Chem. Senses 27: 407-416,
2002
© Oxford University Press 2002
Ratings of Different Olfactory Judgements in Schizophrenia
Neuroscience and Sensory Systems, Claude-Bernard University (UMR CNRS 5020), 50, Avenue Tony Garnier, F-69007 Lyon Cedex 07, France 1 Psychopathology and Neurobiology of Schizophrenia and Psychosis Vulnerability (EA 3092), Claude-Bernard University, Hôpital du Vinatier, 95, Boulevard Pinel, Bron-Lyon, F-69677, France 2 INSERM U534, 16 Avenue Lépine, Bron-Lyon, F-69676, France
Correspondence to be sent to: J. Hudry, Neuroscience and Sensory Systems (UMR CNRS 5020), Université Claude-Bernard Lyon 1, 50, Avenue Tony Garnier, 69366 Lyon Cedex 07, France. e-mail: hudry{at}olfac.univ-lyon1.fr
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Abstract |
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We assessed the influence of schizophrenia on different olfactory tasks. Forty patients with schizophrenia (20 males and 20 females) and 40 control subjects (20 males and 20 females) were tested. The experiment included two sessions. Initially, 12 odorants were presented at a rate of one per minute. The subjects were asked to rate intensity, pleasantness, familiarity and edibility for each odour using linear rating scales. The odorants were then presented a second time and the subjects were asked to identify them. The results showed that the scores for pleasantness, familiarity, edibility and identification but not intensity were disturbed in patients when compared with control subjects. Furthermore, the familiarity judgement of male patients was more often deficient than that of female patients and they rated odorants as being inedible when the women judged them as neutral. Considered together, these data show that our olfactory test may be used in patients with schizophrenia for evidencing various dysfunctions specific to different types of olfactory processing that represent steps in the odour name identification process.
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Olfactory dysfunction in patients with schizophrenia has been the subject of an increasing number of studies. With a few exceptions (Campbell and Gregson, 1972
;
Bradley, 1984) olfactory
deficits in schizophrenia have been reported in odour detection
(Gross-Isseroff et al.,
1987; Kopala et al.,
1989,
1992;
Geddes et al., 1991),
similarity judgement and discrimination
(Gregson and Fearnley, 1974;
Malaspina et al.,
1994), recognition memory (Wu
et al., 1993), identification (Kopala et al.,
1989,
1992,
1994;
Hurwitz and Clark, 1990;
Kopala and Clark, 1990;
Serby et al., 1990;
Seidman et al., 1992;
Wu et al., 1993;
Houlihan et al.,
1994; Stedman and Clair,
1998) and naming (Saoud et
al., 1998).
Deficits in odour identification have been found to be more common in men
than in women (Kopala et al.,
1992), more marked in post-menopausal than in pre-menopausal women
with schizophrenia (Kopala et
al., 1995) and closely linked to illness duration
(Moberg et al.,
1997b). Thus, independently of the normal ageing effect and
cognitive deficit, elderly patients with schizophrenia displayed a greater
magnitude of olfactory deficit than younger patients and this effect was not
related to medication (Serby et
al., 1990; Kopala et
al., 1992). Conducting a meta-analytic review of the English
language literature on olfaction in schizophrenia, Moberg et al.
found no significant influence of medication status or smoking on differential
deficits across the domains of detection threshold sensitivity,
discrimination, memory and identification. They concluded that their findings
support the hypothesis of a primary dysfunction in the olfactory system
(Moberg et al.,
1999).
Using the University of Pennsylvania's Smell Identification Test (UPSIT),
Moberg et al. found pronounced deficits in patients with Alzheimer's
disease as well as in elderly patients with schizophrenia
(Moberg et al.,
1997a). They suggested that, since performance on an odour
identification test did not discriminate between these two disorders, similar
pathological processes in olfactory brain regions might be involved. In a
recent study that investigated patients with Alzheimer's disease we proposed
an original test that allowed us to assess different olfactory judgements in
addition to the classic olfactory identification test
(Royet et al.,
2001a). Taking into account cognitive psychology concepts
(Craik and Lockhart, 1972;
Craik and Tulving, 1975;
Schab, 1991; Kosslyn and
Koenig, 1992) we suggested that subjects assessed intensity, familiarity,
pleasantness and edibility before identifying odours (Royet et al.,
1999,
2000a,b,
2001b). We then showed that
patients with Alzheimer's disease presented lower familiarity and
identification scores than age-matched control subjects. In contrast, no
difference was observed between either group of subjects for intensity,
pleasantness and edibility judgements.
The aim of the present study was to examine, for the first time, the
influence of schizophrenia on the performance of these alternative olfactory
judgement tasks. The test was divided into two sessions: a first one in which
intensity, pleasantness, familiarity and edibility judgements were rated for
several odorants and a second one in which the subjects were additionally
asked to identify these odorants. Intensity, pleasantness, familiarity and
edibility were successively assessed using linear rating scales. A list of
five alternative odour names was proposed for the identification task. We
postulated that, in addition to the well-documented impairment in identifying
the odours, more specific deficits could be observed in the various olfactory
judgements. Knowing that schizophrenia patients commonly present a disturbed
experience of pleasure (Becker et
al., 1993; Brewer et
al., 1996) we could also presume that these patients would
display an impaired pleasantness judgement
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Methods |
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Subjects
Forty schizophrenia patients (20 males and 20 females) and 40 control
subjects (20 males and 20 females) participated in this experiment
(Table 1). All patients were
recruited from the Vinatier Hospital in Lyon, France and met the criteria of
the fourth edition of the Diagnostic and Statistical Manual of Mental
Disorders (DSM-IV) for schizophrenia
(American Psychiatric Association,
1994). They were clinically stable with no change in medication
for at least 1 month before the study. The control subjects were group matched
in age and gender to the schizophrenia patients. The experiments were
conducted on fully informed subjects who had given their written consent.
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Psychiatric diagnoses were established on the basis of the Schedule for
Affective Disorders and Schizophrenia (SADS)
(Fyer et al., 1985)
and a review of medical records. The SADS was used for selecting healthy
comparison subjects who were confirmed to have neither current DSM-IV Axis I
psychiatric disorder or schizophrenia spectrum personality disorder. The
Positive and Negative Syndrome Scale (PANSS)
(Kay et al., 1987)
was also used for assessing psychopathology in patients
(Table 1). Furthermore, no
comparison subject had any family history of psychopathology as assessed by
family research diagnostic criteria
(Endicott et al.,
1975). The exclusion criteria for all subjects included possible
brain damage, major medical problems, current substance abuse, lithium
medication, known anosmia or a current cold.
Stimuli
A set of 12 odorants (Table
2) was chosen from 185 odorants previously evaluated by a large
number of control subjects (Royet et
al., 1999). The odours were recognized as rather familiar,
but either strong or weak, either pleasant or unpleasant and either edible or
inedible. Seven odorants were furnished by Givaudan-Roure (France) or
International Flavor and Fragrances (France) and were mixtures of odorants
(lemon, lavender, citronella, strawberry, mint, pine and smoked salmon). The
other five (mushroom, clove, ether, vinegar and gas) were obtained from simple
chemical compounds (1-octen-3-ol, eugenol, diethyl ether, acetic acid and
tetrahydrothiophene respectively) and were provided by manufacturers of
chemical products (Aldrich or Sigma, France).
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The odorous products were contained in 15 ml yellow glass jars with screw lids in polypropylene (Fisher, Erlancourt, France). The jars were opaque in order to mask any visual cues as to identity. The odorants were diluted in mineral oil to prepare 5 ml of odorous solution (1%) and absorbed by compressed filaments of polypropylene. Because tetrahydrothiophene, acetic acid and ether released a very strong odour they were diluted 1000 times. The odorants were kept in a refrigerator when not in use and were removed before the experiment began and left to reach room temperature.
Experimental procedure
The whole experiment included two sessions that were separated by an
interval of a few minutes. Before the first session, the subjects were only
given instructions concerning the tasks to be performed immediately. The
experimenter then presented 12 odorants to the subjects at a rate of one per
minute, with each odorant being presented for 
5 s. The subjects were
asked to rate the intensity, pleasantness, familiarity and edibility of each
odorant in order using linear 5 cm rating scales that were regularly segmented
and numbered from 1 to 10. In order to indicate further the degree of
judgement demanded, the extremities were marked `very weak and `very strong',
`very unpleasant' and `very pleasant', `very unfamiliar' and `very familiar'
and `very inedible' and `very edible' for intensity, pleasantness, familiarity
and edibility respectively. The four linear rating scales were presented on
the same page for each odorant. The subjects were not allowed to adjust their
previous ratings while making a current judgement.
The same 12 odorants were presented again in the same order in the second
session and with the same inter-stimulus interval as in the first session. The
subjects had to choose one name for each odorant presented among a written
list of five alternative proposals that comprised the veridical label, one
name evoking a similar odour and three names evoking more distinct odours,
either edible or not (Table 2).
The presentation order of the odorants was the same for all subjects for both
sessions. Each session lasted 12 min and the entire test lasted 30
min.
Quantitative and statistical analyses
The scores obtained for intensity, pleasantness, familiarity and edibility
were directly deduced from the value selected on the rating scales for each
odour by each subject. The odour identification scores were determined by
attributing the value 1 to a response when a subject selected the veridical
label and the value 0 to that response when they selected one out of the four
other alternative names indicated in Table
2. We chose to code the five alternative choices simply as correct
or incorrect responses instead of distributing the responses into the
categories of veridical label, near miss and far miss
(Rabin and Cain, 1984;
Lyman and McDaniel, 1984)
because we felt that extracting near misses from incorrect responses could
give redundant information with those processed in the four other tasks of
olfactory judgement, particularly that of the edibility judgement. In the
frame of our hypotheses emanating from cognitive psychology
(Royet et al., 1999),
the intensity, hedonicity, familiarity and edibility judgements represent
different categories of odour processing, all of which contribute to the
identification process.
The intensity, pleasantness, familiarity and edibility judgements and odour
identification were considered as being different olfactory tasks involving
different olfactory processing. However, it has previously been shown that
there is a significant correlation between these tasks
(Henion, 1971;
Doty et al., 1984;
Distel et al., 1999;
Royet et al., 1999).
Therefore multivariate analysis of variance (MANOVA) with group (patient
versus control), gender (male versus female) and judgement type (intensity,
hedonicity, familiarity, edibility and identification) was performed with
repeated measurements on the odorant factor. Three-way analyses of variance
(ANOVA) (group x gender x odorants) with repeated measurements
(Winer, 1962) were then used
for separately analysing the scores relative to the different olfactory
judgement tasks. The differences between groups of means were assessed by
multiple orthogonal contrasts. The normality of the samples and the
homogeneity of their variance were controlled with the Lilliefors
(Conover, 1971) and the
Hartley (Winer, 1962) tests
respectively.
The relationships between olfactory performances and the demographic or clinical characteristics of the schizophrenia patients were assessed using Spearman correlations. They were performed on the results observed for each odour judgement task, for age, for PANSS positive and PANSS negative performances, duration of illness and for the educational level of the schizophrenia patients.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Olfactory performances
All subjects provided the required ratings so that no data were missing.
The arithmetic means of the scores obtained for intensity, pleasantness,
familiarity, edibility and identification were computed as a function of the
subject groups (schizophrenia versus control), of gender (male versus female)
and of the 12 odorants (Figure
1). The results of the MANOVA showed a significant effect of the
group [Wilks' 
(11,370) = 5.982 and P < 0.0001] and
judgement factors [Wilks' (44,1417) = 23.705 and P <
0.0001], but not the sex factor [Wilks' (11,370) = 1.314 and
non-significant]. Significant interactions between the group and judgement
[Wilks' (44,1417) = 2.090 and P < 0.0001] and group and
gender factors [Wilks' (11,370) = 3.025 and P < 0.0007],
but not between the sex and judgement [Wilks' (44,1417) = 1.180 and
non-significant] and group, gender and judgement factors [Wilks'
(44,1417) = 1.274 and non-significant] were also observed. A
Bonferroni test showed significant differences between the different olfactory
tasks (intensity, hedonicity, familiarity, edibility and identification)
compared by pair (P < 0.05 at least). Univariate tests with
three-way ANOVAs were then performed for these five olfactory tasks.
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We observed that only the odorant factor had a significant effect for the intensity judgements [F(11,836) = 27.74 and P < 0.0005]. The ANOVA for the pleasantness judgements revealed that the odorant factor had a significant effect [F(11,836) = 52.17 and P < 0.001] and that there were significant interactions (P < 0.05 at least) between three factors (group x gender x odorant). Multiple orthogonal comparisons of the means showed that the pleasantness performances were significantly lower in the schizophrenia patients than in the control subjects for both genders. The ANOVA for the familiarity judgements revealed a significant effect of the group [F(1,76) = 14.29 and P < 0.0005] and odorant [F(11,836) = 16.83 and P < 0.0005] factors and a significant interaction between these two factors [F(11,836) = 2.54 and P < 0.005]. Multiple orthogonal comparisons showed that the familiarity scores were significantly lower in the male than in the female schizophrenia patients [F(1,76) = 5.29 and P < 0.025] and also significantly lower in the male schizophrenia patients than in the male control subjects [F(1,76) = 15.86 and P < 0.0005]. The ANOVA revealed a significant effect of the odorant [F(11,836) = 42.92 and P < 0.0005] factor and a significant interaction between the group and gender [F(1,76) = 7.75 and P < 0.005] and the group and odorant factors [F(11,836) = 2.80 and P < 0.0005] for the edibility judgements. Multiple orthogonal comparisons showed that the edibility scores were significantly lower in the male than in the female schizophrenia patients [F(1,76) = 9.01 and P < 0.005] and significantly less contrasted in the male schizophrenia patients than in the male control subjects [F(1,76) = 5.76 and P < 0.025]. The ANOVA revealed a significant effect of the group [F(11,836) = 28.68 and P < 0.0005] and odorant factors [F(11,836) = 6.07 and P < 0.0005] and a significant interaction between the three factors [F(11,836) = 1.95 and P < 0.05] for the identification scores. Multiple orthogonal comparisons showed that the identification scores were significantly lower in the male and female schizophrenia patients as compared with their respective control groups [F(1,76) = 17.96 and P < 0.005 and F(1,76) = 11.13 and P < 0.001 respectively]. The identification scores of the male and female patients within the schizophrenia group were not significantly different [F(1,76) = 0.293 and non-significant] and those seen in the male and female subjects within the control group were also not significantly different [F(1,76) = 2.081 and non-significant].
The percentages of the schizophrenia patient performances were further
rated in comparison to those of the control subjects. The mean scores for the
12 odorants were directly computed for the schizophrenia and control groups as
a function of gender for the intensity, familiarity and identification tasks
(Table 3). Differences between
the performances observed in the schizophrenia patients and control subjects
were then calculated for each odorant and expressed as a percentage of the
control group performance. The percentages were indirectly calculated after
normalization of the data for the pleasantness and edibility judgements. Given
that the pleasantness judgement is a bipolar dimension, from unpleasant to
neutral and from neutral to pleasant
(Moskowitz and Barbe, 1976;
Doty, 1991), the calculation
of the mean scores for the 12 odorants could suppress differences between the
groups. The pleasantness data were therefore standardized into normalized
scores by computing the deviation of each score (absolute value) relative to
the middle score (value 5). We applied the following empirical formula:
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Demographic and clinical variables and olfactory performances
The mean age and educational level of the subjects were compared as a function of the group (schizophrenia versus control) and gender factors (male versus female) with two-way ANOVAs. The analysis did not show any significant effect for both variables of group factor [age, F(1,76) = 0.01 and non-significant and education, F(1,76) = 2.90 and non-significant] and gender factor [age, F(1,76) = 3.74 and non-significant and education, F(1,76) = 0.51 and non-significant] or any significant interaction between the two factors [age, F(1,76) = 0.08 and non-significant and education, F(1,76) = 2.58 and non-significant]. PANSS negative and PANSS positive scores, duration of illness and education levels were compared between the male and female schizophrenia patients. No significant difference was noted between either sex as a function of PANSS negative scores [F(1,38) = 0.03 and non-significant], PANSS positive scores [F(1,38) = 1.04 and non-significant] and duration of illness [F(1,38) = 0.242 and non-significant].
With regard to the within-group correlations between the demographic/clinical variables and olfactory scores, Spearman correlations only revealed a few significant associations between the olfactory scores and demographic and clinical variables. We mainly found weak but significant correlations between the intensity scores and the PANSS positive scores (r = 0.097 and P = 0.034) and between the familiarity scores and the PANSS positive and negative scores (r = -0.108 and P = 0.018 and r = 0.096 and P = 0.036 respectively).
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Olfactory performances in schizophrenia
The present study highlighted the influence of schizophrenia on different
odour processing. It showed that the pleasantness, familiarity and edibility
judgements and also odour identification but not the intensity judgement were
differentially affected in the schizophrenia subjects when compared with the
control subjects. Thus, although it has previously been shown that there is
correlation between these olfactory tasks
(Henion, 1971;
Doty et al., 1984;
Distel et al., 1999;
Royet et al., 1999),
they can underlie different odour processing and, as a consequence, involve
different olfactory neural networks. Since deficits of odour identification in
schizophrenia have largely been reported in the literature (Kopala et
al., 1989,
1992,
1994;
Hurwitz and Clark, 1990;
Kopala and Clark, 1990;
Serby et al., 1990;
Seidman et al., 1992;
Wu et al., 1993;
Houlihan et al.,
1994), the deficits observed in the present study for olfactory
pleasantness, familiarity and edibility judgements are demonstrated for the
first time. However, at a recent congress Moberg et al. also
described impairment of odour hedonics in patients with schizophrenia
(Moberg et al.,
2001). Moreover, in a previous work
(Royet et al., 2001a)
we claimed that familiarity judgement can represent long-term recognition
memory because familiarity feelings are closely related to experience and
necessarily involve remote information. From this assumption, our results are
coherent with data established in an earlier study
(Wu et al., 1993)
demonstrating that medicated or never-medicated schizophrenia patients
performed worse than control subjects on an odour match-to-sample test.
A performance decrease in pleasantness judgement can be related to physical
anhedonia, a well-known schizophrenia symptom corresponding to a `disturbed
experience of pleasure, i.e. a gradual loss of the ability to feel
emotionally moved, or to experience physical or psychic pleasure'
(Becker et al., 1993).
Conversely to their expectations, these authors
(Becker et al., 1993)
could not prove this relation between anhedonia and pleasantness rating in
psychosisprone subjects. However, it is worth noting that these authors only
used one odour.
It does not appear that the schizophrenia patients linked the edibility judgement to the pleasantness one, since several odorants (lemon, lavender and smoked salmon) actually gave totally different edibility and pleasantness scores. Thus, both the schizophrenia patients and control subjects could judge an odorant as pleasant, although inedible (e.g. lavender and citronella). However, this dysfunction in edibility judgement can be linked to that found for familiarity judgement. The loss of familiarity judgement ability, which was mainly in the male schizophrenia patients, could lead them to consider odorants as being inedible. In other words, an unknown odorant could not be correctly judged edible or inedible, but could just be perceived as inedible.
The current study furthermore showed a clear dissociation between the
olfactory performances of the male and female schizophrenia patients in their
familiarity and edibility judgements. Thus, these performances for familiarity
judgement mainly revealed score decreases in the males but not the females
when compared with those of control subjects of the same gender (23.4 and 8.2%
respectively). Although such ratio differences were not observed for the
edibility judgement (due to its bipolar dimension), the analyses also proved
lower edibility scores in the males than in the females. This also supports
P.J. Moberg's (personal communication) observations showing that male but not
female patients also modified their pleasantness ratings. The gender
differences found in the present study were not related to age, since both
groups were age matched. In contrast, they could be related to Kopala's
studies indicating that the deficit in odour identification was more marked in
male than in female patients and more marked in post- than pre-menopausal
women with schizophrenia (Kopala et al.,
1989,
1992,
1995). These authors suggested
the involvement of a mechanism related to sex hormones such as oestrogen that
could play a protective role in schizophrenia females. They emphasized the
higher concentrations of oestrogen receptors in the amygdala, hippocampus and
orbitofrontal cortex, which are all structures involved in olfaction and which
are found to be abnormal in post-mortem studies of schizophrenia patients.
However, several other studies did not show such gender differences using an
odour identification test (Houlihan et
al., 1994; Malaspina
et al., 1994; Moberg et al.,
1997a,b;
Seidman et al.,
1997). We suggest that these gender differences, which are not
systematically observed, are due to a dysfunction in brain areas in male
patients. These areas participate in familiarity and edibility judgements that
are supposed to be steps in the odour name identification process. Finally, we
showed that the identification scores were inversely related to the duration
of illness and age. The identification scores were lower when the illness
duration was increased, thus corroborating previously reported results
(Moberg et al.,
1997b). The identification performances were also lower in the
oldest schizophrenia patients. However, this last relationship is rather
tentative and explains why this data has not been previously published.
Schizophrenia and neural networks involved in odour processing
No histochemical or morphological abnormalities of the olfactory epithelium
were observed in an immunohistochemical analysis of post-mortem olfactory
tissues removed from schizophrenia patients
(Smutzer et al.,
1998). The olfactory bulb volume has been found to be smaller in
schizophrenia patients than in comparison subjects, but no correlation between
the olfactory bulb volume and odour threshold sensitivity was observed in
patients (Turetsky et al.,
2000). Thus, any olfactory deficits observed in schizophrenia were
likely to present a central origin. There is indeed a growing body of evidence
suggesting that schizophrenia is a neurobehavioural disorder resulting partly
from brain temporolimbic dysfunctions
(Fuster, 1989; Arnold et
al., 1991,
1997,
1998;
Seidman et al., 1995;
Moberg et al., 1999).
The limbic system is a well-known region of olfactory projection in mammals
(Shipley and Reyes, 1991) and
damage to this system in schizophrenia could explain a reduction in
performance with pleasantness and familiarity judgements. The amygdala is
considered to be the key structure in emotion
(LeDoux, 1987) and cerebral
imaging of healthy subjects has for instance revealed an increased amygdalian
regional cerebral blood flow in response to both pleasant and unpleasant
odours (Zald and Pardo, 1997;
Royet et al., 2000b).
We have also recently shown that pleasantness scores are significantly reduced
in epileptic patients whose seizures originate in the amygdala and the
hippocampus (Hudry et al.,
1999). Finally, the left temporal lobe volume has recently been
shown to be significantly smaller in male schizophrenia patients than in male
comparison subjects (Bryant et
al., 1999). These data are consistent with our own recent
findings obtained from cerebral imaging, which has shown strong lateralization
of the emotional processing of odours, i.e. that in healthy subjects the left
hemisphere was clearly activated (Royet
et al., 2000b).
It is usually hypothesized that aspects of schizophrenic symptomatology can
reflect differential expressions of the disorder in two partially independent
frontal subcortical regions: the left dorsolateral and the right ventral
prefrontal systems (Seidman et
al., 1992; Brewer et
al., 1996; Purdon,
1998). The left dorsolateral part is reported to be involved in
executive functions (Weinberger et
al., 1986; Seidman et al., 1994), whereas the right
ventral part, that is the orbitofrontal cortex, is implicated in olfactory
processing (Jones-Gotman and Zatorre,
1988; Zatorre and
Jones-Gotman, 1991; Zatorre
et al., 1992). However, there appears to be discrepancies
since two recent studies concluded that odour identification ability might be
associated with the function of the dorsolateral prefrontal cortex
(Brewer et al., 1996;
Saoud et al.,
1998).
Only a few studies have used cerebral imaging in patients with
schizophrenia (Clark et al.,
1991; Wu et al.,
1993; Bertollo et al.,
1996; Malaspina et
al., 1998). They indicated lower rates of metabolism relative
to healthy controls in the frontal lobe and more particularly in the inferior
frontal gyrus or the orbitofrontal cortex. Such a hypometabolism could explain
olfactory deficits in schizophrenia, but unfortunately no olfactory
performances were measured in patients by these authors during imaging scans.
However, it has recently been demonstrated that the pattern of activation in
the right and left orbitofrontal cortices of healthy subjects varies depending
on whether odour processing is related to familiarity or pleasantness
judgements (Zald and Pardo,
1997; Zald et al.,
1998; Royet et al.,
1999,
2000a,
b,
2001b). The right
orbitofrontal cortex activity was highest during the familiarity judgement,
whereas the left orbitofrontal cortex activity increased significantly during
the pleasantness judgement. We would like to suggest that the lower metabolism
observed in these areas in patients with schizophrenia could explain the poor
olfactory performances observed in the present study for the familiarity and
pleasantness judgements.
Comparisons of data in patients with Alzheimer's disease and schizophrenia
Substantial olfactory deficits have been found in Alzheimer's disease and
schizophrenia in the domain of odour detection threshold sensitivity,
discrimination, memory and identification. However, a meta-analytic study of
the English language literature on olfactory dysfunction in schizophrenia did
not find differential deficits in these olfactory domains
(Moberg et al.,
1999). Neither was any difference found between either disease,
Alzheimer's disease and elderly schizophrenia using the UPSIT
(Moberg et al.,
1997a). In a previous study with Alzheimer's disease patients, we
showed deficits for familiarity judgement and the identification of odours,
but not for intensity, pleasantness and edibility judgements when their
performances were compared with those of control subjects matched in age
(Royet et al.,
2001a). In the present study we found deficits for the
familiarity, pleasantness and edibility judgements and odour identification.
Thus, even without further comparative statistical analysis, we can underline
the differences in olfactory performances found between Alzheimer's disease
and schizophrenia patients with our test for pleasantness and edibility
judgements. We can therefore conclude that the present olfactory test, as a
function of the olfactory judgements investigated, is suitable for
demonstrating differential deficits in olfactory functioning in Alzheimer's
disease and schizophrenia and for allowing us to evidence the involvement of
different neuronal circuits. Furthermore, this test could be sensitive enough
to differentiate schizotypic and at-risk groups and we feel that this may
deserve further investigation.
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Acknowledgments |
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We thank anonymous reviewers for substantial and helpful comments on a draft of this manuscript and are very grateful to W. Lipski for correcting the English language of the paper.
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References |
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|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
American Psychiatric Association (1994)DSM-IV: Diagnostic and Statistical Manual of Mental Disorders , 4th edn. Washington, DC, American Psychiatric Press.
Arnold, S.E., Hyman, B.T., Hoesen, G.W.V. and Damasio,
A.R. (1991) Some cytoarchitectural abnormalities of the
entorhinal cortex in schizophrenia. Arch. Gen. Psychiat.,48
, 625-632.
Arnold, S.E., Han, L.Y. and Ruscheinsky, D.D. (1997) Further evidence of cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia using spatial point pattern analyses. Biol. Psychiat., 42,639 -647.[Web of Science][Medline]
Arnold, S.E., Smutzer, G.S., Trojanowski, J.Q. and Moberg, P.J. (1998) Cellular and molecular neuropathology of the olfactory epithelium and central olfactory pathways in Alzheimer's disease and schizophrenia. Ann. NY Acad. Sci.,855 , 762-775.[Web of Science][Medline]
Becker, E., Hummel, T., Piel, E., Pauli, E., Kobal, G. and Hautzinger, M. (1993) Olfactory event-related potentials in psychosis-prone subjects. Int. J. Psychophysiol., 15,51 -58.[Web of Science][Medline]
Bertollo, D.N., Cowen, M.A. and Levy, A.V. (1996) Hypometabolism in olfactory cortical projection areas of male patients with schizophrenia: an initial positron emission tomography study. Psychiat. Res., 60,113 -116.[Web of Science][Medline]
Bradley, E.A. (1984) Olfactory acuity to a pheromonal substance and psychotic illness. Biol. Psychiat., 19,899 -905.[Web of Science][Medline]
Brewer, W.J., Edwards, J., Anderson, V., Robinson, T. and Pantalis, C. (1996) Neuropsychological, olfactory, and hygiene deficits in men with negative symptom schizophrenia. Biol. Psychiat., 40,1021 -1031.[Web of Science][Medline]
Bryant, N.L., Buchanan, R.W., Vladar, K., Breier, A. and
Rothman, M. (1999) Gender differences in temporal lobe
structures of patients with schizophrenia: a volumetric MRI study.Am. J. Psychiat.
, 156,603
-609.
Campbell, E.A. and Gregson, R.A. (1972) Olfactory short term memory in normal, schizophrenic and brain-damaged cases. Austr. J. Psychol., 24,179 -185.
Clark, C., Kopala, L., Hurwitz, T. and Li, D. (1991) Regional metabolism in microsmic patients with schizophrenia. Can. J. Psychol.,36 , 645-650.
Conover, W.J. (1971) Practical Nonparametric Statistics. John Wiley & Sons, New York.
Craik, F.I.M. and Lockhart, R.S. (1972) Levels of processing: a framework for memory research. J. Verbal Learn. Verbal Behav., 11,671 -684.
Craik, F.I.M. and Tulving, E. (1975) Depth of processing and the retention of words in episodic memory.J. Exp. Psychol. Gen. , 104,268 -294.[Web of Science]
Distel, H., Ayabe-Kanamura, S., Martínez-Gómez,
M., Schicker, I., Kobayakawa, T., Satio, S. and Hudson, R.
(1999) Perception of everyday odors—correlation between
intensity, familiarity and strength of hedonic judgement. Chem.
Senses, 24,191
-199.
Doty, R.L. (1991) Olfactory system. In Getchell, T.V., Doty, R.L., Bartoshuk, L.M., and Snow, J.B. (eds),Smell and Taste in Health and Disease . Raven Press, New York, pp. 175-203.
Doty, R.L., Shaman, P. and Dann, M. (1984) Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol. Behav., 32,489 -502.[Medline]
Endicott, J., Andreasen, N.C. and Spitzer, R.L. (1975) Family History Research Diagnostic Criteria. New York State Psychiatric Institute, New York.
Fuster, J. (1989) The Prefrontal Cortex, 2nd edn. Raven Press, New York.
Fyer, A.J., Endicott, J., Mannuzza, S. and Klein, D.F. (1985) Schedule for Affective Disorders and Schizophrenia—Lifetime Anxiety Version. New York State Psychiatric Institute, New York.
Geddes, J., Huws, R. and Pratt, P. (1991) Olfactory acuity in the positive and negative syndromes of schizophrenia. Biol. Psychiat.,29 , 774-778.[Web of Science][Medline]
Gregson, R.A.M. and Fearnley, H. (1974) Atypical relative similarity judgements in schizophrenia. Br. J. Soc. Clin. Psychol., 13,80 -90.[Web of Science][Medline]
Gross-Isseroff, R., Stoler, M., Ophir, D., Lancet, D. and Sirota, P. (1987) Olfactory sensitivity to androstenone in schizophrenic patients. Biol. Psychiat.22 , 922-925.[Web of Science][Medline]
Henion, K.E. (1971) Odor pleasantness and intensity: a single dimension? J. Exp. Psychol.,90 , 275-279.[Web of Science][Medline]
Houlihan, D.J., Flaum, M., Arnold, S.E., Keshavan, M. and Aliger, R. (1994) Further evidence for olfactory identification deficits in schizophrenia. Schizophr. Res.,12 , 179-182.[Web of Science][Medline]
Hudry, J., Ryvlin, P., Gervais, R., Mauguière, F. and Royet, J.P. (1999) Olfactory disturbances in refractory partial epilepsy. Epilepsia,40 , 266.
Hurwitz, T.A. and Clark, C. (1990) Olfactory functioning in schizophrenia and depression (letter).Biol. Psychiat. , 27,458 .[Web of Science]
Jones-Gotman, M. and Zatorre, R.J. (1988) Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia,26 , 387-400.[Web of Science][Medline]
Kay, S.R., Fiszbein, A. and Opler, L.A. (1987) The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophr. Bull.,13 , 261-276.
Kopala, L. and Clark, C. (1990) Implications of olfactory agnosia for understanding sex differences in schizophrenia. Schizophr. Bull.,16 , 255-261.
Kopala, L., Clark, C. and Hurwitz, T.A.
(1989) Sex differences in olfactory functioning
schizophrenia. Am. J. Psychiat.,146
, 1320-1322.
Kopala, L.C., Clark, C. and Hurwitz, T. (1992) Olfactory deficits in neuroleptic naive patients with schizophrenia. Schizophr. Res., 8,245 -250.
Kopala, L.C., Good, K.P. and Honer, W.G. (1994) Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders.Schizophr. Res. , 12,205 -211.[Web of Science][Medline]
Kopala, L.C., Good, K.P. and Honer, W.G. (1995) Olfactory identification ability in pre- and postmenopausal women with schizophrenia. Biol. Psychiat.,38 , 57-63.[Web of Science][Medline]
LeDoux, J.E. (1987) Emotion. In Plum, F. and Mountcastle, V.B. (eds), Handbook of Physiology. The Nervous System. American Physiological Society, Bethesda, MD, pp.419 -459.
Lyman, B.J. and McDaniel, M.A. (1984) Effects of encoding strategy on long-term memory for odours.Quart. J. Exp. Psychol. , 38A,753 -765.
Malaspina, D., Wray, A.D., Friedman, J.H., Amador, X., Yale, S.,
Hasan, A., Gorman, J.M. and Kaufmann, C.A. (1994)
Odor discrimination deficits in schizophrenia: association with eye
movement dysfunction. J. Neuropsychiat. Clin. Neurosci.,6
, 273-278.
Malaspina, D., Perera, G.M., Lignelli, A., Marshall, R.S., Esser, P.D., Storer, S., Furman, V., Wray, A.D., Coleman, E., Gorman, J.M. and Van Heertum, R.L. (1998) SPECT imaging of odor identification in schizophrenia. Psychiat. Res.: Neurolmaging Sect., 82,53 -61.
Moberg, P.J., Doty, R.L., Mahr, R.N., Mesholam, R.I., Arnold, S.E., Turetsky, B.I. and Gur, R.E. (1997a) Olfactory identification in elderly schizophrenia and Alzheimer's disease. Neurobiol. Aging, 18,163 -167.[Web of Science][Medline]
Moberg, P.J., Doty, R.L., Turetsky, B.I., Arnold, S.E., Mahr,
R.N., Gur, R.C., Bilker, W. and Gur, R.E. (1997b)
Olfactory identification deficits in schizophrenia: correlation with
duration of illness. Am. J. Psychiat.,154
, 1016-1018.
Moberg, P.J., Agrin, R., Gur, R.E., Gur, R.C., Turetsky, B.I. and Doty, R.L. (1999) Olfactory dysfunction in schizophrenia: a qualitative and quantitative review.Neuropsychopharmacology 21,325 -340.[Web of Science][Medline]
Moberg, P.J., Turetsky, B.I., Lourea, B.L., Doty, R.L., Gur, R.C. and Gur, R.E. (2001) Impairments of odor hedonics in patients with schizophrenia. Schizophr. Res.,49 , 115.
Moskowitz, H.R. and Barbe, C.D. (1976) Psychometric analysis of food aromas by profiling and multidimensional scaling. J. Food Sci., 41,567 -571.[Web of Science]
Purdon, S.F. (1998) Olfactory identification and Stroop interference converge in schizophrenia.J. Psychiat. Neurosci. , 23,163 -171.[Web of Science][Medline]
Rabin, M.D. and Cain, W.S. (1984) Odor recognition: familiarity, identifiability, and encoding consistency. J. Exp. Psychol. Learn. Mem. Cogn.,10 , 316-325.[Web of Science][Medline]
Royet, J.P., Koenig, O., Gregoire, M.C., Cinotti, L., Lavenne, F., Le Bars, D., Costes, N., Vigouroux, M., Farget, V., Sicard, G., Holley, A., Mauguière, F., Comar, D. and Froment, J.C. (1999) Functional anatomy of perceptual and semantic processing for odors. J. Cogn. Neurosci.,11 , 94-109.[Web of Science][Medline]
Royet, J.P., Hudry, J. and Vigouroux, M. (2000a) Application de l'imagerie cérébrale à l'etude de l'olfaction. In Christen, Y., Collet, L. and Droix-Lefaix, M.T. (eds), Rencontres IPSEN en ORL, Tome 4. Editions Irvinn, Paris, pp. 73-87.
Royet, J.P., Zald, D., Versace, R., Costes, N., Lavenne, F.,
Koenig, O. and Gervais, R. (2000b) Emotional
responses to pleasant and unpleasant olfactory, visual, and auditory stimuli:
a PET study. J. Neurosci., 20,7752
-7759.
Royet, J.P., Croisile, B., Williamson-Vasta, R., Hibert, O.,
Serclerat, D. and Guerin, J. (2001a) Rating of
different olfactory judgements in Alzheimer's disease. Chem.
Senses, 26,409
-417.
Royet, J.P., Hudry, J., Zald, D.H., Godinot, D., Gregoire, M.C., Costes, N., Lavenne, F. and Holley, A. (2001b) Functional neuroanatomy of different olfactory judgments.Neurolmage , 13,506 -519.
Saoud, M., Hueber, T., Mandran, H., Dalery, J. and d'Amato, T. (1998) Olfactory identification deficiency and WCST performance in men with schizophrenia. Psychiat. Res., 81,251 -257.[Web of Science][Medline]
Schab, F.R. (1991) Odor memory: taking stock. Psychol. Bull., 109,242 -251.[Web of Science][Medline]
Seidman, L.J., Talbot, N.L., Kalinowski, A.G., McCarley, R.W., Faraone, S.V., Kremen, W.S., Pepple, J.R. and Tsuang, M.T. (1992) Neuropsychological probes of fronto-limbic system dysfunction in schizophrenia. Olfactory identification and Wisconsin Card Sorting Performance. Schizophr. Res.,6 , 55-65.
Seidman, L.J., Yurgelun-Todd, D., Kremen, W.S., Wood, B.T., Goldstein, J.M., Faraone, S.V. and Tsuang, M.T. (1995) Relationship of prefrontal and temporal lobe MRI measures and neuropsychological performance in chronic schizophrenia. Biol. Psychiat., 35,235 -246.
Seidman, L.J., Goldstein, J.M., Goodman, J.M., Koren, D., Turner, W.M., Faraone, S.V. and Tsuang, M.T. (1997) Sex differences in olfactory identification and Wisconsin Card Sorting performance: relationship to attention and verbal ability. Biol. Psychiat., 42,104 -115.[Web of Science][Medline]
Serby, M., Larson, P. and Kalkstein, D. (1990) Olfactory sense in psychoses. Biol. Psychiat., 28,829 -830.[Web of Science][Medline]
Shipley, M. and Reyes, P. (1991) Anatomical of the human olfactory bulb and central olfactory pathways. In Laing, D.G., Doty, R.L. and Breipohl, W. (eds), The Human Sense of Smell. Springer-Verlag, Berlin, pp.29 -60.
Smutzer, G., Trojanowski, J.Q., Lee, V.M.H. and Arnold, S.E. (1998) Human olfactory mucosa in schizophrenia.Ann. Otol. Rhinol. Laryngol. , 107,349 -355.[Web of Science][Medline]
Stedman, T.J. and Clair, A.L. (1998) Neuropsychological, neurological and symptom correlates of impaired olfactory identification in schizophrenia. Schizophr. Res., 32,23 -30.[Web of Science][Medline]
Turetsky, B.I., Moberg, P.J., Yousem, D.M., Doty, R.L., Arnold,
S.E. and Gur, R.E. (2000) Reduced olfactory bulb
volume in patients with schizophrenia. Am. J. Psychiat.,157
, 828-830.
Weinberger, D.R., Berman, K. and Zec, R.F.
(1986) Physiologic dysfunction of dorsolateral prefrontal
cortex in schizophrenia: regional cerebral blood flow evidence.Arch. Gen. Psychiat.
, 43,114
-124.
Winer, B.J. (1962) Statistical Principles in Experimental Design. McGraw-Hill, New York.
Wu, J., Buschbaum, M.S., Moy, K., Denlea, N., Kesslak, P., Tseng, H., Plosnaj, D., Hetu, M., Potkin, S., Bracha, S. and Cotman, C. (1993) Olfactory memory in unmedicated schizophrenics. Schizophr. Res., 9,41 -47.[Web of Science][Medline]
Zald, D.H. and Pardo, J.V. (1997)
Emotion, olfaction, and the human amygdala: amygdala activation during
aversive olfactory stimulation. Proc. Natl Acad. Sci. USA,94
, 4119-4124.
Zald, D.H., Donndelinger, M.J. and Pardo, J.V. (1998) Elucidating dynamic brain interactions with across-subjects correlational analyses of positron emission tomographic data: the functional connectivity of the amygdala and orbitofrontal cortex during olfactory tasks. J. Cereb. Blood Flow Metab.,18 , 896-905.[Web of Science][Medline]
Zatorre, R.J. and Jones-Gotman, M. (1991) Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain,114 , 71-84.
Zatorre, R.J., Jones-Gotman, M., Evans, A.C. and Meyer, E. (1992) Functional localization and lateralization of human olfactory cortex. Nature,360 , 339-340.[Medline]
Accepted January 23, 2002
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