by which lateral
orbitofrontal cortex implements these functions
for behaviour is via the striatum (the lateral
orbitofrontal loop projects to ventro-medial
portions of the caudate) (Alexander et al. 1986).
Activation of the striatum in this manner
provides further evidence for its involvement in
‘egocentric’ memory i.e. stimulus–response
memory involving consistent reinforced res-
ponses to environmental cues (White, 1997).
The anterior cingulate forms part of the
anterior attentional network responsible for
focused attention (Goldman-Rakic, 1988). It is
involved in assessing the motivational content of
stimuli and in regulating context-dependent
behaviours (Devinsky et al. 1995). It has been
suggested that it interacts with the ventral
prefrontal area to mediate affective reactivity to
emotionally salient stimuli (Baker et al. 1997).
The lack of specific activation with threatening
statements found in this study favours its role in
the coordination of behavioural responses to
self-salient stimuli, independent of the emotional
valence of those stimuli.
Attention to threatening stimuli deemed rel-
evant to self differentially activated a more
dorsal region of the left inferior frontal gyrus.
This region is involved in inhibitory processing
across a range of cognitive domains (e.g. Taylor
et al. 1997; Jonides et al. 1998), and activation
here may represent the selective biasing or gating
of behaviourally relevant information from
semantic memory representations (Thompson-
Schill et al. 1997) or the mediation of behavioural
withdrawal elicited by threatening stimuli. We
would hypothesize that there would be excessive
activation (in terms of voxel number and
amplitude of response) in these defined regions
in the symptomatically deluded state, reflecting
excessive attention to self-referential (and in
particular threatening self-referential) infor-
mation.
Attributional bias
The process of imagining events and then making
an attributional decision is likely to engage
numerous cognitive processes. These include
ecphory (i.e. retrieval cues within the presented
sentences interacting with stored information so
that an image or representation of that in-
formation in question appears) (Tulving, 1983),
autonoietic awareness (the introspective process-
ing accompanying any recollection in which we
focus on our own subjective experience) (Tulv-
ing, 1993), hypothesis generation, hypothesis
testing and resolution of conflicting attributional
options. In addition, the stimuli are likely to be
encoded into declarative memory (allowing
subsequent recall of the sentences displayed).
However, these processes are common to both
internal and external attributional decisions and
are thus unlikely to be confounds in the direct
comparison between the two.
The neural activation observed with the
internal attribution of both positive and negative
events is therefore likely to represent the neural
activity linked to the representation of self as an
intentional or responsible agent (Fig. 2 and
Table 2). Both areas identified have been pre-
viously associated with conceptual processing
in brain imaging studies. The left premotor
cortex in BA 6 has been implicated in studies of
semantic processing, particularly of action words
(Martin et al. 1995, 1996; Chee et al. 1999),
imagined motor activity (Decety et al. 1994;
Leonardo et al. 1995; Grafton et al. 1996),
verbal working memory (Weinrich & Wise,
1982; Smith & Jonides, 1999), and in the
executive control task of response inhibition
(Bush et al. 1998). The left middle temporal
gyrus has been implicated in studies of semantic
processing (Demonet et al. 1992; Martin et al.
1995, 1996; Pugh et al. 1996). The required
semantic aspects of self stored in semantic
memory as self-representations may thus be
stored in this left middle temporal area. The
interaction between these two areas, therefore,
instantiates self in the imagination as an active
causative agent.
The ‘self-serving’ attributional bias (that is,
the internal attribution of positive events and
external attribution of negative events) seen in
normal subjects (and in an accentuated form in
paranoid patients) motivationally serves to
enhance self-esteem and may thus be regarded
as a ‘pre-potent’ response. The increased ac-
tivation of left precentral gyrus in non-self-
serving attributions (taking responsibility for
failure and considering other people or chance
880 N. J. Blackwood and others
factors to be responsible for success: Fig. 3
and Table 3) therefore represents the ac-
tivation inherent in inhibiting this pre-potent
‘self-serving’ bias (Carter et al. 1997 ; Bush et al.
1998). We would thus hypothesize that hypo-
activation of this left-sided prefrontal area in the
symptomatically deluded state would result in
the accentuation (via failure of inhibition) of the
‘self-serving’ attributional bias that has been
documented (Kaney & Bentall, 1989; Candido
& Romney, 1990; Lyon et al. 1994 ; Fear et al.
1996; Sharp et al. 1997).
Methodological issues
These novel experimental paradigms were ex-
amined using a small number of subjects (the use
of main effect and interaction analyses giving a
minimum Nof 8). The area activated specifically
in self-serving attributions failed to reach a
corrected threshold of significance, which may
be due to the exclusion of two negative event
attribution data sets (see results section).
Equally, it was not possible in this preliminary
study to examine the neural networks differ-
entially implicated in making external-personal
or external-situational attributions. While the
effects reported are rigorous for this group of
subjects, we cannot confidently consider them
representative of the normal population at this
stage. All of these processes will thus be
examined further in larger groups in future
experiments.
Conclusions
Our approach has been to detail the functional
neuroanatomy of attentional and attributional
judgements that appear to be of importance in
the formation and maintenance of paranoid
delusions. We are encouraged that the brain
areas activated in the experiments of particular
interest to our hypothesis (that is, attention to
threatening material relevant to self and the
‘self-serving’ attribution bias) are similar to
those correlated with delusion scores in patient
groups. They have, moreover, been shown to be
the site of both structural (Bogerts et al. 1985 ;
Benes & Bird, 1987; Buchanan et al. 1998 ;
Lawrie & Abukmeil, 1998; Goldstein et al. 1999)
and functional (Dolan et al. 1995; Frith et al.
1995; Andreasen et al. 1997 ; Stevens et al. 1998 ;
Fletcher et al. 1998) abnormalities in paranoid
schizophrenia. Anomalous activity or connec-
tivity within these distributed networks provides
a simple model for delusion formation that
can now be tested with functional imaging in
patients.
We thank Chris Andrew for technical assistance in
the performance of this study and two anonymous
reviewers for helpful comments on earlier versions of
this manuscript.
APPENDIX 1
MATERIALS FOR ATTENTIONAL BIAS
PARADIGMS
Experiment 1: Neutral statements
He is sleeping; he is resting; he is listening; he is
eating; he is breathing; he is awake; he is healthy; he
is tired; he is writing; he is talking; he is cooking; he
is calm; he is ready ; he is tidy ; he is hungry ; he is
watching; he is lying down; he is singing; he is
sneezing; he is determined.
Experiment 2: Threatening statements
He is bugged; he is a cheat; he is a coward; he is
useless; he is ugly; he abuses children; he is filthy; he
is illegitimate; he is hated; he is lazy; he is a pervert;
he is unfaithful; he is a racist; he is a rapist; he is a
liar; he is a sinner ; he is an alien ; he is a poisoner ; he
is a thief; he is a homosexual.
APPENDIX 2
MATERIALS FOR ATTRIBUTION BIAS
PARADIGMS
Experiment 3: Attributions of positive events
A friend bought you a present; a friend spent some
time talking to you ; a friend said that she admires
you; a neighbour invited you in for a drink; a friend
thinks you are trustworthy; a friend sent you a
postcard; a friend said that she liked you; a friend
rang to enquire about you; a friend visited you for a
friendly chat; a friend believes that you are honest.
Experiment 4: Attributions of negative events
A friend talked about you behind your back ; a friend
said that he has no respect for you ; a friend refused to
talk to you; a friend made an insulting remark to you ;
a friend said that he resents you ; a friend refused to
help you with a job; a friend picked a fight with you;
a friend thinks you are dishonest; a friend ignored
you; a friend betrayed the trust you had in her.
REFERENCES
Alexander, G. E., DeLong, M. & Strick, P. E. (1986). Parallel
organisation of functionally segregated circuits linking basal
ganglia and cortex. Annual Review of Neuroscience 9, 357–381.
Imaging attentional and attributional bias 881
Andreasen, N. C., O’Leary, D. S., Flaum, M., Nopoulos, P., Watkins,
G. L., Boles Ponto, L. L. & Hichwa, R. D. (1997). Hypofrontality
in schizophrenia: distributed dysfunctional circuits in neuroleptic-
naieve patients. Lancet 349, 1730–1734.
Baker, S. C., Firth, C. D. & Dolan, R. J. (1997). The interaction
between mood and cognitive function studied with PET. Psycho-
logical Medicine 27, 565–578.
Benes, F. M. & Bird, E. D. (1987). An analysis of the arrangement of
neurons in cingulate cortex of schizophrenic patients. Archives of
General Psychiatry 44, 608–616.
Bentall, R. P. (1994). Cognitive biases and abnormal beliefs : Towards
a model of persecutory delusions. In The Neuropsychology of
Schizophrenia (ed. A. S. David and J. Cutting), pp. 337–360.
Lawrence Erlbaum: London.
Bentall, R. P. & Kaney, S. (1989). Content specific information
processing and persecutory delusions: an investigation using the
emotional stroop test. British Journal of Medical Psychology 62,
355–364.
Bentall, R. P., Kaney, S. & Bowen-Jones, K. (1995). Persecutory
delusions and recall of threat-related, depression-related and
neutral words. Cognitive Therapy and Research 19, 331–343.
Blair, R. J. R., Morris, J. S., Frith, C. D., Perrett, D. I. & Dolan,
R. J. (1999). Dissociable neural responses to facial expressions of
sadness and anger. Brain 122, 883–893.
Bogerts, B., Meertz, S. & Schonfelt-Bausch, R. (1985). Basal ganglia
and limbic system pathology in schizophrenia. Archives of General
Psychiatry 42, 784–791.
Brothers, L. (1990). The social brain: a project for integrating
primate behaviour and neurophysiology in a new domain.
Controversies in Neuroscience 1, 27–51.
Brothers, L. & Ring, B. (1992). A neuroethological framework for
the representation of minds. Journal of Cognitive Neuroscience 4,
107–118.
Buchanan, R. W., Vlader, K., Barta, P. E. & Pearlson, G. D. (1998).
Structural evaluation of the prefrontal cortex in schizophrenia.
American Journal of Psychiatry 155, 1049–55.
Bush, G., Whalen, P. J., Rosen, B. R., Jenike, M. A., McInerney,
S. C. & Rauch, S. L. (1998). The counting stroop: an interference
task specialised for functional neuroimaging-validation study with
functional MRI. Human Brain Mapping 6, 270–282.
Candido, C. L. & Romney, D. M. (1990). Attributional style in
paranoid vs. depressed patients. British Journal of Medical
Psychology 63, 355–363.
Carter, C. S., Mintun, M., Nichols, T. & Cohen, J. D. (1997).
Anterior cingulate gyrus dysfunction and selective attentional
deficits in schizophrenia: ["&O] H#O PET study during single trial
stroop task performance. American Journal of Psychiatry 154,
1670–1675.
Chadwick, P. K. (1992). Borderline : A Psychological Study of
Paranoia and Delusional Thinking. Routledge: London.
Chee, M. W. L., O’Craven, K. M., Bergida, R., Rosen, B. R. &
Savoy, R. L. (1999). Auditory and visual word processing studied
with fMRI. Human Brain Mapping 7, 15–28.
Corcoran, R., Frith, C. D. & Mercer, G. (1995). Schizophrenia,
symptomatology and social inference : investigating ‘Theory of
Mind’ in people with schizophrenia. Schizophrenia Research 17,
5–13.
Corcoran, R., Cahill, C. & Frith, C. D. (1997). The appreciation of
visual jokes in people with schizophrenia : a study of mentalising
ability. Schizophrenia Research 24, 319–327.
Damasio, A. R. (1996). The somatic marker hypothesis and the
possible functions of the prefrontal cortex. Philosophical Trans-
actions of the Royal Society of London.Series B:Biological
Sciences 351, 1413–1420.
Deakin, J. F. W. (1994). Neuropsychological implications of brain
changes in schizophrenia: an overview. Psychopathology 27,
251–254.
Decety, J., Perani, D., Jeannerod, M., Bettinardi, V., Tadary, B.,
Woods, R., Mazziotta, J. C. & Fazio, F. (1994). Mapping motor
representations with PET. Nature 371, 600–602.
Demb, J. E., Desmond, J. E., Wagner, A. D., Vaidya, C. J., Glover,
G. H. & Gabrieli, J. D. E. (1995). Semantic encoding and retrieval
in the left inferior prefrontal cortex : a functional MRI study of
task difficulty and process specificity. Journal of Neuroscience 15,
5870–5878.
Demonet, J. F., Chollet, F., Ramsay, S., Cardebat, D., Nespoulous,
J. L., Wise, R., Rascol, A. & Frackowiak, R. (1992). The anatomy
of phonological and semantic processing in normal subjects. Brain
115, 1753–1168.
Devinsky, O., Morrell, M. J. & Vogt, B. A. (1995). Contributions of
anterior cingulate cortex to behaviour. Brain 118, 279–306.
Dias, R., Robbins, T. W. & Roberts, A. C. (1996). Dissociation in
prefrontal cortex of affective and attentional shifts. Nature 380,
69–72.
Dolan, R. J., Fletcher, P., Frith, C. D., Friston, K. J., Frackowiak,
R. S. J. & Grasby, P. M. (1995). Dopaminergic modulation of
impaired cognitive activation in the anterior cingulate cortex in
schizophrenia. Nature 378, 180–182.
Doody, G. A., Gotz, M., Johnstone, E. C., Frith, C. D. & Cunning-
ham Owens, D. G. (1998). Theory of mind and psychoses.
Psychological Medicine 28, 397–405.
Dougherty, D. D., Shin, L. M., Alpert, N. M., Pitman, R. K., Orr,
S. P., Lasko, M., Macklin, M. L., Fischman, A. J. & Rauch, S. L.
(1999). Anger in healthy men : a PET study using script-driven
imagery. Biological Psychiatry 46, 466–472.
Dudley, R. E. J., John, C. H., Young, A. W. & Over, D. E. (1997).
Normal and abnormal reasoning in people with delusions. British
Journal of Clinical Psychology 36, 243–258.
Ebmeier, K. P., Blackwood, D. H. R., Murray, C., Souza, V., Walker,
M., Dougall, N., Moffoot, A. P. R., O’Carroll, R. E. & Goodwin,
G. M. (1993). Single photon emission computed tomography with
**Tc-Exametazime in unmedicated schizophrenic patients. Bio-
logical Psychiatry 33, 487–495.
Elliott, R., McKenna, P. J., Robbins, T. W. & Sahakian, B. I. (1998).
Specific neuropsychological deficits in schizophrenic patients with
preserved intellectual function. Cognitive Neuropsychiatry 3, 45–70.
Fear, C. F. & Healy, D. (1997). Probabilistic reasoning in obsessive-
compulsive and delusional disorders. Psychological Medicine 27,
199–208.
Fear, C. F., Sharp, H. & Healy, D. (1996). Cognitive processes in
delusional disorder. British Journal of Psychiatry 168, 61–67.
Fletcher, P. C., McKenna, P. J., Frith, C. D., Grasby, P. M., Friston,
K. J. & Dolan, R. J. (1998). Brain activations in schizophrenia
during a graded memory task studied with functional neuro-
imaging. Archives of General Psychiatry 55, 1001–1008.
Frith, C. D., Friston, K. J., Liddle, P. F. & Frackowiak, R. S. J.
(1992). PET imaging and cognition in schizophrenia. Journal of the
Royal Society of Medicine 85, 222–224.
Frith, C. D., Friston, K. J., Herold, S., Silbersweig, D., Fletcher, P.,
Cahill, C., Dolan, R. J., Frackowiak, R. S. J. & Liddle, P. F.
(1995). Regional brain activity in chronic schizophrenic patients
during performance of a verbal fluency task. British Journal of
Psychiatry 167, 343–349.
Frith, C. & Corcoran, R. (1996). Exploring ‘ Theory of Mind’ in
people with schizophrenia. Psychological Medicine 26, 521–530.
Garety, P. A., Hemsley, D. R. & Wessely, S. (1991). Reasoning in
deluded schizophrenic and paranoid patients. Journal of Nervous
and Mental Disease 179, 194–201.
Goldberg, T. E., Weinberger, D. R., Berman, K. F., Pliskin, N. H. &
Podd, M. H. (1987). Further evidence for dementia of the
prefrontal type in schizophrenia? A controlled study of teaching
the Wisconsin card sorting test. Archives of General Psychiatry 44,
1008–1014.
Goldberg, T .E., St-Cyr, J. A. & Weinberger, D. R. (1990). Assess-
ment of procedural learning and problem solving in schizophrenic
patients by Tower of Hanoi type tasks. Journal of Neuropsychiatry
and Clinical Neuroscience 2, 165–173.
Goldman-Rakic, P. S. (1988). Topography of cognition: parallel
distributed networks in primate association cortex. Annual Review
of Neuroscience 11, 137–156.
Goldstein, J. M., Goodman, J. M., Seidman, L. J., Kennedy, D. N.,
Makris, N., Lee, H., Tourville, J., Caviness, V. S., Faraone, S. V.
882 N. J. Blackwood and others
& Tsuang, M. T. (1999). Cortical abnormalities in schizophrenia
identified by structural magnetic resonance imaging. Archives of
General Psychiatry 56, 537–547.
Grafton, S. T., Arbib, M. A., Fadiga, L. & Rizzolatti, G. (1996).
Localisation of grasp representations in humans by positron
emission tomography. 2. Observation compared with imagination.
Experimental Brain Research 112, 103–111.
Huq, S. F., Garety, P. A. & Hemsley, D. R. (1988). Probabilistic
judgements in deluded and non-deluded subjects. Quarterly Journal
of Experimental Psychology:Human Learning and Memory 40A,
801–812.
Jaspers, K. (1912\1963). General Psychopathology. Translated by J.
Hoening and M. W. Hamilton. Manchester University Press :
Manchester.
John, C. H. & Dodgson, G. (1994). Inductive reasoning in delusional
thinking. Journal of Mental Health 3, 31–49.
Jonides, J., Smith, E. E., Marshuetz, C., Koeppe, R. A. & Reuter-
Lorenz, P. A. (1998). Inhibition in verbal working memory
revealed by brain activation. Proceedings of the National Academy
of Sciences,USA 95, 8410–8413.
Kaney, S. & Bentall, R. P. (1989). Persecutory delusions and
attributional style. British Journal of Medical Psychology 62,
191–198.
Kaney, S., Wolfenden, M., Dewey, M. E. & Bentall, R. P. (1992).
Persecutory delusions and the recall of threatening and non-
threatening propositions. British Journal of Clinical Psychology 31,
85–87.
Kaplan, R. D., Szechtam, H., Franco, S., Szechtman, B., Nahmias,
C., Garnett, E. S., List, S. & Cleghorn, J. M. (1993). 3 clinical
syndromes of schizophrenia in untreated subjects: relation to brain
glucose activity measured by PET. Schizophrenia Research 11,
47–54.
Kapur, S., Craik, F. I. M., Tulving, E., Wilson, A. A., Houle, S. &
Brown, G. M. (1994). Neuroanatomical effects of encoding in
episodic memory: levels of processing effect. Proceedings of the
National Academy of Sciences USA 91, 2008–2011.
Kemp, R., Chua, S., McKenna, P. & David, A. S. (1996). Reasoning
and delusions: an empirical study. Psychological Medicine 26,
355–362.
Kendler, K. S., Glazer, W. & Morgenstern, H. (1983). Dimensions
of delusional experience. American Journal of Psychiatry 140,
466–469.
Kinderman, P. & Bentall, R. P. (1996). The development of a novel
measure of causal attributions : The Internal Personal and
Situational Attributions Questionnaire. Personality and Individual
Differences 20, 261–264.
Kinderman, P. & Bentall, R. P. (1997). Causal attributions in
paranoia and depression: internal, personal and situational
attributions for negative events. Journal of Abnormal Psychology
106, 103–107.
Kinderman, P., Dunbar, R. I. M. & Bentall, R. P. (1998). Theory of
mind deficits and causal attributions. British Journal of Psychology
89, 191–204.
Kwong, K. K., Belliveau, J. W., Chesler, D. A., Goldberg, I. E.,
Weisskoff, R. M., Poncelet, B. P., Kennedy, D. N., Hoppel, B. E.,
Cohen, M. S. & Turner, R. (1992). Dynamic magnetic resonance
imaging of human brain activity during primary sensory stimu-
lation. Proceedings of the National Academy of Sciences,USA 89,
5675–5679.
Langdon, R., Michie, P. T., Ward, P. B., McConaghy, N., Catts,
S. V. & Coltheart, M. (1997). Defective self and\or other mental-
ising in schizophrenia: a cognitive neuropsychological approach.
Cognitive Neuropsychiatry 2, 167–193.
Lawrie, S. M. & Abukmeil, S. S. (1998). Brain abnormality in
schizophrenia. A systematic and quantitative review of volumetric
magnetic resonance imaging studies. British Journal of Psychiatry
172, 110–120.
Leafhead, K. M., Young, A. W. & Szulecka, T. K. (1996). Delusions
demand attention. Cognitive Neuropsychiatry 1, 5–16.
Leonardo, M., Feldman, J., Sadato, N., Campbell, G., Ibanez, V.,
Cohen, L., Deiber, M-P., Jezzard, P., Pons, T., Turner, R.,
LeBihan, D. & Hallett, M. (1995). A functional magnetic resonance
imaging study of cortical regions associated with motor task
execution and motor ideation in humans. Human Brain Mapping 3,
83–92.
Liddle, P. F. (1987). Schizophrenic symptoms : cognitive perform-
ance and neurological dysfunction. Psychological Medicine 17,
49–57.
Liddle, P. F., Friston, K. J., Frith, C. D., Hirsch, S. R., Jones, T. &
Frackowiak, R. S. J. (1992). Patterns of cerebral blood flow in
schizophrenia. British Journal of Psychiatry 160, 179–186.
Lyon, H. M., Kaney, S. & Bentall, R. P. (1994). The defensive
function of persecutory delusions: evidence from attribution tasks.
British Journal of Psychiatry 164, 637–646.
McGuire, P. K., Silbersweig, D. A., Wright, I., Murray, R. M.,
David, A. S., Frackowiak, R. S. J. & Frith, C. D. (1995). Ab-
normal monitoring of inner speech: a physiological basis for
auditory hallucinations. Lancet 346, 596–600.
McGuire, P. K., Silbersweig, D. A., Wright, I., Murray, R. M.,
Frackowiak, R. S. J. & Frith, C. D. (1996). The neural correlates
of inner speech and auditory verbal imagery in schizophrenia :
relationship to auditory verbal hallucinations. British Journal of
Psychiatry 169, 148–159.
McKenna, P. J., Tamlyn, D., Lund, C. E., Mortimer, A. M.,
Hammond, S. & Baddeley, A. D. (1990). Amnesic syndrome in
schizophrenia. Psychological Medicine 20, 967–972.
McKenna, P. J. (1997). The psychology and neuropsychology of
schizophrenia. In Schizophrenia and Related Syndromes. (ed. P. J.
McKenna), pp. 171–183. Psychology Press : Hove.
Maher, B. A. (1988). Anomalous experience and delusional thinking :
the logic of explanations. In Delusional Beliefs (ed. T. F. Oltmanns
and B. A. Maher), pp. 15–33. Wiley: New York.
Martin, A., Haxby, J. V., Lalonde, F. M., Wiggs, C. L. & Unger-
leider, L. G. (1995). Discrete cortical regions associated with
knowledge of color and knowledge of action. Science 270, 102–105.
Martin, A., Wiggs, C. L., Ungerleider, L. G. & Haxby, J. V. (1996).
Neural correlates of category specific knowledge. Nature 379,
649–652.
Mortimer, A. M., Bentham, P., McKay, A. P., Quemada, I., Clare,
L., Eastwood, N. & McKenna, P. J. (1996). Delusions in schizo-
phrenia: a phenomenological and psychological explanation.
Cognitive Neuropsychiatry 1, 289–303.
Pardo, J. V., Pardo, P. J. & Raichle, M. E. (1993). Neural correlates
of self induced dysphoria. American Journal of Psychiatry 150,
713–719.
Peters, E., Day, S., Linney, Y., Medford, S. & Sharpley, M. (1998).
The correlates of delusional thinking : preliminary findings using
the PDI in the normal population. Schizophrenia Research 29, 39.
Pugh, K. R., Shaywitz, B. A., Shaywitz, S. E., Constable, R. T.,
Skudlarski, P., Fulbright, R. K., Bronen, R. A., Shankweiler,
D. P., Katz, L., Fletcher, J. M. & Gore, J. C. (1996). Cerebral
organisation of component processes in reading. Brain 119,
1221–1238.
Rolls, E. T. (1999). The functions of the orbitofrontal cortex.
Neurocase 5, 305–316.
Sabri, O., Erkwoh, R., Schreckenberger, M., Owega, A., Sass, H &
Buell, U. (1997). Correlation of positive symptoms exclusively to
hyperperfusion or hypoperfusion of cerebral cortex in never-
treated schizophrenics. Lancet 349, 1735–1739.
Sarfati, Y., Hardy-Bayle, M-C., Nadel, J., Chevalier, J-F. &
Widlocher, D. (1997). Attribution of mental states to others by
schizophrenic patients. Cognitive Neuropsychiatry 2, 1–17.
Saykin, A. J., Shatasel, D. L. & Gur, R. E. (1994). Neuro-
psychological deficits in neuroleptic naieve patients with first
episode schizophrenia. Archives of General Psychiatry 51, 124–131.
Shallice, T., Burgess, P. W. & Frith, C. D. (1991). Can the
neuropsychological case-study approach be applied to schizo-
phrenia? Psychological Medicine 21, 667–673.
Sharp, H. M., Fear, C. F. & Healy, D. (1997). Attributional style
and delusions: an investigation based on delusional content.
European Psychiatry 12, 1–7.
Imaging attentional and attributional bias 883
Silbersweig, D. A., Stern, E., Frith, C., Cahill, C., Holmes, A.,
Grootoonk, S., Seaward, J., McKenna, P., Chua, S. E., Schnorr,
L., Jones, T. & Frackowiak, R. S. J. (1995). A functional neuro-
anatomy of hallucinations in schizophrenia. Nature 378, 176–179.
Simpson, J., Done, J. & Vallee-Tourangeau, F. (1998). An un-
reasoned approach: a critique of research on reasoning and
delusions. Cognitive Neuropsychiatry 3, 1–20.
Smith, E. E. & Jonides, J. (1999). Storage and executive processes in
the frontal lobes. Science 283, 1657–1661.
Spence, S. A., Brooks, D. J., Hirsch, S. R., Liddle, P. F., Meehan, J.
& Grasby, P. M. (1997). A PET study of voluntary movement in
schizophrenic patients experiencing passivity phenomena (delu-
sions of alien control). Brain 120, 1997–2011.
Spence, S. A., Hirsch, S. R., Brooks, D. J. & Grasby, P. M. (1998).
Prefrontal cortex activity in people with schizophrenia and control
subjects. British Journal of Psychiatry 172, 316–323.
Spitzer, M. (1990). On defining delusions. Comprehensive Psychiatry
31, 377–397.
Stevens, A. A., Goldman-Rakic, P. S., Gore, J. C., Fulbright, R.K.
& Wexler, B. E. (1998). Cortical dysfunction in schizophrenia
during auditory word and tone working memory demonstrated by
functional magnetic resonance imaging. Archives of General
Psychiatry 55, 1097–1103.
Symons, C. S. & Johnson, B. T. (1997). The self-reference effect in
memory: a meta-analysis. Psychological Bulletin 121, 371–394.
Taylor, S. F., Kornblum, S., Lauber, E. J., Minoshima, S. & Koeppe,
R. A. (1997). Isolation of specific interference processing in the
Stroop task: PET activation studies. Neuroimage 6, 81–92.
Thompson, P. A. & Meltzer, H. (1993). Positive, negative and
disorganisation factors from the schedule for affective disorders
and schizophrenia and the present state examination : a three
factor solution. British Journal of Psychiatry 163, 344–351.
Thompson-Schill, S. L., D’Esposito, M., Aguirre, G. K. & Farah,
M. J. (1997). Role of left inferior prefrontal cortex in retrieval of
semantic knowledge: a re-evaluation. Proceedings of the National
Academy of Sciences,USA 94, 14792–14797.
Tulving, E. (1983). Elements of Episodic Memory. Blackwell : Oxford.
Tulving, E. (1993). Varieties of consciousness and levels of awareness
in memory. In Attention : Selection, Awareness and Control. A
Tribute to Donald Broadbent (ed. A. Baddeley and L. Weiskrantz),
pp. 283–289. Oxford University Press: London.
Ullmann, L. P. & Krasner, L. (1969). A Psychological Approach to
Abnormal Behaviour. Prentice-Hall: Englewood Cliffs.
Verdoux, H., Maurice-Tison, S., Gay, B., van Os, J., Salamon, R. &
Bourgeois, M. (1998). A survey of delusional ideation in primary
care patients. Psychological Medicine 28, 127–134.
Wagner, A. D., Schacter, D. L., Rotte, M., Koutstaal, W., Maril, A.,
Dale, A. M., Rosen, B. R. & Buckner, R. L. (1998). Building
memories: remembering and forgetting of verbal experiences as
predicted by brain activity. Science 281, 1188–1191.
Weinrich, M. & Wise, S. P. (1982). The premotor cortex of the
monkey. Journal of Neuroscience 2, 1329–1345.
White, N. M. (1997). Mnemonic functions of the basal ganglia.
Current Opinion in Neurobiology 7, 164–169.
Winters, K. C. & Neale, J. M. (1983). Delusions and delusional
thinking in psychotics: a review of the literature. Clinical
Psychology Review 3, 227–253.
Young, H. F. & Bentall, R. P. (1997). Probabilistic reasoning in
deluded, depressed and normal subjects. Psychological Medicine
27, 455–465.
