Contributions of emotional prosody comprehension deficits to the formation of auditory verbal hallucinations in schizophrenia.
ABSTRACT Deficits in emotional processing have been widely described in schizophrenia. Associations of positive symptoms with poor emotional prosody comprehension (EPC) have been reported at the phenomenological, behavioral, and neural levels. This review focuses on the relation between emotional processing deficits and auditory verbal hallucinations (AVH). We explore the possibility that the relation between AVH and EPC in schizophrenia might be mediated by the disruption of a common mechanism intrinsic to auditory processing, and that, moreover, prosodic feature processing deficits play a pivotal role in the formation of AVH. The review concludes with proposing a mechanism by which AVH are constituted and showing how different aspects of our neuropsychological model can explain the constellation of subjective experiences which occur in relation to AVH.
- SourceAvailable from: Saskia Steinmann[Show abstract] [Hide abstract]
ABSTRACT: Auditory verbal hallucinations (AVH) are one of the most common and most distressing symptoms of schizophrenia. Despite fundamental research, the underlying neurocognitive and neurobiological mechanisms are still a matter of debate. Previous studies suggested that "hearing voices" is associated with a number of factors including local deficits in the left auditory cortex and a disturbed connectivity of frontal and temporoparietal language-related areas. In addition, it is hypothesized that the interhemispheric pathways connecting right and left auditory cortices might be involved in the pathogenesis of AVH. Findings based on Diffusion-Tensor-Imaging (DTI) measurements revealed a remarkable interindividual variability in size and shape of the interhemispheric auditory pathways. Interestingly, schizophrenia patients suffering from AVH exhibited increased fractional anisotropy (FA) in the interhemispheric fibers than non-hallucinating patients. Thus, higher FA-values indicate an increased severity of AVH. Moreover, a dichotic listening (DL) task showed that the interindividual variability in the interhemispheric auditory pathways was reflected in the behavioral outcome: stronger pathways supported a better information transfer and consequently improved speech perception. This detection indicates a specific structure-function relationship, which seems to be interindividually variable. This review focuses on recent findings concerning the structure-function relationship of the interhemispheric pathways in controls, hallucinating and non-hallucinating schizophrenia patients and concludes that changes in the structural and functional connectivity of auditory areas are involved in the pathophysiology of AVH.Frontiers in Human Neuroscience 01/2014; 8:55. · 2.91 Impact Factor
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ABSTRACT: Recent findings have demonstrated that emotional prosody (EP) attracts attention involuntarily (Grandjean et al., 2008). The automat shift of attention toward emotionally salient stimuli can be overcome by attentional control (Hahn et al., 2010). Attentional control is impaired in schizophrenia, especially in schizophrenic patients with hallucinations because the “voices” capture attention increasing the processing load and competing for top-down resources. The present study investigates how involuntary attention is driven by implicit EP in schizophrenia with auditory verbal hallucinations (AVH) and without (NAVH). Fifteen AVH patients, 12 NAVH patients and 16 healthy controls (HC) completed a dual-task dichotic listening paradigm, in which an emotional vocal outburst was paired with a neutral vocalization spoken in male and female voices. Participants were asked to report the speaker's gender while attending to either the left or right ear. NAVH patients and HC revealed shorter response times for stimuli presented to the attended left ear than the attended right ear. This laterality effect was not present in AVH patients. In addition, NAVH patients and HC showed faster responses when the EP stimulus was presented to the unattended ear, probably because of less interference between the attention-controlled gender voice identification task and involuntary EP processing. AVH patients did not benefit from presenting emotional stimuli to the unattended ear. The findings suggest that similar to HC, NAVH patients show a right hemispheric bias for EP processing. AVH patients seem to be less lateralized for EP and therefore might be more susceptible to interfering involuntary EP processing; regardless which ear/hemisphere receives the bottom up input.Frontiers in Human Neuroscience 03/2013; 7(59). · 2.91 Impact Factor
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ABSTRACT: Emotion perception deficits are a well-established feature of schizophrenia (SZ). Individuals with SZ have difficulty labeling emotional stimuli across auditory, visual, and audio-visual modalities and also misattribute threat towards neutral stimuli. The relationship between a history of psychosis and similar abnormalities in bipolar disorder (BD) is less clear. The current study set out to examine emotion perception across sensory modalities in a sample of 24 stabilized individuals meeting criteria for SZ, 24 remitted individuals meeting criteria for BD with psychotic features, 24 remitted individuals meeting criteria for BD without psychotic features, and 24 healthy controls. Results indicated that the bipolar with psychotic features group had intermediary performance between the SZ group and the other two groups for auditory, visual, and audio-visual items, with particularly poor performance in identifying angry stimuli. The SZ group misattributed neutral stimuli as negative when they were in visual format, but as positive when they were in auditory or audio-visual formats. The bipolar with psychotic features group had a trend towards misattributing more neutral visual stimuli as negative. These findings indicate that emotion perception deficits are present in BD with psychotic features and comparatively spared in BD without psychotic features, and that a similar bias of misattributing negative emotions to neutral visual stimuli may be present across diagnostic boundaries.Schizophrenia Research 04/2013; · 4.59 Impact Factor
Contributions of emotional prosody comprehension deficits to the formation of
auditory verbal hallucinations in schizophrenia
Lucy Alba-Ferraraa,b,⁎, Charles Fernyhoughb, Susanne Weisb, Rachel L.C. Mitchellb, Markus Hausmannb
aRoskamp Laboratory of Brain Development, Modulation and Repair. Department of Psychiatry and Neurosciences, Morsani College of Medicine, University of South Florida, USA
bDepartment of Psychology, Durham University , UK
a b s t r a c t a r t i c l ei n f o
Received 11 April 2011
Received in revised form 6 February 2012
Accepted 8 February 2012
Available online 16 February 2012
Superior temporal gyrus
Deficits in emotional processing have been widely described in schizophrenia. Associations of positive
symptoms with poor emotional prosody comprehension (EPC) have been reported at the phenomenological,
behavioral, and neural levels. This review focuses on the relation between emotional processing deficits and
auditory verbal hallucinations (AVH). We explore the possibility that the relation between AVH and EPC in
schizophrenia might be mediated by the disruption of a common mechanism intrinsic to auditory processing,
and that,moreover, prosodic featureprocessing deficits playa pivotal role inthe formation of AVH. Thereview
concludes with proposing a mechanism by which AVH are constituted and showing how different aspects of
our neuropsychological model can explain the constellation of subjective experiences which occur in relation
© 2012 Elsevier Ltd. All rights reserved.
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Introduction: phenomenology of AVH and EPC . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The link between AVH and EPC at the behavioral level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Neural underpinnings of auditory hallucinations and their overlap with EPC . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Structural and functional connectivity within the EPC and AVH networks
Towards a new neuropsychological model of AVH. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction: phenomenology of AVH and EPC
Emotional impairment in schizophrenia was first observed by
Kraepelin (1919). Disturbances range from flat affect to intense bursts
of inappropriate emotions such as anger and fear (Kraepelin, 1971
). The combination of these emotional disturbances points to
one of the paradoxes of schizophrenia: whilst there can be a flatten-
ing of affect, as in negative symptoms, there can be also an increase
in emotional arousal and reactivity, as in the positive symptoms of
psychosis (Aleman & Kahn, 2005). Traditionally, deficits in emotion
processing have been linked to negative symptoms such as inefficient
social interaction, and apathy and avolition towards social stimuli
(Hoekert, Kahn, Pijnenborg, & Aleman, 2007). However, a possible
link between emotional processing difficulties, particularly for vocal
stimuli, and the presence of hallucinations or delusions (Rossell &
Boundy, 2005) has also been reported. In fact, dysfunctional emotion
processing may also be associated with the positive symptoms of
schizophrenia (Aleman & Kahn, 2005). In line with this idea, it has
been reported that maladapted forms of emotion regulation, such as
expressive suppression, have been associated with severity of halluci-
natory experience (Badcock, Paulik, & Maybery, 2011).
Although emotional disturbances are of central importance in psy-
chosis in general (van 't Wout, Aleman, Kessels, Laroi, & Kahn, 2004),
this review will focus on the impact of such disturbance in relation to
hallucinations. Deficits in the comprehension of vocal emotion are
Clinical Psychology Review 32 (2012) 244–250
⁎ Corresponding author at: Department of Psychology, Durham University, Science
Site, South Road, Durham, Co Durham, DH1 3LE, UK. Tel.: +44 191 334 3275; fax:
+44 191 334 3241.
E-mail address: firstname.lastname@example.org (L. Alba-Ferrara).
0272-7358/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
Contents lists available at SciVerse ScienceDirect
Clinical Psychology Review
thought to be specific for schizophrenic patients suffering from hallu-
cinations (Rossell & Boundy, 2005; Shea et al., 2007). Additionally
hallucinations in schizophrenia tend to be more often auditory than
visual (Mueser, Bellack, & Brady, 1990). The congruency in modality
between affective processing deficits and abnormal perception
might suggest an underlying common mechanism. Auditory modality
emotion recognition abilities are likely to be of central importance in
the formation of AVH, and the study of this connection promises to
reveal a mechanism linking both phenomena.
In everyday interactions, humans are persistently exposed to ver-
bal communication, meaning that large amounts of social information
are carried by the voice (Belin, Fecteau, & Bedard, 2004). Speech en-
codes semantic information, but also carries non-linguistic informa-
tion collectively known as prosody. These prosodic elements
comprise acoustic features such as pitch, amplitude, and segment
and pause duration, Prosody can be used to disambiguate the mean-
ing of an utterance (i.e. statement vs. question, known as linguistic/
stress prosody) as well as to encode affective information which is
known as emotional prosody (Belin et al., 2004). Thus, prosody allows
for the encoding and decoding of feelings in speech.
One of the central characteristics of AVH is that the voices patients
hear are often spoken in emotional tones (Copolov, Mackinnon, &
Trauer, 2004), most often with a negative emotional valence
(Nayani & David, 1996), e.g., angry voices shouting abusive language.
One interpretation of the link between AVH and EPC deficits lies in
the coincidence in emotional valence between both phenomena. Pa-
tients with AVH seem to have difficulties correctly identifying
happy prosody, possibly because of a tendency to attribute fear or
sadness to any stimulus (Tsoi et al., 2008) and research in schizophre-
nia suggests that perception and labeling of emotions such as anger
and fear may also be impaired (Allen et al., 2004). Regarding per-
ceived intensity of prosodic emotions, it has also been discovered
that patients with AVH generally tend to rate frightening stimuli as
more intense than controls and patients without AVH (Rossell &
Boundy, 2005). Given that patients who hear “malevolent” voices
tend to rate them as “very powerful” more often than patients who
hear benign or benevolent voices (Birchwood & Chadwick, 1997),
these AVH patients might also rate fearful stimuli in EPC tasks as
more intense. It should be noted that this review focuses on AVH in
schizophrenia and not in non-clinical population, as the emotional
valences of hallucinations between both populations seem to differ.
Delusions and hallucinations also seem to be linked. It is reasonable to
assume that individuals experiencing hallucinations may need to explain
sions. From this point of view, hallucinations are understood as a primary
phenomenon, and delusion a consequence of the former (Maher, 2006).
The relation between EPC deficits and AVH might also be mediat-
ed by attentional mechanisms. In the early literature, it was proposed
that a breakdown in selective attention may overload working mem-
ory with irrelevant sensory data. Such an overwhelming sensorial in-
flux putatively makes it difficult to integrate current perceptions with
past experience, giving rise to abnormal perception and resulting in
hallucinations (Chapman & McGhie, 1964). This proposal, however,
does not explain why the perceptions reaching consciousness very
often have a negative affective tone. Instead, this review proposes
that an attentional bias towards negative affects in EPC tasks may in-
crease the likelihood of experiencing AVH or even act as a trigger for
them. Therefore, it is essential to determine the direction of causation
in any such relation. On the one hand, emotionally negative AVH
might lead to a negative mood state, which is reflected in a bias to-
ward negative affects in EPC tasks. This has been shown in the visual
modality, in that depressed patients show a bias to perceive neutral
emotional facial expressions as negative (Hale, Jansen, Bouhuys, &
van den Hoofdakker, 1998). Thus, it is plausible that patients may
live in an emotional negative state because of the intrusive hallucina-
tions they experience, and this negative emotional state might bias
judgements regarding the emotional expressions of others, such as
in the evaluation of emotional prosody. On this interpretation, the
bias in EPC may be based in the distress that results from the experi-
ence of emotionally negative AVH. In this causal model, AVH cause
distress, and distress may lead to EPC deficits.
That interpretation notwithstanding, we intend to discuss how
AVH might be associated with underlying EPC disturbances, with
the direction of causation leading from emotion processing deficits
to the psychotic symptom. We will consider how EPC deficits may
contribute to the formation of AVH and to what extent aberrant audi-
tory processing might be underlying both phenomena. In order to
demonstrate this link we will consider behavioral and brain function-
al and structural findings connecting AVH and EPC, and we will inte-
grate this evidence to suggest a new neuropsychological model of
AVH with the aim of explaining the phenomenology of the abnormal
2. The link between AVH and EPC at the behavioral level
Until recently, the idea of an affective prosody impairment as a
modular deficit in schizophrenia was controversial. It was assumed
that impaired prosodic processing in schizophrenia patients merely
reflects basic sensory deficits such as misperception of pitch and am-
plitude (Leitman et al., 2005). For example, Leitman et al. (Leitman et
al., 2005) suggested that prosody processing deficits may be due, in
part, to low-level pitch discrimination defects (Leitman et al., 2005).
However, there is evidence to suggest that prosody processing defi-
cits in schizophrenia cannot be solely explained by pitch perception
defects. In fact, pitch is a feature of emotional as well as linguistic
prosody. If pitch perception impairment were the only cause of pros-
ody processing deficits, linguistic as well as emotional prosody should
be equally affected in schizophrenia, but contrary to this assumption,
stress prosody comprehension seems to be preserved in patients with
schizophrenia (Murphy & Cutting, 1990). In line with this observa-
tion, it is plausible that the dysfunction of low-level auditory proces-
sing, even if partially contributing to EPC impairment, is not sufficient
to explain the complexity of the emotional prosody deficits in schizo-
phrenia and that these may rather relate to a specific emotion proces-
In addition to the specificity of EPC impairment as an emotion pro-
cessing deficit, EPC difficulties are particularly prominent in the sub-
group of patients with schizophrenia who have a tendency towards
AVH. In a study comparing patients with and without AVH in an
EPC discrimination task (Rossell & Boundy, 2005), it was observed
that when EPC performance was tested with non-lexical speech
sounds spoken in different tones of voice, only the AVH patient
group were impaired relative to controls. When EPC stimuli con-
tained prosodic as well as semantic elements, both patient groups
showed significantly worse performance than controls. The authors
interpret these findings as suggesting a dissociation between EPC
for auditory stimuli with prosodic and semantic content, which fur-
ther supports the idea of a specific connection between AVH and
EPC. The additional processing of semantic content may mask the re-
lation between EPC and AVH. Deficits in semantic processing are
found in schizophrenia in general, without being linked to any symp-
tomatic manifestations of the disorder in particular (Rossell & David,
2006) while emotional prosodic deficits seem to be specific to the
AVH subgroup (Rossell & Boundy, 2005).
Interestingly, someresearchdidnotfindanassociation between EPC
ative symptomsandEPC deficits was found (Leitman et al., 2005). How-
ever, it should be noted that the cited study collapsed patients with
different diagnoses in the same group (i.e. schizophrenia and schizoaf-
fective disorder) and it applied a tool for the measurement of positive
symptoms which did not distinguished between different modalities
of hallucinations. Thus, it might be the case that prosody deficits might
L. Alba-Ferrara et al. / Clinical Psychology Review 32 (2012) 244–250
not be linked to hallucinations in other modalities and other diagnosis
categories besides auditory hallucinations in schizophrenia.
A further factor mediating the formation of hallucinations is voice
identity recognition. Prosodic features such as pitch intensity and
pitch duration are important cues in differentiating voices (Belin et al.,
2004). When prosodic features processing is impaired, recognition of
voice identity becomes more difficult, and thus a voice may sound like
someone else's (Cutting, 1990). In other words, voice identity recogni-
tion as well as vocal emotion recognition partly relies on processing of
the same paralinguistic acoustical features (Belin et al., 2004), of
which the most salient are fundamental frequency, intensity and inter-
val (Perrot, Aversano, & Chollet, 2007). In fact, professional imitators
use variations in pitch, tone and rhythm, to impersonate someone else
(Orchard & Yarmey, 1995; Perrot et al., 2007). Variations in these
same parameters can affect the emotion conveyed by the voice. Even
so, it is importantto note that some dissociations between voice identi-
ty recognition and emotional prosody comprehension have been found
(Garrido et al., 2009), suggesting that both processes share a common
paralinguistic ground. Following Cutting's approach (Cutting, 1990),
Shea and colleagues suggested that vocal emotion may serve as one of
the cues to determine the identity of the voice (Shea et al., 2007).
Thus, prosody could be one of the contributing factors in identifying
both others' as well as one's own voice, such as heard in inner speech.
From a cognitive perspective, prosodic features impairment may lead
to misattribution of inner speech via an incapacity to use the prosodic
cues to estimate the origin of the stimuli. If the patients cannot recog-
nize the origin and identity of their own inner voice, they might attri-
bute the voice to someone else. It is important to note that many
voices encountered in AVH have clear identities (Stephane, Thuras,
Nasrallah, & Georgopoulos, 2003). Additionally, it has been claimed
that misidentification of one's own inner speech relates to abnormal
self-monitoring (Johns et al., 2001). Our interpretation explores the
possibility that abnormal prosody processing may be a mechanism me-
diating misidentification of inner speech, which also contains prosodic
cues helping the individual to recognize the identity of the speaker
(Belin et al., 2004). Following this line of argument, inaccurate proces-
ute to a misidentification of the identity of one's own inner voice.
Inaccurate decoding of prosodic features might also lay a founda-
tion for the formation of certain AVH triggered by external sounds.
In fact, a direct relationship has been reported between the timbre
and pitch of real environmental sounds and how a degraded percep-
tion of them can be mistaken as an AVH (Hunter & Woodruff, 2004). A
similar mechanism of degraded auditory perception might not only
operate in the case of external environmental sounds but also for
voices as features such as timbre are also involved in voice identifica-
tion. It has been proposed that speaker identification is based on the
extraction of paralinguistic features such as frequency and pitch
(Formisano, De Martino, Bonte, & Goebel, 2008) (prosodic aspects of
speech). EPC deficits, may account for the misidentification of self-
generated auditory objects which lead to the formation of AVH. If
this conclusion is correct, it might also explain why many AVH con-
tain specific prosodic features and voice identities.
The idea that disrupted integration of external and propioceptive
perceptions are the basis of hallucinations has already been formulat-
ed by Chapman (1967), who proposed that distorted sensory infor-
mation from memory and proprioceptive information might be
perceived abnormally. Such perceptions may have diffuse qualities
and yet they might feel like a real perception from external stimuli
3. Neural underpinnings of auditory hallucinations and their
overlap with EPC
Studying gray matter abnormalities in patients with a history of
AVH offers additional evidence about the neural mechanisms
underlying the abnormal perception phenomenon. A recent study in
a large sample of 99 schizophrenia patients found reduced gray mat-
ter density bilaterally in the superior temporal gyri which was corre-
lated with hallucination severity (Nenadic, Smesny, Schlosser, Sauer,
& Gaser, 2010). Another recent study investigating the link between
AVH and gray matter volume reported significant structural differ-
ences between AVH patients and controls particularly in the left and
right superior temporal gyrus (STG), left inferior frontal gyrus, left
amygdala, and insula bilaterally (Garcia-Marti et al., 2008). The au-
thors, basing their interpretation on a previous model of emotional
dysfunction in schizophrenia (Aleman & Kahn, 2005), concluded
that the amygdala and insula as key regions of the emotional brain
may be involved in the emotional load of AVH (Garcia-Marti et al.,
2008), particularly in the emotional prosody conveyed by AVH.
One of the pioneering neuroimaging studies applied positron emis-
sion tomography (PET) to assess the pattern of regional cerebral blood
flow in schizophrenia patients when they were actively hallucinating.
Activation was found in left temporal lobe and Broca's area, suggesting
that certain language processes, such as speech production, inner
speech, and AVH share similar neural mechanisms (McGuire, Shah, &
Murray, 1993). A related functional magnetic resonance (fMRI) study
assessed patients with schizophrenia while hallucinating and during
auditory stimulation (Dierks et al., 1999) and found an activation of
the superior and medial temporal gyrus and primary auditory cortex
(predominantly in the left hemisphere for two patients and in the
right hemisphere for the third patient) for both conditions. Interesting-
ly, a recent study demonstrated that hallucinators activate the left pri-
mary auditory cortex to a lesser extent that controls when listening to
tunes, indicating that this region is tonically turned on to process irrel-
evant auditory objects (Ford et al., 2009).
Dierks and colleagues study also showed that during hallucina-
tions, the fronto-parietal operculum, the hippocampus, and the
amygdala showed an increase of the BOLD signal. The authors sug-
gested that the activation of the primary auditory cortex during the
hallucination may explain why hallucinations are perceived as real
and often external sounds (Dierks et al., 1999), whereas the amygdala
activation was considered to reflect an emotional response relating to
the emotional content of the voices. Moreover, the authors inter-
preted the activation of the left temporal lobe as an indication of se-
mantic processing in hallucinations, even though the relative
contributions of semantic and prosodic aspects of language were
not compared directly. Unfortunately, the lateralization of semantic
(normally left-lateralized) and prosodic processes (normally right-
lateralized) was not directly assessed in this study. Thus, these results
cannot be related to evidence of a reduced lateralization of linguistic
processing in schizophrenia particularly in those patients suffering
from severe hallucinations (Sommer, Ramsey, & Kahn, 2001; Weiss
et al., 2006).
Unlike the lateralization of linguistic processing, findings about
the lateralization of prosody processing in schizophrenia are equivo-
cal. While some evidence found a left lateralization of the normally
right-lateralized response to prosody (Mitchell, Elliott, Barry,
Cruttenden, & Woodruff, 2004), a more recent study found increased
right lateralization of emotional prosody in schizophrenic patients
(Bach et al., 2009). The findings from the cited studies are limited
by small sample sizes.
Only a very few studies have directly assessed the neural link be-
tween EPC and AVH. Evidence comes from an fMRI study of patients
with schizophrenia, in which neural activation in patients with and
without history of AVH was compared while listening to external
speech (Woodruff et al., 1997). This study found an increased activa-
tion particularly in the right middle temporal gyrus (MTG) for the pa-
tient group as a whole, relative to healthy controls during external
speech stimulation. The authors suggested that this might indicate
an inherent natural hyperresponsivity to emotional prosody of speech
in the patient group. In fact, right hemisphere hyperresponsivity has
L. Alba-Ferrara et al. / Clinical Psychology Review 32 (2012) 244–250
been found in other clinical populations such as violence offenders,
who also show deficits in the perception of emotional cues (Lee,
Chan, & Raine, 2009). Woodruff at al. also scanned schizophrenic pa-
tients during the hallucinating state when they were simultaneously
listening to external speech, finding that during AVH the response to
external speech in the right MTG was decreased. This finding suggests
that AVH compete with external speech for auditory processing re-
sources within the temporal cortex, including those regions which in
healthy population are known to be necessary for EPC (Woodruff et
al., 1997). However, as it has been previously said, the lateralization
of EPC in patients with schizophrenia remains controversial (Bach et
al., 2009; Mitchell et al., 2004).
Several studies addressed the overlap of the neural correlates of
AVH and perception of prosodic and semantic aspects of speech. For
listening to emotional speech, one study (Sanjuan et al., 2007)
found enhanced activation of the left middle and right superior tem-
poral lobe, insula, thalamus, and middle and superior frontal lobes in
a group of patients with AVH in comparison to controls. The stimuli
used in this study were based on patients' individual reports of the
content of their AVH, where words were selected as stimuli based
on their frequency in the reported AVH. The selected words contained
an emotional semantic meaning and were recorded in an imperative
prosodic tone. This study found an increase in brain activity in a
fronto-temporal network involving the orbitofrontal cortex, the left
medial temporal gyrus and right STG in the patient's group in com-
parison to controls, and this activation pattern was interpreted as re-
lated to AVH (Sanjuan et al., 2007). As this study did not test
schizophrenia patients without AVH, however, the results should be
interpreted with caution. Differences in the neural networks underly-
ing semantic and prosodic aspects of speech processing between
schizophrenia patients and healthy controls may be related to other
aspects of the disorder and not specifically to AVH. In opposition to
Sanjuan and colleagues, a recent study found decrease activity in su-
perior temporal and inferior parietal areas, and in bilateral insula in
AVH patients compared to patients without AVH when performing a
memory recollection task (Wible et al., 2009). The authors interpret
that as tonically elevated activity within these regions. The differ-
ences between studies might be due to the diverse paradigms they
employed. Since the stimuli used by Sanjuan and colleagues may
have triggered AVH, the task used in Wible et al. (2009) was meant
to compete for neural resources with AVH.
Along with the STG, the amygdala is one of the structures that
seem to be involved in AVH as well as in EPC, specifically for anger
and fear. Amygdala involvement in processing of angry voices may
relate to the fact that angry voices “threaten” the listener, which is es-
pecially pertinent in schizophrenia given the negative focus of AVH
outlined above. Further, it has been demonstrated that, at a resting
state, the amygdala shows higher metabolism in patients with schizo-
phrenia than in healthy controls. This might indicate a tonic hyperac-
tivation of the amygdala in schizophrenia, as opposed to a phasic
activation in the presence of salient emotional stimuli in healthy con-
trols. Interestingly, hypometabolism of the amygdala during emotion
judgment tasks has also been found in schizophrenia (for a review,
see Aleman & Kahn, 2005). In fact, a study assessing patients' neural
response to nonverbal emotional auditory stimuli (crying and laugh-
ing) found that patients with a history of AVH showed reduced activ-
ity in the left amygdala and bilateral hippocampus during crying
sounds in comparison with patients without such a history (Kang et
al., 2008). A different study found increased amygdala activation in
AVH patients during passive listening to emotional words in compar-
ison to NAVH and controls (Escarti et al., 2010). However, this study
did not control for occurrence of hallucinations during the scanning,
which was a likely eventuality given that AVH patients obtained
high scores in a scale measuring hallucinatory experience in the pre-
vious 24 h to the testing session. Thus, the fMRI results might rather
have been related to the experience of hallucinations itself than to
the experimental stimuli. Possibly, the constant hypermetabolism of
the amygdala in schizophrenic patients prevents the detection of dif-
ferences in BOLD response between baseline and threatening stimuli
conditions. Furthermore, tonic pattern of amygdala activation might
explain the ubiquitous perception of threats some patients suffer
from, resulting in constant (implicit) processing of emotional stimuli
leading to lead to feelings of being emotionally overwhelmed that
precedes development of AVH.
4. Structural and functional connectivity within the EPC and
Studies of structural connectivity with diffusion tensor imaging
(DTI) have revealed that AVH schizophrenia patients, compared
with non-AVH schizophrenia patients, showed an increased connec-
tivity in the temporo-parietal section of the arcuate fasciculus (Hubl
et al., 2004; Shergill et al., 2007), which connects the STG and medial
temporal gyrus (MTG) with the inferior frontal lobe (Glasser & Rilling,
2008). It should be noted that a right temporo-parietal network has
been identified as underlying emotional prosody processing (Alba-
Ferrara, Hausmann, Mitchell, & Weis, 2011; Bach et al., 2008;
Mitchell, Elliott, Barry, Cruttenden, & Woodruff, 2003). Moreover, it
has been proposed that perturbations in a left posterior temporal
and inferior parietal regions network comprising the dorsal “where”
auditory pathway results in the AVH to be perceived in external
space making them sound more “real”(Badcock, 2010). AVH patients
also showed increased structural connectivity in the left cingulated
bundle, which is part of the limbic system (Hubl et al., 2004;
Shergill et al., 2007). The increased connectivity between language-
related areas may lead to an abnormal hyperactivation of the circuit
which processes external speech, increasing noise in the speech pro-
cessing system and lowering the threshold for the intrusion of aber-
rant auditory perceptual input (Rotarska-Jagiela et al., 2009).
Additionally, a functional connectivity study showed that schizo-
phrenic patients with AVH had poor functional integration between
anterior cingulate cortex (ACC) and STG (Mechelli et al., 2007). The
authors claim that this network underlies the evaluation of speech
source (Mechelli et al., 2007). The aberrant activation of the neural
correlates of speech perception without the regulation of the ACC
might partially contribute to the formation of hallucinations via defi-
cient source monitoring of inner speech. Moreover, increased struc-
tural connectivity within the temporo-frontal network might result
in increased spreading of activation in the speech network, introduc-
ing noise and increasing excitability of the system (Rotarska-Jagiela et
al., 2009), which, in addition to the poor functional integration in this
network, might further contribute to abnormal perception. It is im-
portant to note that abnormal fluctuations in the BOLD signal can
also be detected at resting state in patients with schizophrenia
(Garrity et al., 2007), and it has been proposed that there is spontane-
ous activity in auditory sensory areas which might form the basis of
auditory perception in the absence of external stimuli (Hunter et al.,
In conclusion, AVH and EPC in schizophrenia seem to be based on
overlapping neural networks, in which the STG seems to play a pivot-
al role. Interestingly, targeting the STG with TMS has been shown to
reduce the severity of AVH (Aleman, Sommer, & Kahn, 2007), sug-
gesting a causal involvement of this structure in hallucinations. Addi-
tionally, a combined fMRI and TMS study found that even when the
BOLD response during hallucinations appear to be distributed in a
network comprising the left and right inferior frontal gyri and the
left superior temporal gyrus, only TMS applied on the left superior
temporal gyrus ameliorated the AVH (Hoffman et al., 2007). The au-
thors concluded that this area plays a critical role in the genesis of
AVH (Hoffman et al., 2007). Additional evidence demonstrated that
patients with a history of AVH have reduced gray matter density in
the STG (Garcia-Marti et al., 2008; Nenadic et al., 2010) suggesting
L. Alba-Ferrara et al. / Clinical Psychology Review 32 (2012) 244–250
that this structure is constitutively involved in the generation of hal-
lucinations. Additionally, there is evidence of abnormal structural and
functional connectivity of STG with frontal areas in AVH patients
which might come on top of the gray matter abnormalities of this
area. It is important to note that numerous findings have associated
this structure not just with AVH and prosodic processing but also
with a variety of cognitive domains, including audiovisual integration,
theory of mind and speech processing. Within the variety of neural
networks the STG is temporally coupled to (Hein & Knight, 2008),
for our model we will focus on the cases in which it interacts with
the EPC and AVH networks.
5. Towards a new neuropsychological model of AVH
Some AVH seem to be triggered by external sounds and there is
some supplementary evidence indicating that inaccurate perception
of prosodic features of external sounds, such as timbre, amplitude,
and timing, might contribute to the formation of AVH. Along these
lines, a case study has shown that false perceptions may derive
from misinterpretation of real sounds as exemplify in the case of a pa-
tient who heard a real engine sound and parallelly perceived a voice
with “mechanical timbre” (the voice sounded “like a machine”)
(Hunter & Woodruff, 2004). In this case, acoustical features of the
AVH were already present in an original environmental sound
(Hunter & Woodruff, 2004) and features corresponding to the timbre
of sounds seem to be misprocessed in a way that triggers false per-
ceptions. We suggest that this primary sensory processing impair-
ment plays a necessary role in false perception, but it is not
sufficient to form hallucinations per se.
While some AVH appear to be triggered by an external sound,
other AVH appear to be generated intrinsically and in the absence of
external stimuli. At the neurophysiological level, it has been shown
at resting state there is spontaneous activity in the primary auditory
cortex, superior temporal gyrus (STG), and anterior cingulate cortex
(ACC) in healthy populations (Hunter et al., 2006). Such spontaneous
activity establishes the possibility of this circuitry being involved in
perception when external stimuli are absent. It has been proposed
that disruption in the physiological modulation of this network at
resting state, or some defect in the intrinsic functional connectivity
of this network, could contribute to an enhanced sensitivity of the
primary auditory cortex, which might lead to an increased sensitivity
to irrelevant (auditory) signals, and thus to hallucinatory processes
(Hunter et al., 2006). Considering that the primary auditory cortex
has been shown to be prone to spontaneous activity, the existence
of external stimulation might not be necessary for AVH and thus
AVH might additionally be purely intrinsically generated. Thus, we
hypothesize that such spontaneous fluctuation in the network
might trigger the perception of AVH in absence of external stimuli
in some cases, while in other cases it might lowers the excitability
threshold facilitating neural firing in the presence of external stimuli.
Regardless whether auditory stimuli are internally or externally
generated, they are integrated into a common percept after sensory
evaluation. Evidence suggests that the STG is the neural substrate of
this integration process in the healthy population (Leitman et al.,
2008) and it has been shown that STG, a pivotal structure underlying
EPC (Hoekert, Bais, Kahn, & Aleman, 2008; Mitchell et al., 2004), is
also active during AVH (Stephane, Barton, & Boutros, 2001;
Woodruff et al., 1997). The posterior section of STG in the left hemi-
sphere is considered to be the location of Wernicke's area, the neural
substrate of speech comprehension. Indeed, it may be the multifari-
ous associations of the STG with numerous brain regions that explain
why this structure is the focus of overlap between EPC and AVH.
Functional connectivity analyses and DTI techniques have shown
that STG is connected with auditory primary cortex, medial ventral
frontal cortex, prefrontal cortex, ACC, and amygdala (Hunter et al.,
2006; Mechelli et al., 2007).
Furthermore, the STG also forms part of an anatomically con-
nected triadic network which also includes the amygdala and orbito-
frontal cortices (Ghashghaei & Barbas, 2002). The amygdala may
contribute to EPC specifically for the valences of fear and anger, and
these two emotional valences are probably the most frequent affec-
tive tone of AVH. The amygdala receives inputs from the prefrontal
cortex which regulates its activity via afferents suppressing amygdala
output (Rosenkranz & Grace, 2001), but this amygdala regulation by
prefrontal cortex is disrupted in schizophrenia (Leitman et al.,
2008). Therefore, in schizophrenia, prefrontal circuitry may fail to
down-regulate amygdala activity, which might therefore drive atten-
tion towards certain features of prosody, particularly negative tones,
coincidently with the emotional valence of most of the AVH that pa-
tients suffer from. The amygdala thus lacks prefrontal inhibitory con-
trol and becomes hyperresponsive, i.e., it fails to suppress this
stimulus-driven (bottom-up) process. In combination, the inefficient
top-down control of the amygdala, and dysfunction of bottom-up
processes (sensorial misperception) may account for the mechanism
underlying the relationship between AVH and EPC in schizophrenia.
Amygdala disinhibition increases emotional reactivity (Siever, 2008)
and consequently biases attention towards threatening stimuli,
which ultimately causes abnormal emotion processing.
Finally, we suggest that a final element of the network mediating
the contribution of EPC to AVH is the abnormal connectivity between
ACC and STG. Evidence suggests that this abnormal connectivity
causes difficulty judging whether a stimulus was internally or exter-
nally generated (Erkwoh et al., 2006), thus leading to misattribution
of inner auditory objects such as inner speech.
It should be noted that the proposed model also has some limita-
tions and some aspects require further exploration and research.
Moreover, the present model does not claim that the impaired mech-
anisms found in AVH patients and specifically EPC deficits are suffi-
cient to produce hallucinations, nor can it explain the full
phenomenology of AVH. Instead, our aim has been to draw attention
to the association between EPC deficits and hallucinations which have
so far been neglected in the literature. The present model does not in-
validate previous cognitive models of AVH which have been useful to
at explain certain phenomenological aspects of AVH. For example,
Badcock (2010) model can elegantly explain why AVH are perceived
in external auditory space. Additionally, memory frameworks can ex-
plain the content and derogatory tone of auditory hallucinations in
those patients with traumatic experiences, although such experiences
do not appear in all patients suffering from AVH. Our model should
thus be seen as complementing previous models, and filling some
gaps in previous theoretical frameworks. Pointed out by Jones
(2008) different models may be needed to explain particular types
of hallucinations because the phenomenological diversity of halluci-
natory experiences is vast. The present model seeks to account for
the specific type of AVH that is most characteristic of schizophrenia
The neuropsychological model proposed here accounts for the di-
verse phenomenology of AVH, considering that different aberrant
processes may result in similar abnormal perceptions. We contribute
to previous literature by integrating phenomenological and behavior-
al aspects of AVH in an empirically verifiable neural model. Regard-
less of whether AVH are triggered by the misperception of external
sounds, by spontaneously generated intrinsic fluctuations in the audi-
tory system, or by a combination of both, hallucinations in schizo-
phrenia may occur at the stage of transition from primary sensory
processing regions to integrative regions such as STG. Deficits in per-
ception and integration of stimulus features may lead to EPC deficits
which contribute to the formation of AVH, for example, via voice
identity misidentification. Given that the right STG is involved in
L. Alba-Ferrara et al. / Clinical Psychology Review 32 (2012) 244–250
voice identity recognition and EPC, which are in turn associated with
AVH, future empirical research should focus on how the STG is func-
tionally and structurally altered in AVH patients and how these alter-
ations are linked to deficits that patients might present at the
behavioral level (such as prosody decoding and voice identity recog-
nition deficits). Moreover, this model opens the possibility to inter-
vene by training patients to withdraw attention from threatening
auditory stimuli, as it has been shown that such stimuli capture atten-
tion triggering the formation of AVH. Lastly, we propose to perform
an fMRI study in patients at the time they are actively hallucinating.
From such study, three different strands of information can be
extracted. a) Recent fMRI analyses show that it is possible to establish
correlation in the activity of two or more brain regions and to demon-
strate how the activity of one region is affected but the activity in an-
other characterizing not only co-activated brain regions but also
causal effects acting over time. Thus, such analysis could be applied
to identify the coupling of neuronal activity along the brain structures
pinpointed in the present AVH model. Such research would allow to
test how adequate is the model given the empirical data. b) The appli-
cation of this paradigm to non-clinical population of voice hearers
could demonstrate that hallucinations between this group and
schizophrenia patients not only differ in phenomenological aspects
but also in its neural underpinnings. c) A seed region could be created
based on the peak voxel during the AVH in schizophrenia patients.
This region could become the target of clinical interventions such as
the application of neurodisruptive techniques (i.e. TMS) which may
hopefully diminish AVH precursor processes in patients resistant to
the medication and thus reduce the human cost of the symptom.
The authors thank Simon McCarthy-Jones for his comments on an
earlier version of the manuscript. This work was supported by the Ex-
perimental Psychology Society awarded to Prof. David Milner.
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