The Cognitive Basis of Disorganization

The Cognitive Basis of Disorganization
Symptomatology in Schizophrenia and Its
Clinical Correlates: Toward a Pathogenetic
Approach to Disorganization
by Marie'Christine Hardy'Bayle, Yves Sarfati, and Christine Passerieux
This article focuses on the schizophrenic disorganization syndrome, which was initially described by Bleuler
(who used the term "dissociation") as lying at the heart
of schizophrenia. While adopting a neo-BIeulerian
approach, we describe schizophrenic disorganization
using a pathogenetic hypothesis and a three-part structure. First, we discuss previous approaches to characterizing and defining schizophrenic disorganization,
providing arguments in favor of a complementary
approach to describing schizophrenic disorganization
that relies on a pathogenetic analysis of the disorganization syndrome, and especially thought and language
disorders. Second, we present two possible cognitive
pathophysiologica] mechanisms that may explain schizophrenic disorganization: (1) a deficit in the integration
of contextual information, based on the results of
semantic priming studies; and (2) a theory of mind
deficit, based on the results of studies of the attribution
of mental states to others. We propose a cognitive
model of schizophrenic dysfunctioning on the basis of
these two anomalies. Third, we summarize our published findings to examine the implications of these two
cognitive pathophysiological mechanisms for schizophrenic disorganization. On the basis of the same two
anomalies, we then propose and illustrate a neoBIeulerian approach to the assessment of communication disorders that is critical to the improvement of
schizophrenic disorganization's clinical description.
Keywords: Schizophrenia, disorganization,
semantic priming, contextual information, theory of
mind, communication disorders.
Schizophrenia Bulletin, 29(3):459-471,2003.
work on dementia praecox the subtitle "the group of schizophrenias" (Bleuler 1911). Throughout his work, he insists
on the fact that all the patients who develop this illness,
however different they may appear outwardly, suffer from
the same pervasive disruption of their mental processes.
Schizophrenia as an illness is therefore not defined clinically but in terms of a unique underlying morbid process
that he terms "Spaltung"—"a loosening of associations."
Although the term "schizophrenia" has been established
for nearly a century, the same is not true of the concept of
"loosening of associations."
However, it is clear that the mental dissociation
described by Bleuler is again being studied with increasing frequency and under new designations: formal thought
disorders, disorganization subtype, misconnection syndrome. A variety of studies conducted over the last decade
have undeniably reasserted the importance of mental dissociation by reaffirming both its existence and its relevance. On the one hand, it is becoming increasingly clear
that specific abnormalities in information processing, such
as thought and language disorders, are correlated with
indicators of the disorganization of the illness. On the
other hand, integrative approaches to schizophrenia propose that all the diverse signs and symptoms involved in
schizophrenia could be the result of disruptions in functional neural circuits and even go so far as to speak of neoBIeulerian models (Andreasen 1999).
We explicitly adhere to this neo-BIeulerian approach
and base our work on the postulate that the disorganization
syndrome is an important subject of study involving
pathophysiological mechanisms that it is vital to understand. This article consists of three parts: the first part
briefly looks at the different approaches previously used to
define schizophrenic disorganization; the second part pre-
The term "schizophrenia," which means "a mind that is
torn asunder" (Old Greek), was proposed by the Swiss
psychiatrist Eugen Bleuler, who gave his authoritative
Send reprint requests to Dr. Y. Sarfati, Centre Hospitalier de
Versailles, HSpital Mignot, Consultation de Psychiatrie et de
Psychologic 177, rue de Versailles, 78157 Le Cbesnay, France; e-mail:
[email protected].
Abstract
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Hardy-Baylg et al.
sents a cognitive approach to schizophrenic disorganization in terms of two cognitive anomalies that may explain
it; and the third part presents experimental evidence in
favor of this characterization and describes the implications of this approach for the clinical assessment of disorganization.
Defining Schizophrenic Disorganization:
Precedents
Disorganization Symptoms Within the Bleulerian
Description. Bleuler (1911) postulated that "mental dissociation" is the disorder that generates the illness of schizophrenia and from which all the symptoms of the illness derive
either directly or indirectly. The so-called primary symptoms, including thought disturbance, represent the most
direct clinical expression of mental dissociation. Thought
disturbance is also considered to be fundamental—that is, it
is both characteristic of and constant in schizophrenia.
Bleuler therefore attributes considerable importance to
thought and speech disorders. However, despite the importance of thought disturbance within both a pathogenetic and
a clinical perspective, Bleuler's approach to disorganization
may be considered confusing and vague: confusing because
thought disturbance is sometimes considered not as the
cause but as the consequence of affect disturbance, and
vague because the description of thought disturbance is
imprecise: "the relations between ideas lose solidity; they
can be replaced by others of whatever nature"; "the thought
process turns away from the normal paths that are acquired
by experience; thought is then so truncated that we speak of
dislocated thought and incoherence." The Bleulerian concept
of dissociation has often been criticized for a lack of objectivity and for leaving too much up to the subjective impressions of the clinical practitioner, thus causing a significant
level of diagnostic imprecision. These criticisms can be
explained by the fact that Bleuler chose to describe thought
disturbance in terms of an underlying theory of dissociation
rather than on the basis of a precise observation of clinical
indexes. The International Pilot Study on Schizophrenia confirmed the complexity covered by the term "mental dissociation" and the diagnostic expansion in which it has resulted
(WHO 1973). Fortified by these criticisms, research that
emerged in the 1970s, and especially the dimensional
approach, chose to employ a logic radically different from
Bleuler's: it was based on the most evident (objectivized)
and most operational (formalized) clinical indicators, while
doing without any underlying pathogenetic theory.
Disorganization Symptoms Within the Dimensional
Approach. The dimensional approach proposes that the
symptoms of schizophrenia tend to cluster together to
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constitute dimensions. The procedure used to assess the
different dimensions can be summed up as follows: the
clinical characteristics of the illness are precisely
described by instruments for assessing symptoms; several
factor analyses are then conducted across different samples to confirm the structure of the clinical dimensions in
schizophrenia. Many rating scales of schizophrenic symptoms and many factor analyses have been proposed during
the past 30 years, and this article will not exhaustively
examine all of them but instead show how the dimensional approach has contributed to the definition of schizophrenic disorganization.
The most frequently used instruments for assessing
symptoms are the Scale for the Assessment of Negative
Symptoms (SANS) (Andreasen 1983), the Scale for the
Assessment of Positive Symptoms (SAPS) (Andreasen
1984), and the Positive and Negative Syndrome Scale
(PANSS) (Kay et al. 1987). Factor analytic studies conducted using the SAPS, the SANS, and the PANSS have
demonstrated the existence of a disorganization dimension
that has become the object of attention because it has been
shown to be strongly reproducible across many studies
(Peralta and Cuesta 2001). The symptoms that most commonly tend to cluster together to constitute the disorganization dimension are positive formal thought
disorders (pressure of speech, tangentiality, derailment,
incoherence, illogicality), poverty of content of speech,
bizarre behavior, alogia, inappropriate affect (item from
the SAPS and SANS), conceptual disorganization, difficulty in abstract thinking, poor attention, unusual
thoughts, disturbance of volition, stereotypic thinking,
poor insight, and mannerism (items from the PANSS)
(Bell et al. 1994; Lindenmayer et al. 1994; Peralta and
Cuesta 1994; Von Knorring and Lindstrom 1995; Sauer et
al. 1999; Stuart et al. 1999). These data have provided evidence that formal thought and speech disorders are regular
and fundamental components of the disorganization
dimension. In contrast, some analyses have emphasized
the heterogeneity of other items brought together under
the term "disorganization" (Liddle 1987; Liddle and
Barnes 1990; Brown and White 1992; Bell et al. 1994;
Bryson et al. 1999): some seem to be more related to the
positive dimension (unusual content of thought), others to
the negative dimension (problems of volition), while others seem epiphenomenal to sample characteristics (inappropriate affect, mannerism).
To summarize, the dimensional approach has shed
additional light on Bleuler's intuition that the disorganization dimension is closely linked to the formal thought and
speech disorders and has made it possible to provide a
more precise definition of thought disturbance than that
proposed by Bleuler. For example, the Thought and Language Disorder scale (TLC) (Andreasen 1979), which
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although not the only instrument for assessing formal
thought and speech disorders is certainly the most widely
used, is an atheoretical scale composed of 18 clearly
defined items. All the definitions of these items are based
on observations of the speech and language behavior of
psychiatric patients. Unlike Bleuler's' "mental dissociation," most of the studies involving an analysis of the
items of the TLC have shown a high level of interjudge
reliability.
Why a Pathogenetic Approach to Disorganization? As
defined today by most of the instruments for assessing
symptoms, and despite dramatic improvements in achieving a description that is as objective as possible, schizophrenic disorganization continues to pose unresolved
questions. First, there is some consistent evidence that
items reflecting disorganization are particularly unstable
(Peralta and Cuesta 2001). Second, the factor-analytically
derived dimension called "disorganization" is formed differently by different factor analyses. There is an item
overlap for the components linked to formal thought and
speech disorders but a number of different item groupings
have been proposed, and an unambiguous definition of the
disorganization dimension is still not available. Third,
items reflecting disorganization are not specific to schizophrenia patients: the formal thought and speech disorders
reported as the direct expression of disorganization—tangentiality, derailment, incoherence, and illogicality—
occur with almost equal frequency in schizophrenia
patients and patients with mania (Harvey 1984;
Andreasen and Grove 1986; Docherty et al. 1988).
Problems currently encountered in trying to improve
the description of schizophrenic disorganization could be
partially resolved by a pathogenetic approach. Current
definitions of disorganization issues yielded by the dimensional approach do not refer to any pathogenetic theory
and do without any underlying mechanisms of disorganization. Therefore, many authors currently stress that
pathophysiological mechanisms to explain clinical symptoms must be found, and the search for a psychometrically
and clinically relevant symptom-based method for measuring the disorganization dimension continues to be
important (Bryson et al. 1999; Docherty et al. 2000; Peralta and Cuesta 2001). We assume that cognitive research
may be a promising area of investigation.
In effect, one way of providing a more precise
description of schizophrenic disorganization is to take
cognitive abnormalities that underlie thought and speech
disorders in schizophrenia as guides for rereading clinical
symptoms and indicating new clinical signs. As far as cognitive psychopathology is concerned, Bleuler's psychopathological approach has lost none of its relevance
because it is an attempt to explain and describe the clinical
indexes that are most specific to schizophrenic disorders
on the basis of a pathogenetic theory. The cognitive
research embodied in the model that we support in this
article is inspired by the Bleulerian tradition: our pathogenetic approach, in which pathophysiological abnormalities are considered, is intended to provide a description of
schizophrenic disorganization that is valid from the cognitive point of view and potentially heuristic in clinical
terms.
A Cognitive Model Specifying
Candidate Mechanisms for
Schizophrenic Disorganization
Cognitive Mechanisms of Schizophrenic Disorganization: Hardy-Bayly's Model. The model that we propose
postulates that two cognitive anomalies are common to all
disorganized schizophrenia patients and could be considered as central pathophysiological mechanisms of schizophrenic disorganization: (1) a deficit in the integration of
contextual information, and (2) a "theory of mind" deficit
The first deficit can be described as a difficulty in taking
account of contextual information in a way that is appropriate to the situation. Formulations have been advanced
about disorganized schizophrenia patients' difficulty in
using contextual information to select an appropriate
response (Widlocher and Hardy-Bayle" 1989; Cohen and
Servan-Schreiber 1992; Cohen et al. 1999; Harrow et al.
2000). The second deficit corresponds to an inability to
attribute mental states to others; to infer other people's
intentions, desires, and beliefs; and to respect the rules
involved in communication. Innovative research has suggested that a difficulty in understanding other people's
mental states could induce signs such as poor, incoherent,
or inappropriate speech (Frith 1992, 1994; Sarfati 2000).
Of all the situations encountered in everyday life,
communication with others requires the greatest ability to
adapt to the context and to attribute mental states: a conversation, consisting as it does of verbal and nonverbal
exchanges with other people, is by definition a shifting and
uncertain context, and the data associated with it must be
constantly inferred and updated on the basis of peripheral
information (Sperber and Wilson 1986; Leslie 1987).
Many of the thought and speech disorders and the conversational difficulties observed in disorganized schizophrenia patients can therefore be understood as arising from
impairments in these two cognitive processes.
The two cognitive processes underlying schizophrenic disorganization may not be unrelated: According
to Pickup and Frith (1997), "theory of mind and contextual
deficits may reflect a single underlying cognitive impairment in schizophrenia" (p. 121). The theory of mind
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deficit may have its roots in a key underlying deficit in the
integration of contextual information, which is known to
be the source of other cognitive impairments (Harrow et
al. 2000). The ability to take account of contextual information, which is considered to be an elementary cognitive
process, could have consequences at a higher cognitive
level in the theory of mind abilities, which also require the
absorption of the relevant contextual material in order to
supply an appropriate response (Hardy-Bayl6 1994, 1996).
A deficit in the cognitive processes that make an action
relevant within the context in which it occurs could compromise the inference of other people's mental states from
the context in which they occur (Sarfati et al. 1997i>).
understanding of a sentence requires the integration of the
available information in order to construct a semantic representation of the sentence. Using an online word-monitoring task, Kuperberg et al. (1998) observed a reduced
sensitivity to linguistic context in thought-disordered
schizophrenia subjects.
Arguments in Support of a Theory of Mind Deficit
Frith's team provided experimental evidence that some
schizophrenia patients are unable to attribute intentions
(Frith and Corcoran 1996) or beliefs (Corcoran et al.
1995) to others. The data provide support for the argument that patients with behavioral signs such as incoherent speech are the poorest at inferring mental states, while
patients with phenomena of passivity exhibit normal performances. However, the groups of disorganized patients
were too small for it to be possible to draw a conclusion.
A more recent article confirmed that patients with behavioral signs scored significantly worse than remitted or
paranoid patients (Pickup and Frith 2001).
Other studies have provided clearer evidence that subjects exhibiting incoherent speech and/or a pattern of disorganization have significant difficulty in attributing mental states to others, whatever the method used to test this
ability: social skills (Cutting and Murphy 1990), understanding of metaphors (De Bonis et al. 1997), humor (Corcoran et al. 1997), or false beliefs (Mazza et al. 2001). The
idea that there is a link between disorganization and difficulties in attributing intentions has recently received support, in particular in the form of statistics illustrating the
correlation between the level of disorganization and the
number of correct responses in tasks designed to evaluate
theory of mind (Greig et al. 1999). However, the comparison of the different data is made more difficult by the fact
that there are different ways of defining disorganized subgroups.
Arguments in Support of a Deficit in the Integration of
Contextual Information. When the use of contextual
information is tested under precise experimental conditions, the deficit is often found in disorganized schizophrenia patients.
The lexical decision task, which permits the online
study of the processes involved in the processing of the
semantic context, has been by far the most popular paradigm for assessing the link between clinical patterns of
schizophrenia and context-processing anomalies. The task
consists of the sequential presentation of two items, a
prime item (which constitutes the context) and a target
item with a lexical decision based on only this target item
and that consists of deciding whether the target item is a
word or pseudoword. Results show that the subject's
response is facilitated when the context item is semantically related to the target item (e.g., doctor-nurse) (Neely
1977). This facilitory (or priming) effect has been generally interpreted as the result of the integration of contextual information in which the target word is presented. The
subject uses the regular occurrence of pairs of associated
words to comply with the instruction: the higher the proportion of semantically related words, the greater the
effects of integrative processes (de Groot 1984; Neely
1991; Shelton and Martin 1992; Passerieux et al. 1997).
All the studies that have used a lexical decision task to
examine the integration of contextual information in disorganized schizophrenia patients (Manschreck et al. 1988;
Henik et al. 1992, 1995; Spitzer et al. 1993, 1994; Spitzer
1997; Aloia et al. 1998; Weisbrod et al. 1998) have, with
one exception (Blum and Freides 1995), identified anomalies in semantic processing in such patients. In the majority of these studies, schizophrenia subjects with disorganization were compared with those with no disorganization:
the latter did not exhibit similar anomalies.
The link between the deficit in the integration of contextual information and disorganization has also been
demonstrated using a phrasal context. To an even greater
extent than the understanding of an isolated word, the
Confirming Hardy-Bayly's Model of Schizophrenic
Disorganization. As we have seen, various results have
established the consistency of the hypothesis that two cognitive impairments could be considered to be central
pathophysiological mechanisms of schizophrenic disorganization: (1) a deficit in the integration of contextual information; and (2) a theory of mind deficit. At the same time,
a large amount of additional experimental evidence has
been collected that runs counter to the hypothesis that the
disorganization syndrome could be due to a single, generalized deficit (Weinberger and Gallhofer 1997; Schatz
1998). Of course, a number of other hypotheses have been
proposed concerning the cognitive basis of schizophrenic
disorganization. One of the most consistent suggests that
schizophrenic disorganization might be associated with
attentional dysfunction and a failure to suppress inappro-
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priate responses (Liddle 1996). But recent data have
shown that disorganization symptoms are not associated
with attentional dysfunction as measured by the
Continuous Performance Test; are not (or not specifically)
associated with perseverations on the Wisconsin Card
Sorting Test (WCST), which indicate a failure to suppress
inappropriate responses; and are not associated with working memory problems as measured by the Span
Apprehension test (Aloia et al. 1998; Goldberg et al. 1998;
Nieuwenstein et al. 2001). Nonspecific abnormalities on
the WCST may be considered a rough indication of some
executive dysfunction in schizophrenic disorganization,
but, as Frith claims, we think that "progress in our understanding of the signs and symptoms of schizophrenia
requires studies of executive processes which are conducted at a high level of detail . . . and which require the
development of novel test procedures" (Laws 1999, p. 32).
In the third part of this article, we present an exhaustive review of the literature—not of all the presumed cognitive mechanisms of schizophrenic disorganization but of
all the research conducted within the cognitive framework
of Hardy-Bayle's model. This research provides a detailed
analysis of the integration of contextual information, and
of theory of mind—specifically in disorganized versus
nondisorganized schizophrenia patients—and helps confirm the link between these cognitive processes and disorganization. At the same time, it represents a study of the
nature of the contexts ignored by disorganized schizophrenia patients and of the conditions that influence this processing; helps identify the nature of the cognitive abnormalities; and helps clarify what conditions modify the
functioning of these skills. Thus, the data concerning
schizophrenia patients provided by cognitive neuropsychology will identify specific anomalies that can help us
define the clinical items that are thought to represent the
anomalies' clinical expression.
of contextual information. A first major result was the
preservation of the automatic processes and a lack of
application of controlled integrative processes in a group
of 17 schizophrenia subjects who exhibited mild to severe
formal thought disorders, compared with 10 normal subjects (Passerieux et al. 1995). The clinical specificities of
patients presenting this cognitive pattern were better characterized in a second study, which compared three groups:
11 healthy control subjects; a disorganized group of 11
schizophrenia patients with a score greater than or equal to
7 on Andreasen's TLC (mean score = 17.6); and a nondisorganized group of 11 schizophrenia patients with a score
lower than 7 on the TLC (mean score = 4.3). The results
revealed a significant facilitory effect of the contextual
information in the healthy control group and the nondisorganized schizophrenia patients, with the disorganized
schizophrenia patients differing significantly from these
two groups in exhibiting no facilitory effect (Passerieux et
al. 1997). These data were then replicated in an experiment that involved 14 inpatients suffering from a major
depressive episode, 20 healthy control subjects, and 20
hospitalized controls from the surgical wards; and 34
schizophrenia patients, 10 of whom had no formal thought
disorders, and 24 of whom had a score of at least of 7 on
the TLC. From this point on, the presence of thought and
language disorganization with a score of 7 or more in the
TLC is taken to define the disorganized schizophrenia
group. Once again, it was only in the disorganized schizophrenia patients that no facilitory effect was observed, and
this group differed significantly from the other four groups
(Besche et al. 1997).
One other experiment was designed to determine
whether the deficit in the integration of contextual information was generalized or specific to a certain type of context. Our hypothesis was that certain links between the
context item and the target item are processed normally by
disorganized schizophrenia patients, whereas others are
not. We therefore compared the performances of these five
groups of subjects in tasks involving syntactic relations
versus semantic relations. This experiment was presented
under two different conditions: a sequential presentation
with a stimulus onset asynchrony (SOA) of 500 milliseconds as in the first experiment and a simultaneous presentation with an SOA of 0 milliseconds. The results revealed
that only the semantic relations were ignored, while schizophrenia subjects processed the syntactic context normally, whatever the conditions of presentation (Besche et
al. 1996, 1997).
To further investigate the functional character of the
contextual deficit, we conducted a series of experiments
into the role of both the experimental material and the
instructions in the nonemergence of the facilitory effect in
disorganized schizophrenia patients. First, we considered
Experimental Evidence in Favor of
Hardy-Bayly's Model: The
Pathophysiological Mechanisms of
Disorganization in Schizophrenia
Characterization of the Deficit in the Integration of
Contextual Information. Our studies have attempted to
provide direct experimental arguments in favor of the
existence of a link between a specific deficit in the integration of contextual information and the clinical pattern
of disorganization by using the well-known lexical decision task.
The primary experiments were designed to explore
both the automatic mechanisms of spreading activation
and the controlled processes responsible for the integration
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Hardy-Bayle et al.
one experimental variable to be crucial, namely the level
of material structuring—that is, the more or less frequent
occurrence of the semantically related word pairs (e.g.,
doctor-nurse) in the experimental material. We hypothesized that schizophrenia patients would neglect context
under only limited conditions in which the context was
"weakly structured"—that is, in a lexical decision task
with only a low proportion of semantically related word
pairs. In the earlier studies (Besche et al. 1997; Passerieux
et al. 1997), context was weakly structured (17.5% of
semantically associated words). We therefore further
hypothesized that reinforcing the structuring of the context
would enable disorganized schizophrenia patients to
process the context normally and would provide evidence
that the deficit in the integration of contextual information
is a functional deficit. Second, we imagined that instructions that reinforced the semantic processing of the context word would help schizophrenia subjects implement
the controlled operations that underlie the facilitory effect
This type of hypothesis has been indirectly verified in
memory tasks (Koh 1978) but not in online tasks such as
the lexical decision task. We considered the dual lexical
decision task, in which subjects are asked to decide
whether both the context item and the target item are
words or pseudowords, to be an instructive situation. To
test these two hypotheses, an experiment was designed in
which we crossed two types of factors: the "level of material structuring" factor (strong or weak) and the "instruction" factor (single or dual decision). Fifteen disorganized
schizophrenia patients and 15 healthy control subjects
took part in this study. The results (Besche-Richard and
Passerieux, in press) confirmed that the facilitory effect
tends to be normalized in disorganized schizophrenia
patients by the dual lexical decision task as well as by the
enhancement of the structure of the material, and provided
evidence of the functional character of the deficit.
We are currently continuing the characterization of
the contextual deficit by using the evoked potential
method (Passerieux et al. 1998, 2000a, 2000b). We are primarily concerned with N400, which is thought to be the
electrophysiological counterpart of the integration of contextual information (Kutas and Hillyard 1980). N400
anomalies have been clearly established in disorganized
schizophrenia patients (Grillon et al. 1991; Koyama et al.
1991, 1994; Mitchell et al. 1991; Adams et al. 1993;
Nestor et al. 1997; Niznikiewicz et al. 1997; Strandburg et
al. 1997; Condray et al. 1999). We are currently conducting a lexical decision task that makes use of two types of
context: a single word (a classical semantic priming task)
and a phrasal context, as used in the majority of studies
that have reported N400 anomalies in schizophrenia
patients. A sentence represents a context that is stronger
than a single word in the sense that such a context can be
very difficult to ignore: the final word of the sentence,
which is the target item, is therefore highly predictable
(e.g., phrasal context = "He takes the letters to the"; target
item = "post office"). The data that we recorded for a
group of 8 disorganized schizophrenia patients revealed
that N400 was modulated by the context. When the context is a sentence, patients behave like healthy controls.
When the context is reduced to a single word, N400 modulation is reduced. This result therefore represents an additional argument in favor of a functional deficit in the integration of contextual information in disorganized patients.
It also clearly argues against the concurrent hypothesis of
a working memory deficit, because the context formed by
a sentence imposes a greater memory load than that generated by a single word (Passerieux et al. 2000b).
Characterization of the Theory of Mind Deficit.
Unlike the study of the contextual deficit, which has been
able to make use of existing tasks, the study of the theory
of mind deficit has made it necessary to develop original
material, hi effect, it was necessary to test the attribution
of intentions to others in adult subjects while avoiding the
bias that verbalization of the material itself or of the
response may constitute in thought- and speech-disordered schizophrenia patients. None of the tests used for
assessing theory of mind fulfilled these conditions:
because they generally test the attribution of incorrect
beliefs in children and require an open, verbal response,
they were suitable neither for the hypothesis in question
nor for the tested population, hi the light of an original
experiment using picture stories (Baron-Cohen et al.
1986), Sarfati and coworkers developed a protocol that
used cartoon strips but no verbal material. Each cartoon
strip was designed to present a character in a series of 3
pictures and acquired coherence only when the character's
intention was inferred from his or her behavior. A forcedchoice response made it possible to determine whether the
tested subject was attributing correct or incorrect intentions to the character.
An initial version of this material (Sarfati et al. 1997b)
was used to test three groups of 12 subjects: healthy controls,
depressed subjects, and schizophrenia subjects. The results
showed that only certain schizophrenia subjects experienced
difficulty in identifying the intentions of the cartoon characters. These were the subjects who exhibited clear signs of
thought and language disorders, with a score higher than 7
on Andreasen's TLC scale. Following the same logic as with
contextual deficit, the clinical specificities of patients presenting a theory of mind deficit were better characterized in a
second study that compared four groups: a disorganized
group of 12 schizophrenia patients with a score greater than
or equal to 7 in Andreasen's TLC (mean score = 17.3); a
nondisorganized group of 12 schizophrenia patients with a
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total score lower than 7 in the TLC with no single item
greater than 1 (mean score = 4.3); 24 healthy controls; and
12 depressed patients. The results confirm that only the disorganized schizophrenia subjects differed in their level of
incorrect responses from the normal, depressed, or nondisorganized schizophrenia subjects (Sarfati et al. 1997a). These
data were then replicated in a new experiment that involved
15 disorganized schizophrenia patients, 10 nondisorganized
schizophrenia patients, 10 subjects with a moderate manic
state, and 15 control subjects. Once again, while manic subjects behaved like the healthy controls, a theory of mind
deficit was found in only disorganized schizophrenia patients
(Sarfati and Hardy-Bayle" 1999).
The aim of the latter experiment was also to reveal the
strategy used by these disorganized schizophrenia patients
to provide their response. The type of answer cards that
they chose (0% nonsense answer) formally refuted the
idea that their responses could be due to chance, to a lack
of attention, or to a general deficit. On the contrary, when
these subjects failed to interpret the actions of other people
as a function of their mental state, they used a cognitive
strategy of substitution based on the frequency of the associated actions. These subjects answered as if they voluntarily relied on the everyday or dominant character of an
action in order to make sense of the behavior of others
rather than taking account of the mental state underlying
it, as suggested by the specific context in which it takes
place (Sarfati and Hardy-Bayle" 1999).
To further investigate the functional character of the
contextual deficit, we conducted a series of experiments
into the effect of the introduction of verbal material on
performance. To do this, we asked the patients to respond
immediately by designating response pictures in some
cases and response sentences in others (Sarfati et al. 1999,
2000). This variant was intended to demonstrate that verbal material is able to force the tested subjects to perform a
more thorough processing of the relevant contextual elements when responding to a theory of mind task and that it
improves performance. This precise hypothesis was not
confirmed, even though the data demonstrated that the
patients who were able to improve their performance as a
result of verbalization were those exhibiting the shortest
periods of evolution. This effect of the duration of the illness on the ability to restore a defective cognitive function
had already been indicated within the framework of
research into theory of mind and designated as a generative factor of social deficit. This suggests that in schizophrenia that has not yet become chronic there is a functional theory of mind deficit that is affected by clinical
changes and can disappear in remitted patients (Drury et
al. 1998; Pickup and Frith 2001).
Just as was the case with the deficit in contextual processing, our research is being continued with a study
involving cerebral activity. We intend to establish a relation between the cognitive and the cerebral processes
involved in the attribution of intentions to others. All published studies on this topic provide evidence that the ability to attribute mental states is mediated by highly circumscribed brain systems that are activated during tasks that
directly call on a theory of mind; these are, in particular,
the right or left anterior mediofrontal gyms and, less frequently, the left temporoparietal junction (Baron-Cohen et
al. 1994; Fletcher et al. 1995; Goel et al. 1995; Gallagher
et al. 2000). The protocol developed on the basis of HardyBayly's model included 8 healthy adult subjects who took
part in a positron emission tomography study. This was
based on the contrast in activity between the target and
control cartoons: the target cartoons called on a theory of
mind while the control cartoons did not (Brunet et al.
2000). As reported in the literature, regardless of modality,
the anterior mediofrontal gyms was shown to be activated
in the condition with theory of mind when compared to the
condition without theory of mind. The right-hand lateralization of the activation can be explained by the sensory
modality called on here: the cartoon task used only pictures, and it is a well-known neuropsychological fact that
propositional representations are lateralized on the left and
visuospatial representations are processed on the right.
The role of the right hemisphere has been emphasized
more than the role of the left hemisphere in the theory of
mind literature (Siegal et al. 1996; Winner et al. 1998;
Gallagher et al. 2000). Application of this task to disorganized schizophrenia patients reveals the existence of a
deficit in the areas implicated in normal controls (Brunet
etal. 2001).
Revisiting the Clinical Description of Schizophrenic
Disorganization. Bleuler chose to describe schizophrenic disorganization in terms of an underlying theory
of dissociation rather than on the basis of a precise observation of clinical indexes. In contrast, the dimensional
approach has given rise to precise definitions of disorganization based on objective observations and descriptions of
symptoms rather than on an underlying theory. Adopting a
Bleulerian view of a clinical description based on a pathogenetic approach, we have assumed that it is possible to
further improve the description of schizophrenic disorganization in terms of specificity and subtlety if the description of the clinical signs is based on underlying pathophysiological mechanisms. We have presented a volume
of experimental evidence in favor of the involvement of
two cognitive anomalies in schizophrenic disorganization.
We propose that, now that they are precisely identified
and characterized, these anomalies can serve as guides in
the description of the clinical items that are thought to
represent the anomalies' expression at the clinical level.
465
Schizophrenia Bulletin, Vol. 29, No. 3, 2003
Hardy-Bayl6 et al.
Thus, we have proposed original clinical signs as part
of an instrument designed for the assessment of communication disorders in schizophrenia patients (Schizophrenic
Communication Disorder scale [SCD]). The SCD consists
of 15 items, each of which has been designed to be as far
as possible a clinical expression of one of the two pathophysiological mechanisms that have been shown to underlie the disorganization syndrome: deficit in the integration
of contextual information, and theory of mind deficit. As
an illustration, we present two of these items included in
the version of the scale, which has been published in detail
elsewhere (Olivier et al. 1997).
One of the items that is thought to reflect a deficit in
the integration of contextual information is the inability to
clarify a speech corpus: the patient is unable to make his
or her speech clearer, more understandable, and more
informative when asked to do so by the clinician. The clinician's request constitutes a conversational constraint that
is thought to aggravate conversational difficulty: as soon
as a patient's speech becomes vague, unclear, or incomprehensible, the clinician asks for clarification: "What do
you mean by that?" "Can you explain what your answer
means?" "Can you tell me what you are trying to say?' In
effect, to clarify what has just been said, it is necessary to
integrate the contextual information that has just been
evoked in the conversational exchange. A normal subject
with no deficit in the integration of contextual information
should be able to clarify his or her speech, to adapt it
within the conversation by using the elements of the conversational context, and to add information to clarify what
he or she has just said (Harrow et al. 2000). We postulated
that a patient who suffers from a deficit in the integration
of contextual information would not be able to provide
any information relating to the prior topic and would not
make his or her speech any clearer.
Another kern among those that are thought to reflect a
theory of mind deficit is the inability to attribute an intention to another person: the patient has an impaired perspective as discussed in Harrow et al. (1989). The patient
is unable to describe or recognize the intentions of his or
her relatives. Once again, we should stress that the pathogenetic logic requires the patient to be placed in a constrained conversational situation that is necessarily artificial because it needs, to the greatest possible extent, to call
on the cognitive functions that are thought to be defective
in the patient: the clinician assesses the patient's ability to
attribute intentions to others by asking him, during the
interview, to describe the intentions of various familiar
people: "In your opinion, what does your [father, mother,
friend, doctor, team, neighbor] think about [you, your
problems]?" In effect, to reply to such a question, the
patient must possess a theory of mind—that is, a personal
representation of the mental states of others. Without that,
the patient is unable to provide his or her own view about
the other person's opinion together with all the doubts that
go with it.
The frequency of the 15 items in the SCD has been
assessed in a total of 80 subjects: 43 schizophrenia
patients, 27 subjects with affective disorders, and 10 normal control subjects. The results of this study showed that
most of these items were specific to schizophrenia patients
and, in particular, the global scores made it possible to discriminate between schizophrenia patients and patients
with affective disorders at a statistically significant level,
while, according to the literature, TLC scores are comparable in schizophrenia patients and manic patients with
psychotic symptoms (Harvey 1984; Andreasen and Grove
1986; Docherty et al. 1988). As attempted, the global SCD
score was positively correlated with the global TLC score
(r = 0.75, p = 0.001). When analyzed separately, the TLC
items that had the highest correlations with SCD global
score were poverty of content of speech, tangentiality,
derailment, incoherence, illogicality, neologisms, loss of
goal, perseverance, and self-reference. These are the items
that best represent Bleuler's concept of "loose associations" and that are thought to be specific to schizophrenia
patients. More generally, the items of the preliminary SCD
were positively correlated with the items belonging to the
disorganization dimension: tangentiality, derailment, inappropriate affect, strange behavior, and alogia. By contrast,
pressure of speech, distractible speech, and attentional
impairment were not correlated with the global SCD score
(Olivier et al. 1997).
The search for a psychometrically and clinically relevant symptom-based method for measuring the disorganization dimension is important (Bryson et al. 1999; Peralta
and Cuesta 2001). We assume that items issuing from a
pathogenetic approach could provide a way of assessing
new clinical symptoms and a complementary group of
signs that are relevant from a pathophysiological point of
view. This kind of approach, although new, is beginning to
be illuminated by a number of studies such as our own and
those conducted by Frith's team (Frith 1992). In the future,
a new cognitive interpretation of clinical symptoms could
be proposed.
Conclusion
As Frith (1992) pointed out, cognitive hypotheses are able to
explain only abnormal behavior, not diagnostic categories.
The aim of our research is to provide evidence that some
cognitive hypotheses could explain, at least partially, schizophrenic disorganization especially in connection with communication disorders. In line with the literature, we hypothesized that two pathophysiological mechanisms are involved
466
Disorganization Symptomatology
Schizophrenia Bulletin, Vol. 29, No. 3, 2003
in schizophrenic disorganization: deficit in the integration of
contextual information and deficit of theory of mind. We
attempted to adduce experimental evidence of a cognitiveclinical link between these deficits and thought and language
disorganization. The cognitive-cerebral validity of these two
anomalies was then tested by revealing electrophysiological
indicators of the contextual deficit and neuroanatomical indicators of theory of mind deficit.
The clinical interest of such research and of a pathogenetic approach is due to the fact that cognitive abnormalities can guide the description of a clinical pattern. The
two well-identified cognitive abnormalities thus became
the starting point in the search for new clinical signs
thought to belong to the spectrum of schizophrenic disorganization symptoms. As Bleuler described thought disturbance on the basis of an underlying theory of "Spaltung,"
we were interested in a neo-Bleulerian way of describing
schizophrenic communication disorders in terms of two
underlying cognitive deficits. We have presented the way
in which we constructed new clinical items issuing from
this pathogenetic approach and reflecting either the deficit
in the integration of contextual information or the deficit
of theory of mind. The items were designed to be finegrained and to identify specific communication disorders
elicited under constrained conversational situations. Preliminary results show that this approach is promising, but
much more is needed before the items we have defined can
be implemented in clinical practice. In the future, it will be
necessary to consider the permanent or intermittent nature
of these communication disorders and their sensitivity in
patients who exhibit few or no symptoms. Because the
experimental data suggest that the two cognitive anomalies involved in disorganization have state variables, it is
conceivable that the resulting communication anomalies
may be normalized following an acute episode in patients
undergoing a period of symptomatic remission. Studies
are currently under way to address these points.
Clinical directions that attempt to define a more specific clinical view of schizophrenia on the basis of a pathogenetic approach and that are rooted in the European tradition are largely unrepresented in the literature. It is first
necessary to prove their ability to explain, as here, a specific dimension of the illness before claiming that they can
account for a large proportion, if not all, of the semiology
of schizophrenia. We hope that our research has illustrated
the value of such an approach.
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The Authors
Marie-Christine Hardy-Bayle", M.D., Ph.D., is Professor of
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IConS
International Conference on Schizophrenia
Organized by the Schizophrenia Research Foundation (SCARF), Chennai, India
(WHO Collaborating Center for Mental Health Research)
Co-sponsored by the World Health Organization and the
World Psychiatric Association
January 29-February 2,2004 at Chennai (formerly Madras), India
This conference will showcase the best of schizophrenia research in the world.
There will be a one-day workshop on Cognition in schizophrenia.
For more details: www.icons-scarf.org
For further information, please contact
Dr. R. Thara
Director, SCARF INDIA
e-mail: [email protected], [email protected]