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Brain (2000), 123, 2065–2076

Musical hallucinosis in acquired deafness


Phenomenology and brain substrate
T. D. Griffiths

Department of Neurology, Newcastle University, Correspondence to: Dr T. D. Griffiths, Department of


Newcastle-upon-Tyne and Wellcome Department of Physiological Sciences, Newcastle University Medical
Cognitive Neurology, Institute of Neurology, London, UK School, Newcastle-upon-Tyne NE2 4HH, UK
E-mail: t.d.griffiths@ncl.ac.uk

Summary
Six subjects with musical hallucinations following network distinct from the primary auditory cortex.
acquired deafness are described. The subjects all PET was carried out on the six subjects to identify
experienced the condition in the absence of any other areas where brain activity increased as a function of
features to suggest epilepsy or psychosis. I propose a the severity of the hallucination. In a group analysis,
neuropsychological model for the condition consistent no effect was demonstrated in the primary auditory
with detailed observation of the subjects’ cortices. Clusters of correlated activity were
phenomenology. The model is based on spontaneous demonstrated in the posterior temporal lobes, the right
activity within a cognitive module for the analysis of basal ganglia, the cerebellum and the inferior frontal
temporal pattern in segmented sound. Functional cortices. This network is similar to that previously
imaging was carried out to test the hypothesis that demonstrated during the normal perception and imagery
musical hallucinosis is due to activity within such a of patterned–segmented sound, and is consistent with
module, for which the neural substrate is a distributed the proposed neuropsychological and neural mechanism.

Keywords: music hallucination; deafness; functional imaging; PET

Abbreviations: HG ⫽ Heschl’s gyrus; PT ⫽ planum temporale

Introduction
Musical hallucinosis is a disorder of complex sound that are characterized by fundamental properties such as pitch
processing. Subjects perceive complex sound in the form of and onset time. These sounds are built into a high-level
music in the absence of an acoustic stimulus. As such, the pattern at the temporal level of hundreds of milliseconds.
phenomenon might be regarded as an example of mental Musical hallucinosis requires a mental representation of such
imagery, defined as ‘mental acts in which we seem to re- a high-level pattern. The mental representation might be
enact the experience of perceiving an object when the object based on the same neural mechanism as that active during
is no longer available’ (Halpern and Zatorre, 1999). Mental normal musical perception, although distinct mechanisms for
imagery is, however, usually less vivid than actual perception, musical perception and imagery are also possible. I use the
and is never attributed to an external process. Musical term ‘high-level’ to refer to structure over and above that in
hallucinosis may be associated with structural brain lesions, the individual units; in this sense the term might equally be
epilepsy or psychosis (for reviews, see Berrios, 1990; used to refer to tonal or atonal Western music or African or
Keshavan et al., 1992). However, it is most commonly seen Eastern music.
in subjects with moderate or severe acquired deafness, and Previous studies suggest that the processing of discrete
as such it may represent an auditory form of the Charles sounds depends on a neural substrate different from that used
Bonnet syndrome. This term is more commonly used to for the processing of high-level patterns formed by these
describe formed visual percepts in the absence of visual sounds. Several studies suggest that the processing of pitch
stimulation in subjects with peripheral visual loss (ffytche is related to the function of the human primary auditory
et al., 1998). This study addresses the basis for musical cortex in Heschl’s gyrus (Zatorre, 1988; Pantev et al., 1989;
hallucinosis in six subjects with acquired deafness. Griffiths et al., 1998), whilst the onset time of auditory
Musical hallucinosis is a disorder of the processing of the transients is accurately represented in the primary auditory
high-level pattern in sound. Music comprises discrete sounds cortex of animals (Phillips and Hall, 1990). Stimulation of
© Oxford University Press 2000
2066 T. D. Griffiths

the primary auditory cortex at operation is associated with member, whilst in Subject 5 there were two episodes of acute
the perception of simple noises or tones (Penfield and Perot, lateralized hearing loss following head injuries. The duration
1963). In contrast, the processing of musical patterns formed of symptomatic hearing loss varied between 5 and 40 years.
by individual sounds is related to a network of cortical areas Subjects 4 and 5 experienced accompanying tinnitus whilst
distinct from the primary auditory cortex. Melody is a pattern Subjects 2 and 4 had experienced rotatory vertigo (related to
of sound pitches, whilst rhythm is a pattern of the onset head movement in Subject 2, and in only the early history
times and durations of sounds. Studies of melody perception in Subject 4). No subject experienced a syndrome to suggest
demonstrate a predominantly right-sided network that Menière’s disease (fluctuating deafness, fluctuating tinnitus,
includes the planum temporale and frontal cortex (Zatorre fluctuating vertigo or aural fullness).
et al., 1994), whilst the involvement of the cerebellum and
basal ganglia has been emphasized in studies of rhythmic
processing (Penhune et al., 1998). Stimulation of the superior Case histories
temporal gyrus outside Heschl’s gyrus at operation can be The subjects perceived music in the absence of any musical
associated with the perception of music (Penfield and Perot, stimulus. Several of the subjects had initially thought that
1963). A study using atonal sequences without conventional actual music was playing, but all subjects subsequently
rhythm (Griffiths et al., 1999a) suggests the possibility of a attributed the experience to a problem with the brain or the
general role for superior temporal networks in the analysis ears (the nature of the percept did not change). Apart from
of patterns in segmented sound, rather than a specific role in low mood accompanying the experiences, which all of
the analysis of music. the subjects found distressing, no subject described any
This study is a test of the hypothesis that musical accompanying delusion. There was no description of
hallucinosis in subjects with acquired deafness is related to experiential features (Gloor, 1990) or generalized convulsions
activity within the neural network for the perception of high- in any subject. The abnormal auditory experiences were
level pattern in sound. The hypothesis makes predictions restricted to the musical domain in all of the subjects except
about the phenomenology of, and the brain substrate for, Subject 6, who also experienced auditory hallucinations in
musical hallucinosis. In terms of phenomenology, the the form of speech and environmental sounds. All of the
hypothesis predicts that subjects with musical hallucinosis subjects described an experience of continuous or near-
due to acquired deafness will experience normal high-level continuous musical hallucinations and described variation in
sound patterns because of activation of the normal central the severity of their symptoms over the course of the day
perceptual mechanism. In terms of brain substrate, the (which was an inclusion criterion for the study). There was
hypothesis predicts that musical hallucinosis will be no historical suggestion in any of the subjects of any
associated with activity in distributed networks, distinct from accompanying difficulty with the perception of music, speech
the primary auditory cortex, including the posterior superior or environmental sound over and above that due to the
temporal cortex, frontal cortex and cerebellum. I was deafness; I did not feel that any of the subjects had an
particularly interested to examine whether the planum apperceptive auditory agnosia (Griffiths et al., 1999b). One
temporale is active during musical hallucinosis. Several of the subjects (Subject 1) had noticed a small decrease in
studies suggest a general role for this area in the perception symptoms with the consistent use of a hearing aid. None of
of patterned–segmented sound (Binder et al., 1996; Mummery the other subjects, all of whom had used amplification
et al., 1999). devices, felt that these had any effect on the severity of the
experience.

Patients and methods


Table 1 gives the clinical details for the subjects, all of whom Subject 1
were initially referred to neurologists with the exception of This subject, with 5 years of symptomatic hearing loss, has
Subject 5, who was initially referred for a psychiatric opinion. been reported previously as a single case (Griffiths et al.,
All subjects gave informed consent to take part in this study, 1997). He had a history of ⬍1 year of continuous musical
which was conducted with the approval of the ethical hallucinations in the form of multiple singers singing familiar
committee of the National Hospital for Neurology and melodies with indistinguishable lyrics. The onset was abrupt
Neurosurgery (London). and not related to any other symptoms. The songs included
hymns and rugby songs, and recent popular music.

ENT symptoms/audiometry
All subjects had moderate or severe bilateral deafness, as Subject 2
assessed by pure-tone audiometry (Fig. 1). All subjects This subject, with approximately 40 years of symptomatic
suffered progressive hearing loss. No subject had a family hearing loss, had a history of 3 years of continuous musical
history of deafness. In Subject 2 the symptomatic onset hallucinations. The onset was abrupt and was not
occurred when the subject was working as a tank crew accompanied by other neurological symptoms. The songs
Musical hallucinosis 2067

Table 1 Subject details


Subject Age Sex Hand* Musical† Index Vascular Symptomatic Measured Tinnitus Vertigo Lateralizing Structural EEG
event disease deafness deafness‡ neurological imaging
(dB ISO) signs

1 73 M 6/6 R No No Stable ⬍5 yr bilateral 51 No No No MRI normal Normal


angina
2 71 M 6/6 R No No HT Noise damage 1950s 53 No Occasional No MRI signal
(tank crew) then with head change in
progressive bilateral movement white matter
loss cerebral
hemispheres
3 78 F 6/6 R No No HT Progressive 95 No No No MRI normal Normal
bilateral loss
⬎40 yr
4 58 F 6/6 R No No No risk 23 yr progressive 82 Yes Yes during No MRI normal No specific
bilateral loss early abnormality
deafness
5 65 M 6/6 R No Head injuries No risk L deafness after after 105 Yes No No MRI signal Minor
aged 15, 57 factors head injury at age 15 yr change in slowing
63 yr R deafness after head hemispheric
injury aged 57 yr, then white matter/
bilateral progression pons
6 82 F 6/6 R No Posterior Single stroke Progressive bilateral, 69 No No No R occipital Normal
circulation without risk 15 yr lobe cyst on
stroke aged factors CT
79 yr

*Handedness on six-point Annett scale (Annett, 1970); †defined as passing a grade examination in any musical instrument; ‡mean hearing level (dB ISO) for the two ears
measured at intervals of 1 octave from 250 Hz to 8 kHz. HT, hypertension.

included light operatic pieces, and popular songs by artists Subject 5


including Shirley Bassey and Boyzone. This subject, with more than 40 years of progressive deafness,
had a history of 2 years of continual musical hallucinations
in the form of three or four male singers singing familiar
Subject 3 songs with accompanying musical instruments. The onset
This subject, with 40 years of symptomatic hearing loss, followed shortly after a head injury, and was accompanied
had a history of 9 years of almost continuous musical by hearing a localized noise behind his head and experiencing
hallucinations. The onset was abrupt and not accompanied a hot feeling that rose up the back of his head on two
by other symptoms. The experience would usually take the occasions only. There were no accompanying experiential
form of organ or piano music, which might be accompanied features or depression of his conscious level. The songs
by singers. If accompanied by singers, the lyrics would be usually dated from before the 1970s, when the patient lost
distinguishable. The songs included hymns, nursery rhymes interest in listening to music. He finds the sound of actual
and old popular songs. music distorted.

Subject 4
This subject, with 23 years of symptomatic hearing loss, had Subject 6
a history of more than 10 years of almost continuous musical This subject, with 15 years of progressive deafness, had a
hallucinosis. The onset of the hallucinations was not abrupt. history of less than 3 years of continual musical hallucinations.
The experience was different from that of the other subjects The onset of the events was coincident with an episode when
in that she did not hear instruments or singers but experienced she developed loss of vision, disorientation, perplexion,
musical hallucinations in which the individual notes had slurring of her speech and unsteadiness of body; this is likely
the quality of a buzzy pitch. In psychoacoustic terms her to have been a posterior circulation vascular event. She would
experience would be equivalent to hearing notes with pitch, hear one or more singers and accompanying music in the
where the individual pitches were associated with band-pass form of a piano or band. Unlike the five other subjects, she
noise with different passbands. Her experience had evolved also experienced environmental sound hallucinations and
from almost continuous tinnitus with similar characteristics verbal hallucinations. The environmental sound hallucinations
to the buzzy pitches experienced as music. She currently included wartime planes and sirens, and the sound of dogs
chooses not to listen to actual music because it is so distorted barking and children crying. The verbal hallucinations
at the level she needs to listen. included hearing indistinguishable sounds similar to the
2068 T. D. Griffiths

Fig. 1 Pure-tone audiograms.

murmuring of a crowd and the sound of her sisters talking Functional imaging
to each other. The voices never talked about her or to her. Functional imaging was carried out using PET to measure
She also experienced palinacousis; she described several regional cerebral blood flow as a measure of local cerebral
prolonged hallucinations in the form of hymns triggered by activity. A parametric design was used to demonstrate areas
listening to the television programme ‘Songs of Praise’. of the brain where activity varied as a function of the reported
severity of the hallucinosis (Silbersweig et al., 1995; Griffiths
et al., 1997). For each subject, 12 PET scans were performed
on a Siemens scanner with 3D acquisition using the
Structural imaging intravenous oxygen 15 water bolus technique to estimate
All subjects underwent structural imaging using MRI regional cerebral blood flow. Twelve acquisitions were
(Subjects 1–5) or CT (Subject 6). No subject demonstrated performed in two separate blocks of six that were 12 h apart.
loss of grey or white matter volume. MRI of Subjects 2 and This was in order to maximize the differences in symptom
4 demonstrated multiple areas of signal change in the deep severity corresponding to the scans. Before the onset of each
white matter of the cerebral hemispheres consistent with scan, the subjects were told that a scan was about to be
small vessel disease (Subject 2, Fig. 2). Subject 6 had a large carried out and asked to close their eyes. At the end of each
arachnoid cyst in the right occipital lobe (Fig. 2). scan they were told that the scan had finished and asked to
Musical hallucinosis 2069

Fig. 2 Structural imaging of Subjects 2 and 6. MRI of Subject 2 (left) shows multiple vascular lesions
in the hemispheric deep white matter. CT scan of Subject 6 (right) shows a large arachnoid cyst in the
right occipital lobe.

give a rating, between 1 and 7, of the severity of musical and 2, who had the least severe hearing loss (~50 dB),
symptoms during the scan. A rating of 1 corresponded to no experienced contemporary tunes. In a single scan for one
perception of music and 7 to the most severe experience subject, the reported experience was of music without a
ever. Subjects also reported the features of the experience recognizable tune, although it had similar characteristics to
after each scan in response to structured questions, as shown other pieces heard during scanning. All of the subjects, except
in Table 2. There was no output task during the scan. Subject 4, heard singers during their imaging, with or without
PET image processing and statistical analysis were carried distinct lyrics. Four of the subjects heard distinct or indistinct
out using statistical parametric mapping software (SPM99b, instruments.
http//:www.fil.ion.ucl.ac.uk/spm). Scans were realigned and
spatially normalized (Friston et al., 1995) to the standard
stereotaxic space of Talairach and Tournoux (Talairach and PET study to demonstrate areas of activity
Tournoux, 1988). The data were smoothed with a Gaussian correlated with hallucinosis
filter (filter width at half maximum, 16 mm). Analysis of Individual analyses were carried out on each of the six
covariance was used to correct for differences in global blood subjects except Subject 5, who failed to show any variation
flow between the scans and to implement individual and in the severity of the hallucinations over the course of the
group regression analyses to find areas where blood flow experiment. In Subjects 1–4, the analyses were carried out
increased with symptom severity. The significance of this on realigned, normalized and smoothed data. In Subject 6
regression was assessed with the t statistic at each voxel. the analysis was carried out on realigned and smoothed data,
These statistics (after transformation to a Z score) constitute because of the markedly abnormal brain structure. The
a SPM{Z}. individual analyses were carried out primarily to seek
activation in the primary auditory cortex in Heschl’s gyrus
(HG) as a linear function of hallucinosis strength, taking HG
Results as the a priori region of interest. The centre of mass of
Systematic study of phenomenology HG from the probabilistic map of Penhune and colleagues
Systematic interrogation of the subjects every 8 min over the (Penhune et al., 1996) (left coordinates –45, –20, 8; right
course of the PET experiment yielded the features reported coordinates 45, –15, 5) was used to define the centre of a
in Table 2. All of the subjects showed variation in the severity spherical volume of interest within HG of diameter 1 cm.
of the hallucinosis except for Subject 5, in whom the severity Within this volume, two subjects showed significant activation
was fixed. All subjects reported hearing normal patterns of at the P ⬍ 0.05 voxel level with correction for the size of
pitch and rhythm that formed recognizable tunes consistent the volume of interest: Subject 2 for the left HG (P ⬍ 0.001
with their listening experience and interests. Only Subjects 1 corrected voxel level) and Subject 3 for the right HG
2070 T. D. Griffiths

Table 2 Phenomenology
Scan Score Tune/artist Instrument Singer Distinct lyrics

Subject 1
1 3 ‘Football’s coming home’ No Several male No
2 3 ‘Football’s coming home’ No Several male No
3 2 ‘Football’s coming home’ No Several male No
4 2 ‘Football’s coming home’ No Several male No
5 2 ‘Football’s coming home’ No Several male No
6 2 ‘Football’s coming home’ No Several male No
7 4 ‘Football’s coming home’ No Several male No
8 4 ‘Football’s coming home’ No Several male No
9 4 ‘Football’s coming home’ No Several male No
10 5 ‘Football’s coming home’ No Several male No
11 5 ‘Football’s coming home’ No Several male No
12 4 ‘Football’s coming home’ No Several male No

Subject 2
1 7 ‘What can I do?’, Corrs No Several female Yes
2 7 ‘24 hours from Tulsa’ No One male Yes
3 7 ‘I’ll take you home, Kathleen’ No Single male Yes
4 7 ‘You are my heart’s delight’ Piano Single male Yes
5 7 ‘Edelweiss’ Orchestra 2 female Yes
6 7 ‘Maria’ Guitar 1 male Yes
7 1 No music No No No
8 2 Unrecognized tune Orchestra No No
9 1 No music No No No
10 1 No music No No No
11 4 ‘Sweatheart’ No 1 male/1 female Yes
12 1 No music No No No

Subject 3
1 5 ‘While shepherds’ Organ 1 male/1 female Yes
2 4 ‘While shepherds’ Organ 1 male/1 female Yes
3 6 ‘Poor old Joe’ Organ 1 male Yes
4 7 ‘While shepherds’ Organ No No
5 6 ‘All things bright’ Organ No No
6 7 ‘All things bright’ Organ Several Yes
7 7 ‘Daisy, daisy’ Organ Single male Yes
8 7 ‘Daisy, daisy’ Organ Single male Yes
9 7 ‘Stand up for Jesus’ Organ Single male Yes
10 7 ‘Auld Lang Syne’ Organ 1 male/1 female Yes
11 7 ‘Auld Lang Syne’ Organ 1 male/1 female Yes
12 7 ‘Daisy, daisy’ Organ 1 male/1 female Yes

Subject 4
1 2 ‘Oh my beloved father’ Buzzy pitch No No
2 3 French Christmas carol Buzzy pitch No No
3 3 French Christmas carol Buzzy pitch No No
4 2 ‘Sweet Caroline’, Diamond Buzzy pitch No No
5 3 ‘Pomp and circumstance’ Buzzy pitch No No
6 4 The trout Buzzy pitch No No
7 3 ‘Sound of music’ medley Buzzy pitch No No
8 5 ‘Doe a deer’ Buzzy pitch No No
9 5 ‘Doe a deer’ Buzzy pitch No No
10 5 ‘Doe a deer’ Buzzy pitch No No
11 5 ‘Doe a deer’ Buzzy pitch No No
12 5 ‘Doe a deer’ Buzzy pitch No No

Subject 5
1 5 ‘Che sera sera’ Band Yes several Yes
2 5 ‘Lilly Marlene’ Band Yes several Yes
3 5 ‘Hey there’ Band Yes several Yes
4 5 ‘Runaway train’ Band Yes several Yes
5 5 ‘Three caballros’ Band Yes several Yes
Musical hallucinosis 2071

Table 2 Continued
Scan Score Tune/artist Instrument Singer Distinct lyrics

Subject 5
6 5 ‘Danny boy’ Band Yes several Yes
7 5 ‘When you’re in love’ Band Yes, 4 Yes
8 5 Irish national anthem Band Yes, large group Yes
9 5 ‘More than ever’ Band Yes Yes
10 5 ‘Yellow rose of Texas’ Band Yes Yes
11 5 ‘Lilly Marlene’ Band Yes Yes
12 5 ‘Lilly Marlene’ Band Yes Yes

Subject 6
1 3 ‘Don’t laugh at me ’cause I’m a fool’ Band Yes, several Yes
2 5 ‘Moonlight and roses’ Band Yes, several Yes
3 5 ‘Dreaming’ Piano Yes, several Yes
4 5 ‘Just a rose in a garden of weeds’ Band Yes, several Yes
5 6 ‘Just a rose in a garden of weeds’ Band Yes, several Yes
6 6 ‘Pal of my cradle days’ Piano Yes, several Yes
7 7 ‘Just a rose in a garden of weeds’ Band Yes, several Yes
8 7 ‘Don’t laugh at me ‘cause I’m a fool’ Piano Yes, several Yes
9 7 ‘Just a rose in a garden of weeds’ Band Yes, several Yes
10 7 ‘Just a rose in a garden of weeds’ Band Yes, several Yes
11 7 ‘Good night Vienna’ Piano Yes, several Yes
12 7 ‘Good night Vienna’ Band Yes, several Yes

(P ⬍ 0.005 corrected voxel level). Analysis was also carried P ⬍ 0.05, corrected voxel level). The activation in each
out on the individual data sets to seek activation as a function planum temporale (Fig. 4) formed part of a cluster extending
of hallucinosis strength in the planum temporale (PT) as a on to the lateral surface of the posterior superior temporal
region of a priori interest. The centre of mass of the PT gyrus, as shown in Fig. 3. In the whole-brain analysis,
from the probabilistic map of Westbury and colleagues without taking any prior hypotheses into account (Table 3
(Westbury et al., 1999) (left coordinates –60, –30, 10; right and Figs 3 and 4), significant clusters of activation were
coordinates 65, –30, 10) was used to define the centre of a demonstrated in the right basal ganglia and right frontal
spherical volume of interest within the PT of diameter 1 cm. operculum, the posterior temporal lobes (especially the right),
Three subjects showed significant activation within this both lobes of the cerebellum, the left deep sylvian cortex
volume at the P ⬍ 0.05 voxel level with correction for the and the left frontal lobe.
size of the volume of interest. Significant activation was
demonstrated in the three subjects as follows: Subject 1 (left
PT, P ⬍ 0.05 corrected); Subject 2 (right PT, P ⬍ 0.05 Discussion
corrected); Subject 3 (right PT, P ⬍ 0.005 corrected). In this study I observed the detailed phenomenology of
Group analysis was carried out for Subjects 1–4 (Table 3 musical hallucinosis in six patients with acquired deafness.
and Figs 3 and 4). Subject 5 was excluded from the analysis The subjects all had musical hallucinations that occurred
because of lack of variation in the severity of hallucinosis, after the onset of deafness in the absence of features to
and Subject 6 was excluded from the analysis because of suggest psychosis or epilepsy. Based on the phenomenology,
markedly abnormal brain structure. The group analysis was I will argue for a model for the production of musical
carried out to demonstrate the typical behaviour of the group. hallucinations in such patients based on activity within a
Formally, this represents a fixed-effects analysis. The four common mechanism for the perception of pattern in
subjects’ similar experiences during scanning, age, segmented sound. The functional imaging data suggest a
handedness and musicality justify such an analysis. No neural substrate for this common mechanism.
activation as a function of hallucinosis strength was
demonstrated in HG on either side in the group analysis.
Using the same volume-of-interest method for HG as in the Model
individual analyses, no activation was shown at the P ⬍ 0.05 Figure 5 shows a model for the normal and abnormal
level with correction for the size of the volume. Using the perception of patterned–segmented sound. This is a cognitive
same method for PT as in the individual analyses, significant neuropsychological model (Ellis and Young, 1988) based on
activation as a function of hallucinosis strength was shown modular psychological mechanisms, although I will also
in the left and right plana temporale (left P ⬍ 0.005, right argue for the likely neural substrate for its implementation.
2072 T. D. Griffiths

Table 3 Functional imaging (areas of significant activation Fig. 5, between the perception/imagery module and encoding/
as a linear function of hallucinosis intensity): group recognition modules.
analysis for Subjects 1–4 The model predicts first that musical hallucinosis due to
Region Coordinates (mm) Z score acquired deafness will be associated with the perception of
normal temporal patterns within segmented sound that are
x y z consistent with the subject’s previous experience. This is the
case in all six subjects observed. In the model, this is the
Right basal ganglia 24 –10 2 5.45
(putamen/globus pallidus) 28 –8 –6 4.77 result of the interaction between the perception/imagery and
16 –10 0 4.55 recognition modules, the latter accessing patterns encoded
Right frontal 54 12 –4 4.15 during previous listening experience. All of the subjects
56 12 0 4.09 experienced music that had been heard before they developed
36 8 –6 4.07 severe deafness, and it is notable that Subjects 1 and 2, who
Left sylvian fissure –40 –24 24 5.24 had experienced more contemporary music, have less severe
–34 –14 24 4.77 hearing loss than the others. In the subjects with the most
–34 –20 14 3.69 marked hearing loss (Subjects 4 and 5), there was a disparity
between the normal experience of old tunes during
Right posterior temporal 72 –38 –16 5.07 hallucinosis and the distorted perception of actual music; this
74 –38 –8 4.62
is entirely consistent with the model. Subject 4 is of particular
Left cerebellum –42 –82 –24 4.66 interest with respect to her normal perception of temporal
–44 –82 –36 4.31 pattern during hallucinosis. She perceives normal temporal
–32 –78 –28 4.23 patterns of pitch, although the individual pitches are not
associated with normal musical notes. This is consistent with
Right cerebellum 16 –54 –32 4.43
22 –62 –26 3.65 distinct mechanisms for the processing of the features of
24 –70 –22 3.44 individual sounds compared with the processing of higher-
level patterns formed by these sounds. Essentially, I am
Left frontal lobe –32 16 34 4.25 arguing in her case that abnormal activity in the module for
–50 28 32 3.71 the perception of individual sounds can have a normal higher-
–38 20 40 3.70
–20 36 2 4.23 order structure imposed by the perception/imagery module.
Some studies of tinnitus (Lockwood et al., 1998) suggest
Left posterior temporal lobe –62 –38 4 4.02 low-level activity in the individual sound module (which, I
–70 –44 8 3.88 have argued, is the primary auditory cortex), whereas others
–60 –30 0 3.69 suggest more distributed high-level processing (Giraud et al.,
Clusters demonstrating significant activation as a linear function 1999). This difference might reflect whether the tinnitus has
of hallucinosis intensity at the P ⬍ 0.05 level (corrected for associated high-level temporal or spatial structure associated
multiple comparisons using Gaussian field theory) are shown. The with it.
three most significant maxima within each cluster are shown, Secondly, the model allows for the ‘triggering’ of activity in
except for the large cluster involving the right basal ganglia and
frontal cortex, where six local maxima are shown.
the perception/imagery module by the impoverished auditory
input. For some sounds the low signal-to-noise ratio in such
input might lead to misperception and misrecognition of
certain incoming sounds as music followed by mental
During normal listening to patterned–segmented sounds ‘amplification’ due to the positive feedback loop between
such as music, the auditory input is processed by two the perception/imagery and recognition modules. The model
perceptual mechanisms, operating in a hierarchical fashion also allows for the triggering of activity in the perception/
(Fig. 5, top). The perceptual mechanism for individual sounds imagery module by any abnormal activity from the module for
operates before that for the perception of the pattern formed the perception of individual sounds. Gordon has particularly
by these sounds. After the pattern has been perceived, it is stressed the possible contribution of early parts of the auditory
encoded into memory. The model is based on a single module pathway to musical hallucinations (Gordon, 1994). I would
being active during both the perception and the imagery of point out here only that the proposed model does not require
patterned sound. In acquired deafness there is impoverished the ascending auditory system to represent a true musical
normal input to this module. I propose that this allows pattern to produce the phenomenon of musical hallucinosis.
spontaneous activity within the module (Fig. 5, bottom). I Triggered activity would also provide a mechanism for the
also propose that the recognition system for patterned sound phenomenon of palinacousis seen in Subject 6.
can interact strongly and reciprocally with the perception/ Two questions arise immediately from the model. First,
imagery module in the absence of normal processing activity the model is based on the processing of patterned sound
in the latter. This may produce positive feedback, represented rather than music per se. The question arises of why the
by the bold arrows in both directions in the lower part of subjects do not usually perceive other forms of patterned–
Musical hallucinosis 2073

Fig. 3 Functional imaging (correlated activity with hallucination strength surface reading). PET group
analysis for Subjects 1–4 showing areas where regional cerebral blood flow increased as a linear
function of hallucinosis intensity. The functional data shown were thresholded at the P ⬍ 0.001
(uncorrected) voxel level and rendered on to an MRI surface template with the same degree of
smoothing as the PET data.

segmented sound, such as speech. Speech, like music, perceived speech with accentuated pattern or prosody in the
contains a high-level structure at the level of hundreds of form of singing. Previous studies in a broader population,
milliseconds, called prosody or the ‘melody of language’ including subjects with psychiatric disorders, epilepsy and
(Monrad-Krohn, 1947). Speech, unlike music, is also structural lesions (Berrios, 1990), have also reported verbal
characterized by spectral and temporal complexity within the hallucinations in subjects with musical hallucinations. As in
segmented sounds (in terms of temporal structure, at the level the present study, associated auditory verbal hallucinations
of milliseconds and tens of milliseconds). The production of in the form of spoken speech were found only in a minority
verbal hallucinosis in this model would therefore require of subjects. A second question is why all subjects with
additional abnormal activity in the module for the perception acquired deafness of the degree shown by these subjects do
of individual sounds, as well as in that for the perception of not experience musical hallucinosis, if this is due to the
higher-order pattern. This is possible within the model, activity of a normal module cut off from its normal input?
although less likely. Only one of the six subjects in this study This might reflect differences between subjects in a threshold
also suffered verbal hallucinations in the form of spoken for spontaneous or triggered activity within the perception/
speech, although in 41 of the 72 scans observed the subjects imagery module.
2074 T. D. Griffiths

Fig. 4 Functional imaging. (Top) PET group analysis for Subjects 1–4 showing areas where regional
cerebral blood flow increased as a linear function of hallucinosis intensity (no sound stimulus). The data
shown were rendered on to an axial section of the mean T1-weighted MRI for the four subjects.
(Bottom) For comparison, data for the activation during the normal perception of patterned–segmented
sound in nine normal subjects (Griffiths et al., 1999a) are shown superimposed on an axial section at
the same level. Both sections are at the vertical level z ⫽ 0 mm. A line at y ⫽ –30 mm corresponds to
the anteroposterior maximum for the planum temporale (Westbury et al., 1999). Notice the bilateral
activation in the region of the planum temporale in both analyses.

Fig. 5 (Top) The processes occurring during the normal perception of pattern in segmented sound.
(Bottom) The proposed basis for musical hallucinations, due to spontaneous activity in the module for
the perception and imagery of pattern in segmented sound.
Musical hallucinosis 2075

Model implementation The role of central lesions


In terms of the neural mechanisms that might underlie this The role of central lesions in producing musical hallucinations
model, I argued earlier that the perception of the features of has been the subject of controversy. Although gross structural
individual sounds involved neural mechanisms at or close to lesions in the brainstem or either hemisphere can be associated
the primary auditory cortex in HG, whilst the perception of with musical hallucinosis (Tanabe et al., 1986; Paquier et al.,
higher order patterns formed by such sounds involved more 1992; Inzelberg et al., 1993; Murata et al., 1994) such lesions
widely distributed mechanisms, including the planum are not seen in most patients with this condition. In the
temporale. A prediction of the model is therefore that present study, one subject had a large structural anomaly
increasing intensity of hallucinosis with increasing (arachnoid cyst), of uncertain relevance, in addition to a
spontaneous activity in the module for pattern perception major-territory vascular event. Two other subjects had
will be associated with increasing activation in a network multiple vascular lesions affecting the white matter, whilst
distinct from HG, including the planum temporale. The group two others had vascular risk factors (in addition to age)
analysis has demonstrated that the typical behaviour of the without demonstrated lesions on MRI.
group is to show such increasing activation with increasing Central vascular lesions might be the additional factor that
hallucinosis strength in the planum temporale. The typical distinguishes subjects with musical hallucinosis from subjects
behaviour of the group is not to show such activation in HG, with the same degree of deafness without hallucinosis. Several
although it was shown in one or other HG in two of the mechanisms are possible. First, it is possible that diffuse
individual analyses. vascular disease might lead to a degree of disconnection
A striking feature of this study is the similarity of the between the primary auditory and association cortices. In
activation produced by musical hallucinosis when there is such a way the input to the perception/imagery module might
perception without input and the perception of actual be more diminished in the group with vascular disease. A
patterned–segmented sound in controls (Fig. 4). This is second possibility is that a vascular lesion or lesions within
consistent with the proposed model. However, the perception the network for the perception and imagery of segmented
of actual patterned–segmented sound also leads invariably to sound alters the threshold for spontaneous activity within
activation in the primary auditory cortex, something that has this network. I favour the second mechanism, as the
not been demonstrated in this study of hallucinosis. The distributed nature of the network would make it more likely
analysis of hallucinating patients is not consistent with the to be affected by a stochastic process such as small vessel
primary auditory cortex being a sufficient substrate for higher- disease. Moreover, the second mechanism involves a network
order pattern perception. The model in Fig. 5 does not make that includes deep brain structures, which are more likely to
strong predictions about activation in the module for the be affected by small vessel disease than the superior temporal
perception of individual sounds in hallucinosis, but this could cortex. For either mechanism, vascular disease would act as
occur with descending excitation from the pattern-perception a factor to augment the suggested process in the model
module to the module for the perception of individual sounds. dependent on peripheral deafness. Such vascular disease
If this were the mechanism, the present data suggest that would not be an adequate explanation in itself.
such feedback activation is not universal.
Activation in a cortical network including the right planum
Conclusion
temporale has been shown in previous studies of the basis
I have proposed a model for the production of musical
of musical perception (Zatorre et al., 1994). Moreover, studies
hallucinations in subjects with acquired deafness in the
of musical imagery have demonstrated a network similar to
absence of psychosis or epilepsy. This model is based on
that for perception (Zatorre et al., 1996; Halpern and Zatorre,
spontaneous activity in a module usually involved in the
1999), which supports the common mechanism for musical
normal perception of pattern in segmented sounds. Functional
perception and imagery proposed in this model. This network
imaging data support the hypothesis that such a module is
includes predominantly the right auditory association cortex
physically realized in a distributed cortical network distinct
(including the planum temporale) and the right and left
from the primary auditory cortices.
frontal cortices.
All of the subjects considered here found the experience
The model I propose is based on activity within a module
of musical hallucinations distressing and requested treatment.
for the perception and imagery of pattern within segmented
Only one subject benefited from any treatment, in the form
sound rather than music per se. Imaging studies that
of improved amplification. I recommend that subjects within
incorporate a task which demands imagery of simple auditory
this group are assessed by an audiology service to decide if
patterns (Rao et al., 1997; Penhune et al., 1998) have also
improved amplification may be of benefit, but in general the
demonstrated activation of the right planum temporale in the
prognosis for improving the condition is poor.
absence of activity in the primary auditory cortex. This is
consistent with the activation of the planum temporale in the
current study being a mechanism for the perception and Acknowledgements
imagery of patterned–segmented sound, the primary auditory I wish to thank the patients, many of whom travelled long
cortex having an obligatory role in perception only. distances to undergo detailed assessment and scanning, the
2076 T. D. Griffiths

referring clinicians (R. Brenner, D. Burn, M. Jackson, J. Lockwood AH, Salvi RJ, Coad ML, Towsley ML, Wack DS,
Palace, S. Pereira, P. Reading, J. Spillane, B. Toone, R. Murphy BW. The functional neuroanatomy of tinnitus: evidence for
Wise), members of the Neurootology Department, National limbic system links and neural plasticity. Neurology 1998; 50:
Hospital for Neurology, Queen Square and the Department 114–20.
of Audiology, Kings College Hospital for carrying out the Monrad-Krohn GH. Dysprosody or altered ‘melody of language’.
audiograms, the radiographers at the Wellcome Department Brain 1947; 70: 405–15.
of Cognitive Neurology for expert technical assistance, and Mummery CJ, Ashburner J, Scott SK, Wise RJ. Functional
R. S. J. Frackowiak for helpful comments. I am supported neuroimaging of speech perception in six normal and two aphasic
by the Wellcome Trust (UK). subjects. J Acoust Soc Am 1999; 106: 449–57.
Murata S, Naritomi H, Sawada T. Musical auditory hallucinations
caused by a brainstem lesion. Neurology 1994; 44: 156–8.
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