Institute of Psychiatry, London, UK
Correspondence: Dr S. S. Shergill, Division of Psychological Medicine, Institute of Psychiatry, De Crespigny Park, Denmark Hill, London SE5 8AF, UK. Tel: 020 7848 0350; fax: 020 7848 0350; e-mail: s.shergill{at}iop.kcl.ac.uk
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ABSTRACT |
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Aims To investigate whether the same pattern of functional abnormalities would be evident as the rate of inner speech production was varied.
Method Eight people with schizophrenia who had a history of prominent auditory hallucinations and eight control participants were studied using functional magnetic resonance imaging while the rate of inner speech generation was varied experimentally.
Results When the rate of inner speech generation was increased, the participants with schizophrenia showed a relatively attenuated response in the right temporal, parietal, parahippocampal and cerebellar cortex.
Conclusions In people with schizophrenia who are prone to auditory hallucinations, increasing the demands on the processing of inner speech is associated with attenuated engagement of the brain areas implicated in verbal self-monitoring.
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INTRODUCTION |
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Self-monitoring
Self-monitoring is fundamental to normal cognitive function, in planning,
controlling and anticipating the consequences of complex motor acts. A
feed-forward model has been proposed to explain this mechanism
(Wolpert et al,
1995); in this model the motor outflow of a motor act (plan)
generates an efferent copy that is transmitted to (sensory) brain regions
relevant to this act and serves to anticipate its sensory effects. The
anticipated sensory consequences are then subtracted from the actual sensory
feedback, which has the consequence of cancelling out the sensory effects of
the motor act, thereby leaving sensory information about changes in the
outside world. An everyday example is that during self-generated eye movements
the world is experienced as stable, despite the succession of images passing
the retina. However, when the eye is moved passively by tapping the eyeball,
and therefore there is no cancellation of the sensory effects of the motor
act, it is the visual world that seems to move. This simple cancellation
theory has been superseded by the concept of feed-forward control, whereby the
motor commands themselves are monitored, prior to any actual movement
(Deeke et al, 1969; Erdler et al, 2000).
Further examples of differences in brain activation patterns between identical
externally generated and self-generated actions have been reported in the
auditory and tactile modalities. The auditory cortices are activated in
response to vowel changes in heard speech, but not when the same vowel changes
are self-uttered (Curio et al,
2000). This suggests that motor-to-sensory priming of the auditory
cortex dampens the response to self-produced expected sounds and
occurs on a millisecond timescale.
Self-monitoring of speech
Electrophysiological recordings in both non-human
(Müller-Preuss & Ploog,
1981) and human (Creutzfeldt
et al, 1989) primates indicate that neuronal activity in
the temporal cortex is powerfully modulated by vocalisation. This modulation
can precede articulation by hundreds of milliseconds, suggesting that it is
related to the intention to speak (rather than articulation per se)
and mediated by the direct anatomical connections linking areas that generate
and perceive speech, within the left inferior frontal and bilateral temporal
cortices respectively. Contemporary cognitive models propose that auditory
verbal hallucinations are derived from inner speech that the person has
misidentified as alien through defective self-monitoring
(Frith & Done, 1988). This
suggests that the functional neuroanatomy of monitoring inner speech might be
abnormal in people who are prone to auditory verbal hallucinations.
Functional neuroimaging studies of verbal generation in normal individuals indicate that this process is associated with activation in the left prefrontal cortex and deactivation in the temporal cortex bilaterally (Frith et al, 1995). These findings suggest that output from regions involved in verbal generation might modulate activation in areas involved in speech perception. Initial studies of verbal fluency in schizophrenia indicated that this temporal deactivation was absent (Frith et al, 1995), leading to the proposal that schizophrenia involves a functional frontotemporal disconnectivity. However, more recent studies of verbal fluency in schizophrenia have failed to replicate this finding (Spence et al, 2000).
Auditory verbal imagery imagining another person's speech implicitly involves both the generation and monitoring of inner speech, and in healthy volunteers is associated with activation in the left inferior frontal cortex, and the temporal, parahippocampal and cerebellar cortex (Shergill et al, 2001). A positron emission tomography (PET) study of auditory verbal imagery in participants with schizophrenia who were prone to auditory hallucinations revealed normal activation of the left inferior frontal gyrus, but differential activation of the left temporal cortex, compared with both people with schizophrenia but no history of hallucinations and healthy volunteers (McGuire et al, 1996). A more recent functional magnetic resonance imaging (fMRI) study using a similar paradigm in another group of hallucination-prone participants again demonstrated normal activation of the left inferior frontal gyrus and attenuated activation of the right temporal cortex (Shergill et al, 2000b). In addition, there was relatively attenuated activation in the parahippocampal and posterior cerebellar cortex bilaterally. However, while imagining speech engages verbal self-monitoring, activation associated with this process could also be related to the phonological and semantic demands of reproducing a representation of another person's voice (McGuire et al, 1996; Shergill et al, 2000b). In this study we examined a task that engaged the process of inner speech but did not involve these potentially confounding components.
We used fMRI to study people while they were covertly generating the same word (rest) at different rates. Increasing the rate of covert articulation was designed to increase the demands on the generation and monitoring of inner speech. We compared a group of people with schizophrenia, who were in remission but had a history of prominent auditory hallucinations, with a matched group of healthy volunteers. On the basis of our previous studies of auditory verbal imagery (McGuire et al, 1996; Shergill et al, 2000b) we predicted that:
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METHOD |
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The patients' clinical profile and history at interview were confirmed by liaison with the responsible clinical team and assessment of medical records. All except one person (who was not receiving treatment) had been receiving antipsychotic medication (five were treated with atypical and two with typical antipsychotic drugs) at stable dosages for 4 months or more prior to scanning. Before inclusion, potential participants were assessed on their ability to repeat a word overtly at the two rates (once every 1 s or 4 s) to be used during scanning. They proceeded to scanning when they consistently achieved a 1:4 ratio in the number of repetitions timed over a minute. After a complete description of the study to the participants, their written informed consent to participation was obtained. The study was approved by the Maudsley Hospital ethics committee.
Tasks performed during imaging
Fast v. slow covert articulation (categorical
comparison)
Participants covertly generated the word rest repeatedly at
two self-paced rates (once every 1 s or 4 s; i.e. 60 words/min or 15
words/min), without speaking. During scanning, the two conditions alternated
in an ABAB design, with each condition lasting 30 s, and five cycles of each
condition in a 300 s run. The order of conditions was counterbalanced across
the group. The desired rate during each condition was indicated by a number
visible throughout in the centre of a computer screen (1 for one
word every second and 4 for one word every 4 s). The ability of
participants to generate output at the required rates was demonstrated by
asking them to tap their finger at the two different rates both before and
immediately after scanning. In order to reduce potentially confounding effects
of poor performance on activation, only data from participants who achieved a
consistent timing ratio (on finger-tapping) of 1:4 between the fast and slow
rate, immediately before and after scanning, were analysed.
Image acquisition
Gradient-echo echoplanar magnetic resonance images were acquired using a
1.5 T imaging system fitted with Advanced NMR hardware and software (ANMR,
Woburn, MA, USA) at the Maudsley Hospital, London. A quadrature birdcage head
coil was used for radiofrequency transmission and reception. In each of 14
non-contiguous planes parallel to the intercommissural
(anteriorposterior) plane, 100 T2*-weighted images depicting
blood oxygen level dependent (BOLD) contrast
(Ogawa et al, 1990)
were acquired with echo time 40 ms, repetition time 3000 ms, in-plane
resolution 3.1 mm, slice thickness 7 mm, slice skip 0.7 mm. At the same
session a 43-slice, high-resolution inversion recovery echoplanar image of the
whole brain was acquired in the intercommissural plane (repetition time 16 000
ms, in-plane resolution 1.5 mm, slice thickness 3 mm).
Image analysis
Image analysis was performed using Statistical Parametric Mapping version
SPM99 (Wellcome Department of Cognitive Neurology,
http://www.fil.ion.ucl.ac.uk/spm/).
All data-sets were automatically realigned to the first image to correct for
head movement, normalised using sinc interpolation and transformed into
Talairach space. The transformed data-set for each participant was smoothed
with a Gaussian filter (full width half maximum, 8 mm) to compensate for
normal variations in anatomy. The time series were high-pass (126 s) filtered
to remove low-frequency artefacts.
Fast v. slow covert articulation
Statistical analysis was performed separately for each individual, and the
stereotaxically normalised fMRI time series data from all the participants
were pooled for group analysis. Analysis of the task used a categorical design
revealing activation during the fast relative to the slow rate of generation,
and vice versa. Cluster-level statistics corrected for multiple comparisons
were thresholded at P<0.05.
Functional connectivity of the left inferior frontal gyrus
An analysis of the functional connectivity of the left inferior frontal
cortex was also performed. The time series data from the voxel in the left
inferior frontal gyrus showing the maximally significant response, in the fast
v. slow covert articulation, was selected as the covariate of
interest in each individual. The left inferior frontal gyrus was chosen
because it is the main region implicated in the generation of inner speech
(McGuire et al, 1996; Shergill et al,
2000b,
2001). We thus sought to
identify brain regions whose activity was temporally correlated with activity
in the inferior frontal gyrus, and to compare these between groups. The
statistical parametric maps (SPMs) from this exploratory analysis were
thresholded at P<0.05, with voxel-level statistics corrected for
multiple comparisons.
Between-group analyses
Between-group comparisons assessed the significance of differences in the
magnitude of each of the above analyses comparing the patient and control
groups, using a random effects model. The random effects analysis takes
contrasts from a first-level analysis to a second-level SPM analysis, the
condition-specific effects (from all participants) are summarised with a
contrast and a two-sample t test is applied to the ensuing
individual-specific contrasts at the second level. This analysis treats
variations in activation from person to person as a random effect. The SPMs
were thresholded at P<0.05 with cluster-level statistics corrected
for multiple comparisons; we also reported cluster-level statistics
uncorrected for multiple comparisons in regions included in our a
priori hypotheses.
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RESULTS |
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Imaging data: control group
Fast v. slow covert articulation
The data for the control group have been described in detail elsewhere
(Shergill et al,
2002). In brief, relative to covert generation at 15 words/min,
covert generation at 60 words/min was associated with activation in foci in
the dorsolateral and orbital portions of the left inferior frontal gyrus, and
in the anterior part of the left superior temporal gyrus. There was also a
large area of activation centred on the right precentral gyrus, which included
foci in the adjacent postcentral and superior temporal gyri, and a separate
bilateral activation in the frontal pole. Activation was also present in the
right parahippocampal gyrus and bilateral cerebellar cortices, significant
only at the uncorrected level. The slower rate of generation was associated
with activation in the supplementary motor area, the left precentral gyrus and
the right inferior parietal lobule.
Functional connectivity of the left inferior frontal gyrus
Activity in the left inferior frontal gyrus was positively correlated with
activity in the left middle and superior temporal gyri, inferior parietal
lobule, and claustrum. Right-sided correlations were evident in the homologous
portion of the inferior frontal gyrus, the precentral and postcentral gyri,
and the middle/superior temporal and anterior cingulate gyri. Activity in the
left inferior frontal gyrus was negatively correlated with activity in the
left cerebellar cortex and the right thalamus.
Imaging data: patient group
Fast v. slow covert articulation
As in the control group, the faster rate was associated with activation in
the dorsolateral and orbital portion of the left inferior frontal gyrus, and
in the anterior part of the left superior temporal gyrus. Additional
activation was evident in bilateral thalami, the right middle frontal gyrus
and the supplementary motor area. The slower rate of generation was associated
with activation in the parahippocampal gyri bilaterally and in the left
posterolateral cerebellum and left inferior occipital gyrus
(Table 1).
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Functional connectivity of the left inferior frontal gyrus
Activity in the left inferior frontal gyrus was positively correlated with
activity in the left superior temporal gyrus and the right dorsolateral
prefrontal, middle temporal and posterolateral cerebellar cortices. Activity
in the left inferior frontal gyrus was negatively correlated with activity in
the retrosplenial cingulate and right lingual gyri
(Table 2).
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Between-group differences in activation
Fast v. slow covert articulation
Compared with the control group, the participants with schizophrenia showed
reduced activation in a large right-sided region with distinct foci in the
superior temporal and postcentral gyri, and the inferior parietal lobule.
Attenuated activation was also evident in the right parahippocampal gyrus and
in the posterolateral cerebellar cortex
(Table 3;
Fig. 1). Relatively increased
activation occurred only in the left lenticular nucleus.
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Functional connectivity of the left inferior frontal gyrus
Relative to the control group; in the patient group there was a reduced
correlation with left inferior frontal activity in the right middle and
superior temporal gyri, the right insula, a region encompassing the right
parahippocampal, inferior temporal and fusiform gyri, and in the precentral
gyrus and the medial parietal lobe. This group did not show greater
correlations in any area (Table
4).
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DISCUSSION |
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Generation of inner speech
As predicted, increasing the rate of covert articulation was associated
with activation in the left inferior frontal cortex. This was evident in all
the participants, suggesting that the silent generation of inner speech is not
impaired in people with a history of hallucinations; this is supported by
findings from previous neuroimaging and cognitive psychology studies
(Frith et al, 1995;
McGuire et al, 1996;
Shergill et al,
2000b). The consistent presence of significant left
inferior frontal activation allowed us to generate a functional connectivity
map for this region in each individual.
Verbal self-monitoring
The anticipated activation of the lateral temporal cortex in association
with the faster rate of generation was evident in the healthy participants.
Those in the patient group showed a significant attenuation of activation in
the right (but not the left) superior temporal gyrus, the right
parahippocampal gyrus and the right cerebellar cortex. These data are
consistent with a modulatory effect of left inferior frontal activity on
activity in the temporal and cerebellar cortex in healthy individuals, and an
attenuation of these modulatory effects in people with schizophrenia who are
prone to auditory hallucinations. The interpretation is more complex in the
case of the parahippocampal activation, which might have reflected
deactivation (i.e. greater activation at the slower rate) during
the faster rate of covert articulation in the patients. However, in a previous
fMRI study of auditory verbal imagery, we found similar differences between
hallucination-prone patients and controls in these same three regions
(Shergill et al,
2000b). In that study, these differences could have been
related to the demands on semantic and phonological processing associated with
imagining alien speech, but as the present study simply involved covert
articulation of a single word, this explanation is unlikely.
The involvement of the right as opposed to the left temporal cortex is of interest, as the right temporal cortex has also been a site of differential activation in studies of verbal fluency in schizophrenia (Spence et al, 2000), and this region appears to be more active than its left homologue when people are experiencing auditory hallucinations (Shergill et al, 2000). Although previous functional imaging studies have demonstrated involvement of the right temporal cortex in processing prosody (George et al, 1996) and inference of what is being said, as well as an emotional response to its content (Canli et al, 1998), this study suggests a more fundamental role in monitoring language production than previously thought and this may be reflected in the bilateral activation of the superior temporal gyri during the faster rate of covert articulation in healthy individuals.
A common feature of lateral temporal, parahippocampal and cerebellar cortex is that these regions are all implicated in cognitive self-monitoring (Frith & Done, 1988; Gray et al, 1991; Blakemore et al, 1998). Lesion and neuroimaging studies suggest that the cerebellum acts as a comparator in both motor and verbal tasks, comparing intended with actual performance and modulating cerebral cortical activity appropriately (Blakemore et al, 1998). The hippocampus has also been proposed as the comparator in experimental models of cognitive self-monitoring (Gray et al, 1991), whereas the lateral temporal cortex has been more specifically implicated in the monitoring of inner speech (McGuire et al, 1996; Shergill et al, 2000b).
Functional connectivity of the left inferior frontal gyrus
The functional connectivity analyses generated maps of regions that showed
BOLD activity that was significantly correlated with that in the maximal focus
of activation within the left inferior frontal cortex, over the course of the
experiment. This was an exploratory analysis, which sought to provide a more
stringent temporal test of our hypotheses than the comparison of activity at
fast and slow rates of covert articulation. In those with schizophrenia,
activity in the left inferior frontal gyrus was positively correlated with
activity in the left superior temporal gyrus, the right middle temporal gyrus
and the right lateral cerebellum, providing further support for the
involvement of these structures in a self-monitoring network. A positive
modulation of temporal activity during verbal generation accords with data
from a PET study of whispering at different rates
(Paus et al, 1996),
and from electrophysiological studies
(Müller-Preuss & Ploog,
1981; Creutzfeldt et
al, 1989). However, when compared with the control group,
left inferior frontal activity was less strongly correlated with activity in
the right superior and middle temporal gyri, and the junction of the right
parahippocampal/fusiform gyri. The attenuation of correlation with activation
in the right temporal cortex is consistent with the results of the categorical
comparison discussed above, while the difference in the correlations with
activity in the parahippocampal/fusiform area was close (but lateral) to the
parahippocampal site of differences in activation.
Functional connectivity between cortical grey-matter regions is mediated by axonal projections within cerebral white matter, and diffusion tensor MRI (Basser et al, 1994) by measuring the diffusion characteristics of water molecules in tissuepermits evaluation of white-matter integrity and hence a more direct examination of brain connectivity. Some studies (Lim et al, 1999; Agartz et al, 2001), but not all (Steel et al, 2001), report reduced white-matter integrity in schizophrenia. However, as measurements were only possible in large white-matter regions or easily identified structures such as the corpus callosum, few studies have examined the frontal projections implicated in schizophrenia. However, a study examining the uncinate fasciculus (a major frontotemporal tract) found no direct difference between people with schizophrenia and a control group (Lawrie et al, 2002); however, the former failed to demonstrate the normal leftright (left greater than right) asymmetry evident in the healthy brains. This lends support to the lateralisation hypothesis proposed by Crow et al (1989) in which abnormal neural development of brain lateralisation is critical to the aetiology of schizophrenia. The attenuated activation within right-sided temporal and parietal structures evidenced by the people with schizophrenia in our study could be incorporated into this theory, which posits a disconnection between right-sided spatial or paradigmatic aspects of language and the linear (phonological) output restricted to the left hemisphere. The right-sided attenuation could be evidence of this disconnection, in the presence of normal left-sided language (function, which is suggested to be involved in the development of the nuclear symptoms of schizophrenia; the basis of which may lie in the difficulties that patients have with self v. other distinctions (Crow et al, 1989).
In summary, neuroimaging studies indicate that healthy people show activation in brain regions involved in speech generation (left inferior frontal cortex) and perception (temporal cortex) during the generation and monitoring of inner speech (Shergill et al, 2001, 2002). Verbal self-monitoring seems to be particularly associated with activation in the temporal cortex bilaterally, the right parahippocampal cortex and the right lateral cerebellum (Shergill et al, 2001). The perception of auditory hallucinations in people with schizophrenia is associated with activation in the same parts of frontal and temporal cortices that are normally engaged during the generation and perception of inner speech, in the absence of any right cerebellar or parahippocampal activation (Shergill et al, 2000a). Moreover, when generating inner speech, people whose schizophrenia is in remission but who are prone to hearing voices show relatively reduced activation in the temporal, right parahippocampal and right cerebellar cortex areas implicated in verbal self-monitoring (Shergill et al, 2000b). Our study suggests that this is present even with generation of simple verbal stimuli. Thus, self-monitoring appears dysfunctional even in people whose disease is in remission. However, it is still unclear whether this putative failure of self-monitoring in schizophrenia is specific to the verbal modality or is also apparent during the planning or execution of other sensorimotor acts.
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Clinical Implications and Limitations |
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LIMITATIONS
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ACKNOWLEDGMENTS |
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REFERENCES |
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---|
American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders (4th edn) (DSMIV). Washington, DC: APA.
Annett, M. A. (1970) A classification of hand preference by association analysis. British Journal of Psychology, 61, 303321.[Medline]
Basser, P. J., Mattiello, J. & Le Bihan, D. (1994) MR diffusion tensor spectroscopy and imaging. Biophysical Journal, 66, 259267.[Abstract]
Blakemore, S. J.,Wolpert, D. M. & Frith, C. D. (1998) Central cancellation of self-produced tickle sensation. Nature Neuroscience, 1, 635640.[CrossRef][Medline]
Canli, T., Desmond, J. E., Zhao, Z., et al (1998) Hemispheric asymmetry for emotional stimuli detected with fMRI. Neuroreport, 9, 32333239.[Medline]
Creutzfeldt, O., Ojemann, G. & Lettich, E. (1989) Neuronal activity in the human lateral temporal lobe. II. Responses to the subject's own voice. Experimental Brain Research, 77, 475489.
Crow,T. J., Ball, J., Bloom, S.R., Crow, T. J., Ball, J., Bloom, S. R., et al (1989) Schizophrenia as an anomaly of development of cerebral asymmetry. A postmortem study and a proposal concerning the genetic basis of the disease. Archives of General Psychiatry, 46, 11451150.[Abstract]
Curio, G., Neuloh, G., Numminen, J., et al (2000) Speaking modifies voice-evoked activity in the human voice-evoked auditory cortex. Human Brain Mapping, 9, 183191.[Medline]
Deeke, L., Scheid, P. & Kornhuber, H. H. (1969) Distribution of readiness potential, premotion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements. Experimental Brain Research, 7, 158168.[Medline]
Erdler, M., Beisteiner, R., Mayer, D., et al (2000) Supplementary motor area activation preceding voluntary movement is detectable with a whole-scalp magnetoencephalography system. Neuroimage, 11, 697707.[CrossRef][Medline]
Frith, C. D. & Done, D. J. (1988) Towards a neuropsychology of schizophrenia. British Journal of Psychiatry, 153, 437443.[Abstract]
Frith, C. D., Friston, K. J., Herold, S., et al (1995) Regional brain activity in chronic schizophrenic patients during the performance of a verbal fluency task. British Journal of Psychiatry, 167, 343349.[Abstract]
George, M. S., Parekh, P. I., Rosinsky, N., et al (1996) Understanding emotional prosody activates right hemisphere regions. Archives of Neurology, 53, 665670.[Abstract]
Gray, J. A., Feldon, J., Rawlins, J. N. P., et al (1991) The neuropsychology of schizophrenia. Behavioural and Brain Sciences, 14, 119.
Lawrie, S. M., Buechel, S., Whalley, H. C., et al (2002) Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biological Psychiatry, 51, 10081011.[CrossRef][Medline]
Lim, K. O., Hedehus, M., Moseley, M., et al
(1999) Compromised white matter tract integrity in
schizophrenia inferred from diffusion tensor imaging. Archives of
General Psychiatry, 56,
367374.
McGuire, P. K., Silbersweig, D. A., Wright, I., et al (1996) The neural correlates of inner speech and auditory verbal imagery in schizophrenia: relationship to auditory verbal hallucinations. British Journal of Psychiatry, 169, 148159.[Abstract]
Müller-Preuss, P. & Ploog, D. (1981) Inhibition of auditory cortical neurons during phonation. Brain Research, 215, 6176.[CrossRef][Medline]
Nelson, H. E. (1991) National Adult Reading Test. Windsor: NFERNelson.
Ogawa, S., Lee, T. M., Kay, A. R., A. R., et al (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proceedings of the National Academy of Sciences of the USA, 87, 98689872.[Abstract]
Paus, T., Perry, D. W., Zatorre, R. J., et al (1996) Modulation of cerebral blood flow in the human auditory cortex during speech: role of motor-to-sensory discharges. European Journal of Neurscience, 8, 22362246.
Shergill, S. S., Brammer, M. J., Williams, S., et al
(2000a) Mapping auditory hallucinations in schizophrenia
using functional magnetic resonance imaging. Archives of General
Psychiatry, 57,
10331038.
Shergill, S. S., Bullmore, E. T., Simmons, A., et al
(2000b) The functional anatomy of auditory verbal
imagery in patients with auditory hallucinations. American Journal
of Psychiatry, 157,
16911693.
Shergill, S. S., Bullmore, E. T., Brammer, M. J., et al (2001) A functional MRI study of auditory verbal imagery. Psychological Medicine, 31, 241253.[CrossRef][Medline]
Shergill, S. S., Brammer, M. J., Fukuda, R., et al (2002) Modulation of activity in temporal cortex during generation of inner speech. Human Brain Mapping, 16, 219227.[CrossRef][Medline]
Spence, S. A., Liddle, P. F., Stefan, M. D., et al
(2000) Functional anatomy of verbal fluency in people with
schizophrenia and those at genetic risk. Focal dysfunction and distributed
disconnectivity reappraised. British Journal of
Psychiatry, 176,
5260.
Steel, R. M., et al (2001) Diffusion tensor imaging (DTI) and proton magnetic resonance spectroscopy (1H MRS) in schizophrenic subjects and normal controls. Psychiatry Research Neuroimaging, 106, 161170.[CrossRef]
Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. (1995) An internal model for sensorimotor integration. Science, 269, 18801882.[Medline]
Received for publication September 13, 2002. Revision received November 28, 2002. Accepted for publication December 9, 2002.
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