Brain, Vol. 126, No. 1, 161-169,
January 2002
© 2002 Guarantors of Brain
doi: 10.1093/brain/awg015
A neural basis for the perception of voices in external auditory space
1 Sheffield Cognition and Neuroimaging Laboratory (SCANLab), Academic Department of Psychiatry and 2 Academic Unit of Radiology, University of Sheffield, Sheffield, 3 Wellcome Department of Imaging Neuroscience, Queen Square, London, 4 Auditory Group, Newcastle University Medical School, Newcastle upon Tyne, UK
Correspondence to: Dr Hunter, Sheffield Cognition and Neuroimaging Laboratory (SCANLab), Academic Department of Psychiatry, University of Sheffield, The Longley Centre, Norwood Grange Drive, Sheffield S5 7JT, UK E-mail: m.d.hunter{at}shef.ac.uk
Received May 15, 2002. Revised July 29, 2002. Accepted August 2, 2002.
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Summary |
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We used functional imaging of normal subjects to identify the neural substrate for the perception of voices in external auditory space. This fundamental process can be abnormal in psychosis, when voices that are not true external auditory objects (auditory verbal hallucinations) may appear to originate in external space. The perception of voices as objects in external space depends on filtering by the outer ear. Psychoses that distort this process involve the cerebral cortex. Functional magnetic resonance imaging was carried out on 12 normal subjects using an inside-the-scanner simulation of ‘inside head’ and ‘outside head’ voices in the form of typical auditory verbal hallucinations. Comparison between the brain activity associated with the two conditions allowed us to test the hypothesis that the perception of voices in external space (‘outside head’) is subserved by a temperoparietal network comprising association auditory cortex posterior to Heschl’s gyrus [planum temporale (PT)] and inferior parietal lobule. Group analyses of response to ‘outside head’ versus ‘inside head’ voices showed significant activation solely in the left PT. This was demonstrated in three experiments in which the predominant lateralization of the stimulus was to the right, to the left or balanced. These findings suggest a critical involvement of the left PT in the perception of voices in external space that is not dependent on precise spatial location. Based on this, we suggest a model for the false perception of externally located auditory verbal hallucinations.
Keywords: auditory verbal hallucinations; functional MRI; head-related transfer function; virtual acoustic space
Abbreviations: AVH = auditory verbal hallucination; BOLD = blood oxygenation level-dependent; EPI = echo-planar imaging; fMRI = functional MRI; HRF = haemodynamic response function; HRTF = head-related transfer function; IPL = inferior parietal lobule; MNI = Montreal Neurological Institute; PT = planum temporale; SPM = statistical parametric mapping; STS = superior temporal sulcus
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Introduction |
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In classical phenomenology a distinction is made between auditory verbal hallucinations (AVHs) located in objective external space (‘outside the head’; ‘true’ hallucinations) and those perceived in internal subjective space (‘inside the head’; pseudo-hallucinations) (Jaspers, 1959
). Clinicians often attach significant diagnostic utility to this distinction, but phenomenological surveys of psychosis indicate that the relationship between the spatial location of AVHs and the disease process is not simple (Oulis et al., 1995; Nayani and David, 1996). The perception of AVHs in external space is positively correlated with how realistic they appear to the person experiencing them. However, Jaspers’ assertion that ‘inside head’ AVHs are always less realistic, and necessarily subjective, is not supported by these phenomenological studies. Additionally, in a cross-sectional study, patients recently diagnosed with schizophrenia tended to report AVHs that were external, whilst those with longer histories described ‘voices inside the head’ (Nayani and David, 1996).
Functional imaging has been used to examine patterns of brain activation in the hallucinated state, and has implicated auditory cortices using functional MRI (fMRI; Woodruff et al., 1995; Dierks et al., 1999; Shergill et al., 2000), Broca’s area using single photon emission computed tomography (SPECT; McGuire et al., 1993) and sub-cortical structures using PET (Silbersweig et al., 1995) in the pathogenesis of AVHs. Co-variables, such as the cortical response to external speech (Woodruff et al., 1997) and the monitoring of internal verbal imagery (McGuire et al., 1996), have also been assessed by functional imaging (for reviews see David, 1999; Mitchell et al., 2001). No published functional imaging study has contrasted AVHs located outside and inside the head.
The perception of voices as external sound objects in the natural acoustic world involves the processing of spectrotemporal pattern at different levels. Although robust to a certain loss of spectral (Shannon et al., 1995) or temporal (Saberi and Perrott, 1999) detail, the detection of these features is essential for speech perception. The spatial location of a voice sound imposes further spectrotemporal pattern on that sound. Differences in the time of arrival and intensity of sounds arriving at either ear represent binaural cues for the localization of sounds that are situated on one or other side of the head (Rayleigh, 1876). The processing of such cues first occurs in the brainstem and can be deranged in brainstem disorders (van der Poel et al., 1988). However, the perception of voices as objects in external space depends upon filtering by the outer ear (Hofman et al., 1998). The pinnae impose a transfer function on sounds that corresponds to a spatially dependent filter (Wightman and Kistler, 1989). This fundamental process can be abnormal in psychoses that involve the cerebral cortex (McGuire et al., 1993; Woodruff et al., 1995; Dierks et al., 1999; Shergill et al., 2000) when voices that are not true external auditory objects (AVHs) may appear to originate in external space (Oulis et al., 1995; Nayani and David, 1996).
The analysis of spectrotemporal pattern in speech and the interpretation of spectrotemporal characteristics imposed by the pinnae to allow localization of voices could, a priori, involve early auditory processing before meaning was associated with that pattern. Such processing may occur in the planum temporale (PT), an area of association cortex in the posterior superior temporal plane (Westbury et al., 1999), posterior to the primary auditory cortex in Heschl’s gyrus (Rademacher et al., 2001). The PT is involved in the analysis of a number of different types of spectrotemporal pattern including the analysis of spatially determined sound properties (Table 1). The variety of sounds activating the PT suggest that it is not a specific ‘speech area’, but that it would be a suitable area for the disambiguation of the spectrotemporal effect of localizing a sound in space. Further processing of spatial information might occur in the contiguous inferior parietal lobule (IPL) implicated in the processing of fixed and dynamic spatial sound characteristics (Griffiths et al., 1998a, 2000; Bushara et al., 1999).
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In the current study, we aimed to use fMRI and virtual acoustics to test the hypothesis that the perception of voices in external auditory space depends upon neural processes subserved by a temperoparietal network consisting of PT and IPL. The secondary aim was to investigate the effect of stimulus laterality on the neural processing of ‘externality’. Our longer-term aim was to develop a model of external AVHs capable of generating further hypotheses that could be tested by functional imaging in hallucinating patients.
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Material and methods |
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Subjects
Thirty healthy volunteers (16 male, 14 female; mean age (± SD) = 22.7 ± 0.8 years) participated in an outside-of-scanner psychophysical validation experiment. Twelve different healthy right-handed males participated in the scanning study. These 12 subjects were assessed using the National Adult Reading Test (NART; Nelson, 1982
), the Edinburgh Handedness Inventory (Oldfield, 1971), and had T1- and T2-weighted structural MRI brain scans prior to their participation in the fMRI experiments. The group profile was [mean (± SD)]: age = 25.7 ± 4.1 years; NART IQ = 120.8 ± 3.3; right hand dominance = 88.2 ± 11.6%. All subjects were without clinical histories of neurological, psychiatric or hearing disorder, and gave informed consent to participate in the study, which was approved by the North and South Sheffield Research Ethics Committees.
Stimuli
Nayani and David found that the most typical AVHs were commands spoken in the second person by a single male voice (Nayani and David, 1996). Using this finding as a model, we recorded 300 unique hallucination-like auditory stimuli (spoken commands uttered by the same male voice) under identical conditions at 16 bits and a sample rate of 44.1 kHz. The stimuli were all of three or four words in length, with maximum duration of 2 s. The spoken commands fell within three domains: motor commands (e.g. ‘close the door’), auditory commands (e.g. ‘listen to a CD’) or visual commands (e.g. ‘look at a picture’). Stimuli were emotionally neutral in order to minimize any potential confounding effects due to content. There were equal numbers of stimuli in each semantic domain.
Each stimulus was designed so as to lateralize towards right or left. Normally, presentation of an auditory stimulus via headphones results in a sound that is perceived between the ears (‘inside the head’). Modification of acoustic stimuli using virtual acoustic space techniques allows the perception of objects in external space (‘outside the head’) despite headphone delivery. The modification depends on convolution of the acoustic stimulus with the spatially variable transfer function of the pinnae, the head-related transfer function (HRTF; Wightman and Kistler, 1989). In these experiments, ‘inside head’ stimuli were created by inter-aural amplitude ratio adjustment (3 : 1 in the required direction) and ‘outside head’ stimuli were produced by convolution with a generic HRTF from the University of Wisconsin (Madison, WI, USA) using MATLAB (The Mathworks Inc., Natick, MA, USA) software. The HRTF technique uses eardrum microphone recordings of free-field sounds to derive digital filter characteristics. These mimic the effect of the pinnae and create waveforms at the eardrums that, whilst headphone-delivered, are the same as those that would be produced if the sounds were played in the free-field. The generic HRTF used in these experiments does not allow the same spatial acuity as individual HRTFs (Hofman et al., 1998) but nevertheless reliably produces the required percept especially in the azimuthal plane, the horizontal plane through subjects’ pinnae. All stimuli (‘inside head’ and ‘outside head’) were spatially located in the azimuthal plane.
During scanning, the digital stimuli were presented in random order via a Commander XG MRI compatible sound system with electrostatic headphones (Resonance Technology, Inc., Los Angeles, CA, USA). A sensation level of 20 dB above the background noise of the scanning sequence produced fully intelligible speech.
Psychophysical validation
Outside the scanner, we used a forced-choice paradigm to test whether subjects could detect differences between ‘inside head’ and ‘outside head’ stimuli. One hundred unique pairs of identical elements (spoken commands) were sequentially presented via headphones every 10 s. Each pair was lateralized to right or left in the azimuthal plane. There were equal numbers of right and left sided pairs overall. One element of each pair was ‘inside head’ and the other ‘outside head’; elements were created using the methods described above. The ‘outside head’ element of each pair was randomly assigned to be either the first or the second element that subjects heard in that pair. Subjects listened through headphones and were required to state which of the two elements (first or second) was ‘outside head’ for 100 trials. Responses were recorded on a pre-printed checklist.
Scanning paradigm
Whole-head fMRI was performed on a 1.5 T system (Eclipse, Philips Medical Systems, Cleveland, OH, USA) at the University of Sheffield. At each of 100 time-points, 32 contiguous transverse images were acquired [gradient-recalled echo-planar imaging (EPI); repetition time = 3 s; echo time = 40 ms; slice thickness = 4 mm; field of view = 240 mm; in-plane matrix = 128 x 128]. This acquisition sequence generated 3200 EPI images in 5 min. Subjects fixated on a cross at the centre of the visual field during scanning, in order to minimize any eye movement related brain activation.
Each 5-min scanning experiment comprised five 1-min epochs of speech stimuli. Each epoch consisted of two 30-s conditions in an alternating ‘off’/‘on’ boxcar design, where ‘off’ refers to ‘inside head’ and ‘on’ refers to ‘outside head’ stimuli. In each experiment the contrast was the same (‘outside head’ minus ‘inside head’ stimuli).
All 12 subjects underwent three experimental scans (Table 2). Experiment 1 contrasted ‘outside head’ and ‘inside head’ stimuli when there was a predominance of right-lateralized stimuli in both conditions. Experiment 2 contrasted ‘outside head’ and ‘inside head’ stimuli when there were equal numbers of right- and left-lateralized stimuli in both conditions. Experiment 3 contrasted ‘outside head’ and ‘inside head’ stimuli when there was a predominance of left-lateralized stimuli in both conditions. Scanning order was counterbalanced between subjects.
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Within each condition, a stimulus was presented every 3 s. The content of every stimulus was unique and therefore subjects heard each of the 300 stimuli once. In order to check their attention, subjects were required to press either button A with their right middle finger (if they perceived the command as originating from the right) or button B with their right index finger (if the command originated from the left). The intra-scanner response box was optically connected to PsyScope software (Cohen et al., 1993
) running on an Apple Macintosh G3 computer, via an interface (New Micros Inc., Dallas, TX, USA). Response accuracy was recorded.
Analysis
Group analyses were carried out for all subjects using statistical parametric mapping in SPM99 (http://www.fil.ion.ucl.ac.uk/spm). Images were realigned, spatially normalized (Friston et al., 1995) and smoothed with a Gaussian kernel of 6 mm full width at half maximum. The blood oxygenation level-dependent (BOLD) response was modelled by a boxcar wave convolved with the canonical haemodynamic response function (HRF) and its temporal derivative. Global effects were corrected for using an analysis of covariance. High and low pass filters (derived from epoch duration and the HRF, respectively) were applied to the BOLD response data.
SPM99 combines the general linear model and Gaussian field theory to draw statistical inferences from BOLD response data regarding deviations from the null hypothesis in 3D brain space. We used a fixed-effects model to assess the difference in BOLD response between ‘outside head’ and ‘inside head’ conditions. Such a model is justified by the similarity of each member within the group with respect to gender, age, handedness and intelligence. The voxel-wise analysis of t statistics produced a parametric brain map (SPM{t}) for each experiment in the stereotactic space of the Montreal Neurological Institute (MNI; Evans et al., 1993).
Our study was hypothesis driven and, therefore, the statistical threshold for reporting was set at P < 0.001, uncorrected, for height and extent of activation in the SPM{t}. For the purposes of reporting and neuroanatomical labelling, the co-ordinates of significant areas of activation were transformed from MNI space into the stereotactic space of Talairach and Tournoux (1988).
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Results |
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Outside the scanner, all 30 subjects in the psychophysical validation experiment exhibited 100% accuracy in identifying ‘outside head’ stimuli. Inside the scanner, the 12 subjects all had normal structural MRI brain scans and did not significantly differ in accuracy for identification of individual stimulus laterality between the ‘outside head’ (mean accuracy 99.94%) and ‘inside head’ (mean accuracy 99.67%) conditions [t = 1.7 (35); ns]. All subjects were debriefed and confirmed that they had experienced a stable perception of alternating ‘inside head’ and ‘outside head’ stimulus conditions.
Group fMRI data: ‘outside head’ voices minus ‘inside head’ voices
In each of the three scanning experiments we observed significant activation in the left PT (Table 3; Fig. 1). Strikingly, no activation was shown in any other brain region in any of the individual experiments. Contrasting stimuli originating outside the head, on the right, versus stimuli originating inside the head, also on the right (Experiment 1; Fig. 1A), produced left PT activation posterior to and distinct from Heschl’s gyrus. Combined right- and left-sided stimuli (Experiment 2; Fig. 1B), produced activation foci smaller than, but overlapping with, those in Experiment 1. Using left-sided stimuli (Experiment 3; Fig. 1C) produced another smaller activated area, overlapping with the most medial activity in Experiment 1. Combining the data from Experiments 1, 2 and 3 to produce an ‘all outside-head’ minus ‘all inside-head’ contrast (Fig. 1D) demonstrated the largest extent and height of activity in the left PT (Talairach co-ordinates: x = –62, y = –16, z = 4; 771 voxels exceeded height threshold P < 0.001, uncorrected; peak Z score = 6.69).
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Reverse contrast: ‘inside head’ minus ‘outside head’ voices
In order to check the specificity of the main contrast of interest, we also examined the reverse contrast. This allowed us to see which brain areas were more activated during the baseline condition (‘inside head’ voices) than during the presentation of ‘outside head’ voices. Contrasting right-sided stimuli inside the head versus right-sided stimuli outside the head (Experiment 1) and contrasting left-sided inside head stimuli with left-sided outside head stimuli (Experiment 3) produced no supra-threshold areas of activation. The reverse contrast in Experiment 2 compared right- and left-sided voices inside the head with right- and left-sided voices outside the head, and produced two significant areas of activation, both in the right posterior parietal cortex, which also involved the precuneus (medial cluster, Talairach co-ordinates: x = 8, y = –59, z = 58; 238 voxels exceeded height threshold P < 0.001, uncorrected; peak Z score = 5.84; lateral cluster: x = 46, y = –44, z = 52; 313 suprathreshold voxels; peak Z score = 5.15). There were no areas of activation in the temporal cortex in this reverse contrast.
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Discussion |
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For patients with AVHs the external acoustic environment is often distorted—voices are present in the absence of a speaker or any other apparent stimulus source. Our study contrasted speech stimuli perceived as outside or inside the listener’s head in order to identify the brain areas involved in representing speech in external auditory space. We wanted to develop a model of AVHs in healthy volunteers that would enable us to make predictions about the neural substrate of external hallucinated voices in patient groups. Our results suggest that the neural processing of voices in external auditory space is associated with significant activation in the left PT. This finding supports our research hypothesis that the PT is involved in processing acoustic patterns that are important in the perception of sound spatial location.
The PT and perception of voices in external auditory space
In terms of both its anatomical location and cytoarchitecture, the PT represents a transitional area between auditory association and parietal cortices (for a review see Shapleske et al., 1999). In the macaque, the PT analogue has been postulated to form part of a posterior network involved in processing spatial aspects of sound perception (Romanski et al., 1999). In humans, PT has also been shown to have a role in processing acoustic spatial perception, i.e. moving sounds (Baumgart et al., 1999; Warren et al., 2002).
Recent work suggests that most neurons in primary auditory cortex behave in a linear fashion and are not well suited to the representation of auditory space (Schnupp et al., 2001). We postulate that an acoustic spatial perception system requires pattern-processing beyond primary auditory cortex (PT), and that other aspects of audition also engage this area (Table 1). Such an area may be important when it is necessary to process a spectrotemporal pattern in order to interpret incoming stimuli. Our current findings are compatible with the hypothesis that the PT is involved in the neural representation of speech in external space because of a role in processing pattern imposed on sound by the filtering effect of the pinnae (or, in this study, pattern imposed by a digital filter imitating the pinnae). To our knowledge this is the first attempt to show, using functional imaging, the neural basis for the perception of voices in external auditory space.
The question arises as to why PT activation was so clearly lateralized toward the left. Our stimuli were spoken commands. Scott and colleagues found that the left superior temporal sulcus (STS) had a specific role in the processing of speech and speech-derived auditory stimuli (Scott et al., 2000). In their study, the left posterior STS was engaged by speech-derived stimuli, regardless of intelligibility, as long as the stimuli contained a discernible phonetic pattern. The contrast condition consisted of rotated vocoded speech, which has no such discernible phonetic pattern. We used speech stimuli in both contrasting conditions. Therefore, any lateralization of activation due to speech per se is not likely to be a primary effect, but could be related to modulation of spatial processing by the type of stimulus being used. Previous studies have implicated both hemispheres in the processing of static spatial sound characteristics (Bushara et al., 1999) and the right hemisphere in the processing of sound movement (Griffiths et al., 1998a, 2000; Baumgart et al., 1999). Our results are compatible with a model of the PT as a ‘computational hub’ for disentangling different spectrotemporal patterns in sound. When it is necessary to separate a spatial pattern from a phonetic pattern in speech, then this model can accommodate left-sided PT involvement because of the need to access left hemisphere language areas (Griffiths and Warren, 2002).
The ‘outside head’/‘inside head’ distinction, although the focus of our interest in this experiment, was implicit to our experimental design and covert with respect to subjects’ awareness of it. We deliberately directed attention away from the main effect being studied by requiring subjects to indicate the laterality of every stimulus, a value that was balanced between the condition of interest and its contrast. Inside the scanner, we did not ask subjects to identify every ‘outside head’ stimulus because focusing attention in this way may modulate auditory cortex activation in a non-specific manner, which might confound interpretation of results (Woodruff et al., 1996; Zatorre et al., 1999). This may explain why no activation was observed in the IPL. Earlier work showing the IPL to be involved in sound spatial processing had a clear attentional component (Griffiths et al., 1998a, 2000; Bushara et al., 1999).
Interestingly, in the ‘reverse contrast’ for Experiment 2 (inside versus outside head voices with equal numbers of right- and left-sided stimuli) we did observe significant activation in the right posterior parietal lobe. We believe that this finding may be related to performing the behavioural task. Since inside head stimuli were necessarily more ‘medial’ than outside head stimuli, subjects might have had to direct more attention at discriminating stimulus laterality in order to maintain the overall consistency in performance that we observed. The equal numbers of right- and left-sided stimuli in Experiment 2, compared with the predominance of one or the other side in Experiments 1 and 3, could further increase the attentional demands of the behavioural task. Perhaps this is why parietal activation was seen in the reverse contrast for Experiment 2 but not for Experiments 1 or 3. Our results are compatible with work that has shown, in an auditory task, that activation in the parietal region is positively correlated with attentional load (Belin et al., 1998).
Our findings are supported by lesional studies that have shown both right- (Bellmann et al., 2001) and left-sided (Clarke et al., 2000) superior temporal gyrus lesions, including the PT area, to be associated with auditory spatial deficits in experimental paradigms that used inter-aural phase manipulation to lateralize auditory stimuli. The superior temporal gyrus may also have a role in global spatial awareness. Karnath and colleagues studied patients with right hemispheric lesions and contrasted those with and without spatial neglect (Karnath et al., 2001). These authors found that the right superior temporal gyrus, including the PT, was the most extensively lesioned area in the patients with spatial neglect.
Whilst all three experiments demonstrated activation in similar areas, it is noteworthy that the predominantly right-sided ‘outside head’ minus ‘inside head’ contrast (Experiment 1) showed the largest extent of activation in left PT. This effect of stimulus laterality on neural response may have been because of ‘right ear advantage’ in subjects with a dominant left hemisphere (Kimura, 1967). Theoretically, such a ‘right ear advantage’ effect arises because the bilateral representation of acoustic pathways favours the contralateral hemisphere. Right ear afferents are more directly connected to the dominant auditory cortex than left ear afferents, which must travel via the non-dominant auditory cortex and corpus callosum. This functional asymmetry of the auditory system may also explain why, despite all being within left PT, there were some differences in precise spatial location of activation maxima in the three experiments.
All of the stimuli that we used were unique meaningful phrases and all conditions in each experiment were distinct. We controlled for semantics, but because speech consists of many qualities (e.g. phonetic structure, prosody, duration) it is not possible to state that the ‘outside head’ and ‘inside head’ conditions were the same in all respects except spatial location. However, the probability of any systematic bias in favour of either condition must be very small. The random order of stimulus presentation in both conditions would make this probability even smaller. An alternative approach might have been to use single words that were identical in both conditions, but such stimuli do not phenomenologically resemble the AVHs of schizophrenia.
Our experimental paradigm was designed to address the issue of whether a temperoparietal network is involved in the neural representation of speech in external auditory space. Therefore, a single contrast that examined this question was employed. In this context, the issue of scanner noise needs to be discussed. As stated above, we did not ask subjects to actively detect ‘outside head’ voice ‘targets’ during the scanning experiments, because this may alter activation in the auditory cortex. Instead we undertook a psychophysical validation experiment outside the scanner, which showed the perception of voices in external acoustic space to be robust and not subject to habituation effects. Debriefing subjects from the scanning experiments confirmed that scanner noise had not impaired this perception. This is not surprising since, for each subject, we titrated the amplitude of stimulus delivery to 20 dB above the background level of scanner noise. However, in the absence of quantitative psychophysical data acquired during scanning, the influence of scanner noise on psychophysical robustness is not completely clear. We are not aware of any studies that have sought to specifically develop and test virtual acoustic space techniques for use in the standard fMRI environment, and this remains an interesting area for future psychophysical research. McGuire’s group investigated the neural basis for AVHs using both a noisy and a quiet fMRI sequence (Shergill et al., 2000) and found some differences in brain activation between the two methods, but also considerable overlap of activation in temporal cortex. In our experiments, the noise of the scanner sequence was constant and, specifically, did not vary between the two contrasting conditions. Therefore, we believe that the risk of scanner noise having specifically affected brain activation in one condition, but not the other, in three separate experiments, is likely to be small.
The PT in schizophrenia
The existing functional imaging literature regarding AVHs in schizophrenia supports a general view that these phenomena arise through abnormal activation in the normal audition, speech and language areas (McGuire et al., 1993; Woodruff et al., 1995, 1997; Dierks et al., 1999; Shergill et al., 2000). Based on the cognitive neuropsychiatric principle that clinical phenomenology can be understood in terms of functions altered by lesions, our results will now be discussed with reference to the schizophrenia literature.
The question of whether or not the PT is abnormal in schizophrenic subjects with AVHs is unresolved. Significant abnormalities, characterized by a reversal of the normal left > right asymmetry for surface area, have been described in schizophrenic patients using morphometric MRI (Barta et al., 1997; for meta-analysis see Shapleske et al., 1999). However, this technique has also failed to demonstrate any pathological reversal of laterality (Shapleske et al., 2001). Barta and colleagues found a strong correlation between severity of AVHs and reduction in volume of the entire left superior temporal gyrus (Barta et al., 1990). However, their region-of-interest was not specifically the PT and subsequent volumetric analyses (Shapleske et al., 2001) have failed to find a correlation between hallucination severity and any PT abnormality, although these may be detectable using voxel-based analyses (Rossell et al., 2001). Our results do not predict a link between PT abnormality and AVH severity, but might suggest a positive correlation between PT size and the relative ‘externality’ of AVHs. This is an interesting prediction because there is evidence that PT diminishes in size, over time, in schizophrenia (Mathalon et al., 2001) and also that AVHs become more ‘inside the head’ over time in this disorder (Nayani and David, 1996).
Functional imaging has also implicated left PT in the pathogenesis of AVHs. Dierks and colleagues used fMRI and found increased BOLD response in left PT in two out of the three hallucinating schizophrenic patients in their study (Dierks et al., 1999). The authors did not describe phenomenology in terms of spatial location, but our model would predict that the two patients with left PT activity experienced external AVHs whilst the third patient did not.
Conclusion
We have used fMRI and a virtual acoustics paradigm to implicate left PT in the perception of voices in external auditory space. We believe that this perception can arise because PT has a role in processing spectrotemporal pattern in sound. Specifically, PT may be involved in the neural processing of the pattern imposed on waveforms by the filtering effect of the pinnae that is essential for perceiving spatial aspects of environmental sounds. The opportunity now exists to investigate the function of this region in patients with abnormal speech perceptions and auditory spatial deficits. We speculate that the variable externalization of AVHs in schizophrenia may reflect variable involvement of PT in the disease process. Our findings further delineate the functional organization of the human auditory cortex and predict a critical perturbation of processing in the left PT manifest as the perception of external ‘voices’ in psychosis.
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Acknowledgements |
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We wish to thank the volunteers who participated in the study and radiography colleagues at the Royal Hallamshire Hospital, Sheffield. T.D.G. is supported by the Wellcome Trust (UK). This work was supported by funding from The University of Sheffield.
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