Neural Correlates of Anxiety Associated with
Obsessive-Compulsive Symptom Dimensions in Normal
Volunteers
David Mataix-Cols, Sarah Cullen, Kezia Lange, Fernando Zelaya,
Christopher Andrew, Edson Amaro, Michael J. Brammer, Steven C.R. Williams,
Anne Speckens, and Mary L. Phillips
Background: The neural correlates of anxiety associated
with obsessive-compulsive symptomlike provocation in
normal volunteers are unknown.
Methods: Ten healthy volunteers participated in four
functional magnetic resonance experiments. Subjects were
scanned while viewing alternating blocks of emotional
(normally aversive, washing-relevant, checking-relevant,
or hoarding-relevant pictures) and neutral pictures, and
imagining scenarios related to the content of each picture
type. Nonparametric brain mapping analyses were used.
Results: In response to the provocative pictures in all
experiments, increases in subjective anxiety and activation
in bilateral ventral prefrontal, limbic, dorsal prefrontal,
and visual regions were demonstrated. Anxiety related to
different symptom dimensions was associated with differ-
ent patterns of activation: provocation of washing-rele-
vant anxiety predominantly activated dorsal and ventral
prefrontal regions; checking-relevant anxiety predomi-
nantly activated dorsal prefrontal regions; and hoarding-
relevant anxiety predominantly activated ventral prefron-
tal regions and the left amygdala.
Conclusions: Our findings support a dimensional model
of obsessive-compulsive disorder (OCD) whereby 1) the
brain systems implicated in the mediation of anxiety in
response to symptom-related material in normal subjects
are similar to those identified in OCD patients during
symptom provocation, and 2) anxiety associated with differ-
ent symptom dimensions is associated with differential pat-
terns of activation of these neural systems. Further investi-
gation of the neural basis of OCD symptom dimensions is
required. Biol Psychiatry 2003;53:482– 493 © 2003 Soci-
ety of Biological Psychiatry
Key Words: Obsessive-compulsive disorder, symptom
dimensions, hoarding, neuroimaging, fMRI, emotion
Introduction
F
unctional neuroimaging studies have substantially in-
creased our understanding of the neural mechanisms
underlying obsessive-compulsive disorder (OCD). Symptom
provocation paradigms have used positron emission tomog-
raphy (PET), single photon emission tomography (SPECT),
or functional resonance imaging (fMRI) to compare, in a
single session, the patterns of brain activation during OCD
symptom provocation and control states (Saxena and Rauch
2000). Although findings are discrepant, they strongly
associate OCD symptoms with activation of the orbito-
frontal cortex, with less consistent involvement of lateral
frontal cortex, anterior cingulate gyrus, temporal cortex,
striatum, thalamus, amygdala, and insular cortex (Adler et
al 2000; Breiter et al 1996; McGuire et al 1994; Rauch et
al 1994; Saxena and Rauch 2000).
Obsessive-compulsive disorder is heterogeneous, with
symptoms that can be summarized in a few consistent,
temporally stable, dimensions (Baer 1994; Leckman et al
1997; Mataix-Cols et al 1999a, 2002a; Summerfeldt et al
1999). Despite this phenotypic heterogeneity, most previ-
ous neuroimaging studies of OCD have grouped together
patients with diverse symptom patterns, although they
have included patients with predominantly contamination/
washing or mixed symptoms. To our knowledge, only
three functional neuroimaging studies have examined the
neural correlates of different symptoms in OCD. In one
PET study (Cottraux et al 1996), all patients were predom-
inantly checkers, and symptoms were provoked using an
individually tailored script-driven paradigm that prompted
the urge to check. They found significant increases in
orbitofrontal and superior temporal cortex activity, and-
,contrary to most previous findings, lower activity in the
basal ganglia compared with control subjects. In another
PET study, Rauch et al (1998) found significant correla-
From the Division of Psychological Medicine (DM-C, SC, KL, MLP), Departments
of Neuroimaging Research (FZ, CA, EA, SCRW), Biostatistics (MJB), and
Psychology (AS), GKT School of Medicine and Institute of Psychiatry,
London, United Kingdom.
Address reprint requests to David Mataix-Cols, Ph.D., Department of Psychological
Medicine, GKT School of Medicine and Institute of Psychiatry, 5th Floor
Thomas Guy House, Guy’s Hospital, London SE1 9RT United Kingdom.
Received March 26, 2002; revised June 12, 2002; accepted June 21, 2002.
© 2003 Society of Biological Psychiatry 0006-3223/03/$30.00
doi:10/1016/S0006-3223(03)01504-4