Вы находитесь на странице: 1из 16

Cognitive Neuropsychiatry

ISSN: 1354-6805 (Print) 1464-0619 (Online) Journal homepage: http://www.tandfonline.com/loi/pcnp20

Source flexibility in schizophrenia: specificity


and role in auditory hallucinations

Julien Laloyaux, Clara Della Libera & Frank Larøi

To cite this article: Julien Laloyaux, Clara Della Libera & Frank Larøi (2018): Source flexibility in
schizophrenia: specificity and role in auditory hallucinations, Cognitive Neuropsychiatry
To link to this article: https://doi.org/10.1080/13546805.2018.1530648

Published online: 05 Oct 2018.

Submit your article to this journal

View Crossmark data

Full Terms & Conditions of access and use can be found at


http://www.tandfonline.com/action/journalInformation?journalCode=pcnp20
COGNITIVE NEUROPSYCHIATRY
https://doi.org/10.1080/13546805.2018.1530648

Source flexibility in schizophrenia: specificity and role


in auditory hallucinations
a,b,c c a,b,c
Julien Laloyaux , Clara Della Libera and Frank Larøi
a
Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway; bNORMENT –
Norwegian Center of Excellence for Mental Disorders Research, University of Oslo, Oslo, Norway;
c
Psychology and Neuroscience of Cognition Research Unit, University of Liège, Liège, Belgium

ABSTRACT ARTICLE HISTORY


Introduction: One important aspect of human cognition relies on the Received 27 June 2017
ability to bias attention towards stimulus-independent and stimulus- Accepted 25 September 2018
oriented thoughts and to switch between these states – or source
flexibility. This mechanism has received very little attention in the KEYWORDS
Positive symptoms;
literature, and in particular in schizophrenia. Moreover, there is good delusion; gateway
reason to believe that this mechanism could also be implicated in hypothesis; executive
hallucinations, but this hypothesis has never been examined. Thus, the functions; cognitive flexibility
aim of the present study was, for the first time in the literature, to
explore source flexibility abilities in schizophrenia and their potential
relations with auditory hallucinations.
Methods: Forty persons diagnosed with schizophrenia and 26
healthy controls were evaluated with tasks assessing source
flexibility, cognitive flexibility and processing speed. Patients were
also assessed with a measure of hallucinations and delusions.
Results: Results revealed that persons diagnosed with schizophrenia
presented a poorer performance than healthy controls for source
flexibility. Moreover, results demonstrated that source flexibility
performance could not be explained by a more general impairment of
processing speed or buy difficulties in cognitive flexibility. Finally,
source flexibility was found to be related to hallucinations.
Conclusions: Source flexibility plays an important role in schizophrenia
and in particular is a cognitive mechanism involved in hallucinations.

Introduction
The gateway hypothesis (Burgess, Dumontheil, & Gilbert, 2007; Burgess, Simons,
Dumontheil, & Gilbert, 2005) states that the rostral prefrontal cortex supports important
mechanisms in human cognition that allow one to bias attention towards stimulus-inde-
pendent (SI) (i.e., the thoughts inside one’s head) and stimulus-oriented thoughts (SO) (i.e.,
information from the outside world), and to switch between these sources – source
flexibility. To date, several studies have tested this hypothesis and found that different brain
regions underpin different components of source flexibility. In particular, Burgess, Gilbert
and Dumontheil (2007) (see also, Burgess et al., 2005) showed – in a meta-analysis that
included neuroimaging studies – that the medial part of the rostral prefrontal cortex is related
to stimulus oriented attending (SO), whereas the lateral part is related to stimulus

CONTACT Julien Laloyaux julien.laloyaux@uib.no, j.laloyaux@ulg.ac.be


© 2018 Informa UK Limited, trading as Taylor & Francis Group
2 J. LALOYAUX ET AL.

independent attending (SI) and to the switching between these sources. This suggests that
source flexibility is a multifaceted construct with different neurological underpinnings.
Source flexibility is hypothesised to be implicated in a number of different everyday life
activities and complex cognitive tasks. In fact, many of these activities (e.g., multitasking
activities) require keeping a global goal in mind while conducting another task and are likely
to trigger internal attending (SI) with the person wondering what to do and creating a mental
action plan (Burgess, Dumontheil, et al., 2007).
However, despite the fundamental role of this cognitive mechanism in human cogni-tion,
it has received very little interest in the literature in general and even less so in psychological
disorders such as schizophrenia. Indeed, it is well established that persons diagnosed with
schizophrenia present cognitive impairments in several domains such as processing speed,
working and episodic memory, and executive functions (Bortolato, Mis-kowiak, Kohler,
Vieta, & Carvalho, 2015). To date, however, only one study has adminis-tered a source
flexibility task to a group of persons diagnosed with schizophrenia compared to healthy
controls (Levaux, Van der Linden, Larøi, & Danion, 2012). In par-ticular, they administered
one block of one of the tasks developed by Gilbert, Frith, and Burgess (2005) in which
participants are required to classify capital letters according to whether the letter presented
on the screen contains one or more curves (e.g., B) or only straight lines (e.g., A). During the
task, participants were required to make judgments on either the letters that are shown on the
screen (i.e., external phase, stimulus oriented – SO), or the mental representations of the
letters (i.e., internal phase, stimulus independent
– SI, when no letters are displayed on the screen) – and these two phases alternated during
the entire task. Levaux et al. (2012) reported that the patients were significantly slower than
healthy controls in switching from the external world to internal representations and that
source flexibility was related to multitasking abilities. Unfortunately, in that the authors only
focused on the ability to switch from the external world to internal representations, it is
difficult to drawn strong conclusions regarding source flexibility abilities. There is thus a
need to explore the patients’ ability to switch from internal representations to the external
world and their ability to maintain their attention on one of the sources. In addition, the
authors only focused on the reactions times and did not take into account the quality of the
performance as measured, for instance, with the percentage of errors committed during the
task. Moreover, the study did not investigate if broader cognitive functions (such as pro-
cessing speed) may have a main influence on source flexibility performance. Indeed, proces-
sing speed has been found to be a major cognitive impairment in schizophrenia that can have
a significant influence on other, more specific, cognitive functions (Dickinson, Ragland,
Gold, & Gur, 2008; Dickinson, Ramsey, & Gold, 2007). Finally, the specificity of source
flexibility compared to other forms of flexibility (such as cognitive flexibility) was not
explored. Indeed, cognitive flexibility has been shown to be impaired in schizophrenia
(Mittal, Mehta, Solanki, & Swami, 2014; Orellana & Slachevsky, 2013; Thoma, Wiebel, &
Daum, 2007) and may have an impact on source flexibility.
It could also be hypothesised that source flexibility plays a central role in the apparition
and maintenance of specific symptoms experienced by patients with schizophrenia, in par-
ticular, auditory hallucinations. In fact, when experiencing hallucinations, one needs to
switch attention between the internal (i.e., hallucinations) and external world (i.e., the sur-
rounding environment). It is possible that persons experiencing auditory hallucinations
encounter difficulties in maintaining attention to the external and internal world in
COGNITIVE NEUROPSYCHIATRY 3

addition to difficulties in switching between these sources. Such a hypothesis is


congruent with the self-regulatory executive function model (Wells & Matthews, 1994)
that proposes a dysfunctional pattern of information processing that is characterised by
self-focused attention which becomes excessive, inflexible, and uncontrollable in the
context of different psychological disorders. From this perspective, it is possible to
hypothesise that difficulties in source flexibility play a role in this excessive and
inflexible self-focused attention described by Wells and Matthews (1994). For example,
difficulties in switching between internal representations and the external world may
facilitate self-focused attention as one would have difficulties in disengaging from them.
As for another example, difficulties in attending to the external world may increase the
degree of self-focused attention, as one would lose track of what s/he is attending to
and, in reac-tion, may pay more attention to the internal world.
Source flexibility can also be related to the existing literature on self-recognition deficits
in schizophrenia. To date, a number of studies (for a review, see Brookwell, Bentall, Varese,
2013; Waters, Woodward, Allen, Aleman, & Sommers, 2012) have reported that patients
diagnosed with schizophrenia, especially those with hallucinations, present difficulties in
discriminating between internal and external events and, in particular, in recognising
thoughts and mental events as self-generated. For example, patients showed a tendency to
attribute memories of self-generated material to an external source (source memory), to
perceive words in ambiguous noise (signal detection), and to attri-bute self-generated speech
to an external source (self-monitoring). These externalising biases are believed to play a role
in the development and maintenance of hallucinations although the cognitive mechanisms
underpinning these biases are still unclear. Nonethe-less, it can be hypothesised that
difficulties in source flexibility may be involved in these biases. In particular, difficulties in
attending to the internal and external world and in switching between these sources may lead
to a confusion between them.
The aim of the present study is to explore a potential impairment of source flexibility
in a group of persons diagnosed with schizophrenia. Secondly, we examined whether or
not this cognitive mechanism could be explained by a general impairment of processing
speed or specific difficulties in cognitive flexibility. Finally, the extent to which source
flexibility is related to auditory hallucinations was also investigated. To the best of our
knowledge, this is the first study that has examined these issues.

Material and methods


Participants
Forty persons diagnosed with schizophrenia according to DSM-IV (American
Psychiatric Association, 1994) criteria were recruited from local psychiatric services.
Diagnosis was made by the patient’s regular psychiatrist and confirmed by an
experienced clinical psy-chologist. Exclusion criteria consisted of: the presence of
neurological and/or other psy-chiatric disorders, lack of clinical stability (i.e., presence
of treatment non-compliance and/or lack of decrease of severity of positive symptoms),
mental retardation and signifi-cant change in medication within the past month (e.g.,
new type of medication, major change in dose).
Patients’ medication was converted into three indexes: benzodiazepine (diazepam
equivalence in mg), antipsychotic (olanzapine equivalence in mg), and anticholinergic.
4 J. LALOYAUX ET AL.

Table 1. Demographic and clinical characteristics of participants.


Patients (N = 40) Healthy controls (N = 26)
Mean (SD) Min-max Mean (SD) Min-max
Age 37.57(10.80) 17–63 38.11 (10.76) 18–54
Sex (F/M) 7/33 6/20
Work (Yes/No) 1/39 16/10
Education participants (years) 12.08(2.34) 8–18 12.46 (2.96) 8–18
Education mother (years) 12.36(3.37) 5–17 12.44 (2.95) 6–17
Education father (years) 13.46(3.60) 6–19 12.60 (5.61) 0–25
Cannabis consumption (grams per day) 0.019(0.09) 0–0.50 0.015 (0.06) 0–0.30
Duration of illness from the diagnosis (years) 11.34(7.93) 0.4–29
Number of hospitalisations 4.72(3.25) 0–15
Hospitalized (Yes/No) 10/30
Benzodiazepine (diazepam equivalence in mg) 17.09(15.00) 0–50
Antipsychotic (olanzapine equivalence in mg) 27.41(24.53) 1.5–109.93
Anticholinergic burden (side effect potential) 3.77(2.17) 0–8
a
PSYRATS – Hallucination – Total 7.95(11.15) 0–34
PSYRATS – Delusion – Total 4.42(5.77) 0–18
a
Psychotic symptom rating scale.

Regarding the benzodiazepine index, each benzodiazepine drug was converted into a
dia-zepam equivalence based on the existing data of the literature (e.g., Taylor, Paton, &
Kapur, 2009), and a total score was calculated by adding up each medication. Similarly,
the antipsychotic index involved converting each antipsychotic medication into an olan-
zapine equivalence based on the rates given in the literature (e.g., Davis & Chen, 2004;
Gardner, Murphy, O’Donnell, Centorrino, & Baldessarini, 2010), and a total score was
cal-culated. Finally, for the anticholinergic index, all medications were rated from 0
(signifying no known risk of anticholinergic effects) to 3 (signifying high risk of
anticholinergic effects) based on the literature (e.g., Boily & Mallet, 2008), and a total
score was calculated by adding up each rated medication.
Twenty-eight healthy controls were also included and were selected based on their
simi-larities with patients in terms of sex, age, and number of years of education.
Exclusion cri-teria consisted of the presence of any psychiatric or neurological disorder,
and having a first-degree family history of schizophrenia, schizo-affective or
schizophreniform disorder. Two participants were excluded due to their outlying
performance on several cognitive tests (>3 interquartile range).
The study was conducted in accordance to the Declaration of Helsinki. All participants
provided written informed consent and the study was approved by the local ethics commit-
tee. Participant characteristics are presented in Table 1. Based on independent Student’s t-
tests, there were no significant differences between the two groups for age, years of edu-
cation of the participants, years of education of their parents, and cannabis consumption. A
Fisher’s exact test revealed that both groups were equivalent in terms of gender proportion.

Instruments
Cognitive tasks
All participants were evaluated with several cognitive tasks:

Source flexibility: The test used in the present study is a simplified version of one of
the tasks developed by Gilbert et al. (2005). In this computerised test (Figure 1),
COGNITIVE NEUROPSYCHIATRY 5

Figure 1. Schematic representation of the source flexibility task.

participants are required to classify capital letters according to whether the letter
presented on the screen contains one or more curves (e.g., B) or only straight lines
(e.g., A). The letters are presented in alphabetical order. During the task,
participants have to make judgments on either the letters that are shown on the
screen (i.e., exter-nal phase, stimulus oriented–SO), or the mental representations of
the letters (i.e., internal phase, stimulus independent–SI, when no letters are
displayed on the screen) – and these two phases alternate during the entire task.
Before performing the task, participants are required to recite the ABCs. Thereafter,
they are asked to carry out a training phase divided in two parts: (1) Participants are
first required to do one block of the external phase (SO). They receive the following
instructions: “In this task, you will see letters of the alphabet. If the letter is only
made of straight lines, press the left green key. For example as in the letter ‘A’. If the
letter contains one or several curves, press the right orange key. For example as in
the letter ‘B’”. (2) Thereafter, participants are asked to carry out a few blocks of the
source flexibility task. They receive the following instructions: “Sometimes, the
screen will become black. When this happens, simply keep reciting the ABCs in
your head and keep answering with the help of the keyboard. For example, if the
last letter you saw was ‘R’ and that the screen becomes black, you have to press the
right orange key because the next letter is ‘S’ and contains curves. At some point,
the letters will return to the screen”. The main task is composed of 156 trials divided
into 24 blocks (12 internal and 12 external blocks) of 5 to 8 letters. Participants
have an unlimited amount of time to judge each stimulus. Four reaction time (RT)
measures (excluding reaction times outside the range of 250–5000 ms) were
calculated and four percentage of errors measures were calculated corresponding to
the four conditions: SO, SI, SI to SO (i.e., participants switch from mental
representations to what is shown on the screen) and SO to SI (i.e., participants
switch from what is shown on the screen to mental representations).
Cognitive flexibility (Zimmermann & Fimm, 2010): During this computerised test,
pairs of letters and digits are simultaneously presented on a screen. Participants are
6 J. LALOYAUX ET AL.

required to press the key that is on the side of the target (digit or letter). The target
changes after each trial, thus participants have to alternate between digits and
letters. The median RT and percentage of errors were computed.
Processing speed (Schyns & Poncelet, 2002; Verhaegen & Poncelet, 2013): During
this computerised task, participants are required to judge as quickly as possible if
the digit (1 to 9) shown on the screen is odd or even. The median RT and percentage
of errors were computed.

Clinical measures
All patients were evaluated by an experienced clinical psychologist with the Psychotic
Symptom Rating Scale (PSYRATS; Favrod et al., 2012; Haddock, McCarron, Tarrier, &
Faragher, 1999). The PSYRATS is a measure of auditory hallucinations and delusions based
on a semi-structured interview assessing different characteristics of positive symp-toms. In
particular, the hallucinations subscale assesses the frequency of the voices, the dur-ation, the
location, the loudness, the origin, the amount and degree of negative content, the amount and
intensity of distress, the disruption to life, and the controllability. Similarly, the delusions
subscale assesses the amount and duration of the preoccupation with the delu-sions, the
conviction, the amount and intensity of distress, and the disruption to life.

Statistical analyses
Group comparisons for demographic variables were analysed using Student’s t-test and
Fisher’s exact test (Table 1). Thereafter, Repeated Measure ANOVAs were used to conduct
within and between group comparisons for the performance on the source flexi-bility task.
Post-hoc tests were computed using Fisher’s Least Significant Difference analy-sis (LSD).
Performance on the cognitive flexibility and processing speed tasks were compared between
groups using Student’s t-test. Moreover, Repeated Measure ANCOVA’s (covariance
analyses) were also conducted in order to control for a potential effect of processing speed
and cognitive flexibility on the source flexibility performance. Finally, Pearson’s
correlational analyses were conducted in the patient group between the cognitive measures
and the medication indexes (benzodiazepine, antipsychotic, antic-holinergic). Alpha was set
at 0.05. However, given the number of statistical analyses and the need to balance the
amount of type 1 and type 2 errors, the p value was adjusted with the false discovery rate
method for multiple testing (Benjamini & Hochberg, 1995), which controls for the expected
proportion of falsely rejected hypotheses (false discovery rate).
Thereafter, the patient group was split into two further groups based on the presence or
the absence of current auditory hallucinations. A similar operation was performed regard-ing
the presence or the absence of current delusions. Correlational analyses (Kendall’s Tau test)
were then conducted in the patient group between the source flexibility variables and the
hallucinations and delusions subscale scores (PSYRATS). The critical Tau value was defined
according to the sample size (Kaarsemaker & van Wijngaarden, 1953).

Results
A Repeated Measure ANOVA (Table 2 and Figure 2) was conducted for RT in the
different conditions of the source flexibility task in the patient group and the healthy
COGNITIVE NEUROPSYCHIATRY 7

Table 2. Mean reaction times on the source flexibility task in the two groups (Repeated
Measure ANOVA and LSD post hoc tests).
RT (ms) – SI to
RT (ms) – SO RT (ms) – SI SO RT (ms) – SO to SI
Mean (SE) Mean (SE) Mean (SE) Mean (SE) Within group post
1 2 3 4 hoc tests – LSD
Patients – Mean (SE) 1103.64 (35.35) 1381.07 (65.06) 1628.44 (94.34) 1931.08 (114.13) 1 < 2<3 < 4 ***
Controls – Mean (SE) 879.36 (30.31) 1022.17 (38.55) 1110.10 (56.35) 1276.63 (60.92) 1 < 3**
1 < 4***
2 < 4***
3 < 4*
1 = 2; 2 = 3
Between groups post Patients > Patients > Patients > Patients >
hoc tests – LSD Ctrls* Ctrls*** Ctrls*** Ctrls***
*p < 0.043 (Benjamini-Hochberg correction).
**p < 0.01.
***p < 0.001.

control group. Results revealed a significant main effect of the Group [F(1,64) = 22.55,
p = 0.00001], a significant main effect of the Condition [F(3,64) = 56.79, p < 0.00001]
and a significant interaction effect Group*Condition [F(3,64) = 7.41, p = 0.001]. With a
cor-rected alpha of 0.043 (Benjamini-Hochberg correction), LSD post hoc tests revealed
that the patients were significantly slower than the healthy controls in all the conditions
of the task. Within the patient group, results showed that the RT increased significantly
across the conditions and in particular between the stay and the switch conditions: SO
< SI < SI to SO < So to SI. Within the healthy control group, analyses revealed that the
RT for the switch conditions (SI to SO, SO to SI) were significantly slower than in the
stay conditions (SO and/or SI). In addition, the RT were found to be slower in the SO to
SI condition compared to the SI to SO condition.
Thereafter, the same analysis (Repeated Measure ANOVA) (Table 3 and Figure 2) was
conducted for the percentage of errors in the different conditions of the source flexibility task
in the patient group and the healthy control group. Results revealed a significant main effect
of the Group [F(1,64) = 5.95, p = 0.017] and a significant interaction effect Group*-
Condition [F(3,64) = 5.29, p = 0.001]. The main effect of the Condition was not significant
[F(3,64) = 1.12, p = 0.12]. With a corrected alpha of 0.018 (Benjamini-Hochberg correc-
tion), LSD post hoc tests revealed that the patients committed significantly more errors than
healthy controls in the SI and SO to SI conditions. Within the patient group, results showed
that the percentage of errors was higher for the SI and SO to SI conditions

Figure 2. Mean RT and percentage of errors on the source flexibility task for both groups.
8 J. LALOYAUX ET AL.

Table 3. Percentage of errors committed during the source flexibility task in the two
groups (Repeated Measure ANOVA and LSD post hoc tests).
Error % – SO Error % – SI Error % – SI to SO Error % – SO to SI
Mean (SE) Mean (SE) Mean (SE) Mean (SE) Between groups post
1 2 3 4 hoc tests – LSD
Patients – Mean (SE) 5.72 (1.43) 10.43 (2.32) 4.85 (1.85) 10.48 (2.38) 1 < 2**
1 < 4**
3 < 2***
3 < 4***
1 = 3; 2 = 4
Controls – Mean (SE) 2.05 (0.62) 2.73 (0.75) 4.49 (1.24) 1.28 (0.60) 1 = 2=3 = 4
Between groups post Patients = Patients > Patients = Ctrls Patients > Ctrls***
hoc tests – LSD Ctrls Ctrls**
*p < 0.018 (Benjamini-Hochberg correction).
**p < 0.01.
***p < 0.001.

compared to the SO and SI to SO conditions. Within the healthy control group, analyses
did not reveal any significant differences between the conditions.
Patients and healthy controls were then compared regarding their performance on the
cognitive flexibility and processing speed task (t-tests) (Table 4). Using a corrected
alpha of 0.05 (Benjamini-Hochberg correction – the alpha is unchanged as all the
analyses were highly significant), results revealed that the patients performed worse that
healthy controls for both tasks (i.e., slower RT and a higher percentage of errors).
The fact that most variables significantly differentiated both groups could suggest a global
impairment of processing speed in patients diagnosed with schizophrenia that, fur-thermore,
may have affected the performance on all the conditions of the source flexibility task. Thus,
Repeated Measure covariance analyses (ANCOVAs) were conducted compar-ing
performances between both groups on the source flexibility task while controlling for
processing speed. Results revealed that controlling for RT or the percentage of errors of the
processing speed task did not affect the original within and between group differences.
Repeated Measure covariance analyses (ANCOVAs) were also conducted in order to
examine if the group differences observed for the source flexibility task were not
explained by specific difficulties in cognitive flexibility. Results revealed that controlling
for RT or the percentage of errors of the cognitive flexibility task did not affect the
original within and between group differences on the source flexibility task.
Correlational analyses (Pearson) were then conducted in the patient group between
the medication indexes (benzodiazepine, antipsychotic, anticholinergic) and the
performance on the cognitive tasks (processing speed, cognitive flexibility and source
flexibility). Results revealed no significant correlations.

Table 4. Performance on the cognitive flexibility and processing speed task in the two groups.
Patients – Mean (SE) Healthy controls – Mean (SE) t (64)
Cognitive flexibility
RT (ms) 1543.56 (125.80) 828.21 (57.66) 4.38**
Error % 14.14 (1.73) 4.84 (0.82) 4.12**
Processing speed
RT (ms) 788.92 (20.64) 638.38 (25.90) 4.56**
Error % 12.48 (1.78) 4.10 (0.88) 3.63**
**p < 0.001.
COGNITIVE NEUROPSYCHIATRY 9

Correlational analyses (Kendall’s Tau test) were then conducted in patients with
current hallucinations (N = 15) between performance on the source flexibility task and
the different hallucination dimensions (PSYRATS). Results (Table 5) revealed that the
source flexibility variables were significantly related to several hallucination dimensions
including the duration, the loudness, the degree of negative content, the amount and
intensity of distress, and the disruption to life.
Finally, in order to examine the specificity of the relations between source flexibility
and hallucinations, correlational analyses (Kendall’s Tau test) were also conducted
between performance on the source flexibility task and different delusion dimensions
(PSYRATS) in patients with current delusions (N = 17). Results revealed no significant
correlations except between performance on the RT – SO to SI condition and the
intensity of distress (τ = 0.35; p < 0.05).

Discussion
The aim of the present study was to explore a potential impairment of source flexibility
in a group of persons diagnosed with schizophrenia and to examine if this cognitive
mech-anism could be explained by (1) a general impairment of processing speed and (2)
by specific difficulties in cognitive flexibility. A second aim was to assess the extent to
which source flexibility was related to specific schizophrenia symptoms such as auditory
hallucinations.
Results revealed that persons diagnosed with schizophrenia presented significantly slower
reaction times and a higher percentage of errors for all the cognitive measures, including
source flexibility, cognitive flexibility and processing speed. More specifically, patients
presented a significant slowing for all source flexibility conditions, that is, during the
external (SO) and internal condition (SI) and during both switching conditions (SO to SI and
SI to SO). Concerning the percentages of errors, results demonstrated that patients
committed significantly more errors than healthy controls in the SI and SO to SI conditions.
In addition, within group analyses revealed that both groups showed a similar pattern of
increasing reaction times across the conditions and, in particular, between the stay (SI and
SO) and the switch (SO to SI and SI to SO) conditions, whereby the SO to SI condition was
the slowest. These results are in agreement with the study by Gilbert et al. (2005) in which
the authors reported a similar pattern in healthy participants and, in par-ticular, that the SO to
SI condition was the slowest, and the SO the fastest. Nevertheless, it is interesting to
underline that Gilbert et al. (2005) found that participants were faster in the SI to SO
condition compared to the SI condition, whereas it was the opposite in the present study.
This difference may be explained by the fact that the task used in the present study was
easier than the one used by Gilbert et al. (2005). More specifically, in the version of the task
used in Gilbert et al. (2005), letters were presented in alphabetical order except that two
letters were skipped between each stimuli (e.g., A – D – E), whereas the task used in the
present study did not skip any letters (e.g., A – B – C). It is thus poss-ible to hypothesise that
the original task is more demanding than the task used in the present study. Finally, within
group analyses also showed that, whereas healthy controls demonstrated equivalent error
rates across the conditions, the patients committed signifi-cantly more errors in the internal
and in the external to internal conditions (SI and SO to SI) than in the external and internal
to external conditions (SO and SI to SO). Such results
10
J. LALOYAUX ET AL.
Table 5. Correlations between cognitive variables and hallucination dimensions (PSYRATS).
Hallucinations
Amount of negative Degree of negative Amount of Intensity of Disruption to
Source flexibility Frequency Duration Location Loudness Origin content content distress distress life Controllability
Reaction time – SO −0.16 0.35* −0.11 −0.23 −0.01 0.02 −0.02 −0.02 0.15 0.10 −0.23
(ms) −0.05 −0.05 −0.34* −0.09
Reaction time – SI 0.33* 0.18 0.02 0.04 0.11 0.03 0.11
(ms) −0.12 −0.29 −0.11
Reaction time – SI to 0.40** 0.05 0.03 0.19 0.04 0.11 0.26 0.12
SO (ms) −0.19 −0.07 −0.13 −0.08
Reaction time – SO 0.42* 0.20 0.17 0.02 0.15 0.36* 0.21
to SI (ms) −0.15 −0.39** −0.15 −0.09 −0.22
Error % – SO 0.28 0.01 0.26 0.42** 0.32 0.29
Error % – SI −0.24 −0.11 −0.10 0.24 0.16 0.32 0.29 0.38* 0.41** 0.13 −0.26
Error % – SI to SO 0.11 −0.21 −0.13 0.51*** −0.11 −0.19 0.05 −0.20 −0.05 −0.36* −0.12
Error % – SO to SI −0.09 −0.20 0.00 0.39** 0.23 0.06 0.10 0.14 0.22 0.23 0.08
Note: p values corresponding to the critical Tau values defined according to the sample size (Kaarsemaker & van Wijngaarden, 1953).
*p < 0.05.
**p < 0.025.
***p < 0.01.
COGNITIVE NEUROPSYCHIATRY 11

suggest that patients have particular difficulties in maintaining and switching to internal
representations.
As expected, patients with schizophrenia demonstrated a significant lower performance
on all tasks, which could suggest a global impairment of processing speed that a ffected all
performances. However, controlling for the reaction times or the percentage of errors of the
processing speed task on the source flexibility performance did not affect the original
differences. These results demonstrate that despite difficulties in processing speed, patients
still demonstrated lower performances than healthy controls on the source flexibility
measure. These results thus suggest that these differences could not be explained by a global
impairment of processing speed. We also examined whether differences observed between
patients and healthy controls for the source flexibility task could be explained by specific
difficulties in cognitive flexibility. Results revealed that controlling for reaction times or the
percentage of errors of the cognitive flexibility task did not affect the original differences.
These results thus demonstrate that differences between patients and healthy controls on the
source flexibility task cannot be attributed to poor cognitive flexibility abil-ities, suggesting
that source flexibility and cognitive flexibility can be seen as relatively independent cognitive
mechanisms.
Finally, no significant correlations were found in the patient group between
medication and performance on the various cognitive tasks (processing speed, cognitive
flexibility and source flexibility) suggesting that the performance on these tasks was not
impacted by medication.
In summary, both between and within group analyses showed that patients presented
a global slowing in all the conditions of the source flexibility task compared to healthy
con-trols, but that a similar pattern of reaction times across the conditions was observed.
Con-cerning the error rate, patients significantly committed more errors that healthy
controls in the internal and external to internal conditions (SI and SO to SI), but not in
the external and internal to external conditions (SO and SI to SO). In addition, whereas
healthy con-trols had an equivalent error rate across the conditions, the patients
committed signifi-cantly more errors in the internal and external to internal conditions
(SI and SO to SI) than in the external and internal to external conditions (SO and SI to
SO). No differences in these results were observed when controlling for both processing
speed and cognitive flexibility. Taken together, the results show that patients presented a
global slowing for all the conditions of the source flexibility task while at the same time
showed particular difficulties in maintaining and switching to internal representations.
We have no clear explanation for this profile of difficulties and future studies are clearly
required to further explore source flexibility in schizophrenia.
It could be suggested that the difficulties encountered by the patients in the SI con-
ditions led to the difficulties in the external to internal switching condition. However,
this explanation seems unlikely as patients demonstrated a global slowing for all the
con-ditions (and even after controlling for processing speed) suggesting the presence of
difficulties (but to a lesser extent) in the external (SO) and in the internal to external
con-ditions (SI to SO) as well.
In the source flexibility task, the fact that the error rate of only one switching condition
(the SO to SI condition but not the SI to SO condition) significantly differentiated both
groups is surprising. Nevertheless, these results may be explained by the particular difficul-
ties encountered by patients in that condition. Indeed, within group analyses revealed that
12 J. LALOYAUX ET AL.

the SO to SI condition was the slowest in both groups. However, while the healthy
controls showed a stable error rate across the conditions, patients were found to make
more errors in the conditions related to internal representations (SI and SO to SI). Taken
together, these results suggest that the healthy controls needed more time to maintain
low error rates. On the contrary, this slowing strategy does not seem to be effective in
patients when considering the fact that they already have difficulties in maintaining
internal representations.
It could be asked whether the difficulties in source flexibility observed in the patient
group could be explained by general difficulties in orthographic judgement. This expla-
nation appears unlikely, however, when considering the present results. In particular, the
results demonstrated a global slowing of patients in all the conditions of the source
flexibility task but failed to demonstrate significant differences between patients and
healthy controls for the percentage of errors committed during the external phase (SO)
and the internal to external phase (SI to SO). These results suggest that patients were
able to perform the orthographic judgement task but simply required more time to do so.
On the contrary, patients showed significantly higher error rates for the internal (SI) and
external to internal (SO to SI) conditions, suggesting that they have particular difficul-
ties in maintaining internal representations and difficulties in switching to them.
Finally, it is important to mention that the difficulties in source flexibility observed in
the patient groups may be related to other cognitive impairments. Indeed, patients with
schizophrenia usually present cognitive deficits in many domains such as processing
speed, working and episodic memory, and executive functions (Bortolato et al., 2015).
In fact, the gateway hypothesis (Burgess, Dumontheil et al., 2007; Burgess et al., 2005)
suggests that source flexibility is involved in many cognitive abilities, which would
explain why activation of the rostral prefrontal cortex can be observed when carrying
out many cognitive tasks, from the basic (e.g., auditory perception) to the most difficult
(e.g., problem solving) (Burgess et al., 2005). Thus, impaired source flexibility abilities
could potentially lead to many other cognitive deficits. Future studies are required to
explore the relations between source flexibility abilities and other cognitive domains.
A last aim of this study was to investigate the relations between source flexibility
abil-ities and hallucinations. Results revealed that the different variables on the source
flexi-bility task were significantly related to several hallucination characteristics
including the duration, the loudness, the amount of negative content, the distress, and
the disruption to life. These results suggest that difficulties in maintaining attention to
one’s internal (e.g., thoughts) and external world, and difficulties in switching from one
to the other, are underlying mechanisms in hallucinations. In addition, results revealed
that these relations were specific to hallucinations as only one (out of 48) significant
correlation was observed for delusions (that is between the distress associated with the
delusions and the abilities to switch from the outside world to internal representations).
Indeed, difficulties in discriminating between internal and external events are a main
characteristic of hallucinations (Brookwell et al., 2013; Waters et al., 2012). The present
results suggest that source flexibility could be one underpinning mechanism of these dis-
crimination difficulties as the person constantly loses track of what he/she is attending to and
presents difficulties in switching from the internal world to the external world and vice
versa. This hypothesis is based on the assumption that source flexibility is a fundamental
cognitive mechanism (Burgess, Dumontheil et al., 2007; Burgess et al., 2005). Such results
COGNITIVE NEUROPSYCHIATRY 13

are also consistent with the self-regulatory executive function model (Wells &
Matthews, 1994) that proposes a dysfunctional pattern of information processing that is
characterised by self-focused attention that becomes excessive, inflexible, and
uncontrollable – render-ing the treatment of external information difficult. However, the
present results also suggest that auditory hallucinations are not only related to
difficulties in attending to the external world but also to difficulties in maintaining
attention to the internal world and in switching between these sources. Such results can
also be related to the literature showing that patients diagnosed with schizophrenia –
and in particular those with hallu-cinations – present self-recognition deficits
(Brookwell et al., 2013; Waters et al., 2012). Indeed, between group analyses suggested
that patients with schizophrenia present global difficulties in source flexibility and, in
particular, in maintaining and switching to internal representations. In addition, source
flexibility abilities were found to be related to different hallucination characteristics.
Such results suggest that difficulties in source flexibility may create confusions between
internal and external sources and facilitate the externalisation of internal events. Future
studies are required to specifically explore the relations between source flexibility and
difficulties in discriminating between internal and external sources.
The results observed in the present study have several implications for the treatment of
hallucinations. In particular, regarding the self-regulatory executive function model (Wells
& Matthews, 1994), Wells (1990, 2006) described an Attention Training Technique (ATT)
designed to reduce excessive self-focused attention and to increase metacognitive monitor-
ing. The ATT is composed of auditory external attentional exercises during which several
sounds (e.g., sounds from a radio or a fan) are introduced in the consulting room and outside
of the consulting room (e.g., behind the door). Participants are required to pay atten-tion to
one or several sounds at the same time and to switch their attention between them. If an
internal event occurs (e.g., a thought, a hallucination), participants are asked not to react to it
but to re-focus their attention on the sounds. Recently, a case study (Levaux, Larøi, Offerlin-
Meyer, Danion, & Van der Linden, 2011) demonstrated that the ATT was effective in
reducing positive symptoms in a patient diagnosed with schizophrenia. The results of the
present study suggest that adding a specific training strategy that aims to increase both the
focus on the internal world, and the switching abilities between the internal and the external
world, would also help in reducing hallucinations.
This study contains several limitations that need to be mentioned. The main limitation is
related to the transversal design of the study, which does not allow one to conclude to causal
relationships between difficulties in source flexibility and hallucinations. Longitudi-nal
studies are thus required in order to establish a causal relationship. In particular, it is not
known whether difficulties in source flexibility are a stable trait or not, and whether they
precede the onset of hallucinations or coincide with them. An alternative approach would
consist in comparing source flexibility abilities between patients with or without a history of
hallucinations. Another limitation is related to the fact that only a small number of patients
with current hallucinations were included, thus limiting the study’s statistical power.
However, as this section of the study was exploratory, it was decided not to correct the alpha
for multiple testing for fear of missing potentially meaningful findings that could be explored
in follow-up studies with more patients. However, this is the first study of its kind to have
explored source flexibility as being a potential cognitive mechanism implicated in
hallucinations and the results are encouraging.
14 J. LALOYAUX ET AL.

Disclosure statement
No potential conflict of interest was reported by the authors.

Acknowledgement
The authors have nothing to declare.

References
American Psychiatric Association. (1994). Diagnostic and statistical manual of mental
disorders (4th ed). Washington, DC: American Psychiatric Association Press.
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and
powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B,
57(1), 289–300. doi:10.2307/2346101
Boily, M.-J., & Mallet, L. (2008). Comment évaluer la charge anticholinergique? Pharmactuel,
41 (Sup. 1), 32–36. Retrieved from http://www.pharmactuel.com/pharmactuel/index.php/
pharmactuel/article/view/963/624
Bortolato, B., Miskowiak, K. W., Kohler, C. A., Vieta, E., & Carvalho, A. F. (2015). Cognitive
dys-function in bipolar disorder and schizophrenia: A systematic review of meta-analyses.
Neuropsychiatric Disease and Treatment, 11, 3111–3125. doi:10.2147/ndt.s76700
Brookwell, M. L., Bentall, R. P., & Varese, F. (2013). Externalizing biases and hallucinations in
source-monitoring, self-monitoring and signal detection studies: A meta-analytic review.
Psychological Medicine, 43(12), 2465–2475. doi:10.1017/s0033291712002760
Burgess, P. W., Dumontheil, I., & Gilbert, S. J. (2007). The gateway hypothesis of rostral prefrontal cortex
(area 10) function. Trends in Cognitive Sciences, 11(7), 290–298. doi:10.1016/j.tics.2007.05.004 Burgess,
P. W., Gilbert, S. J., & Dumontheil, I. (2007). Function and localization within rostral pre-frontal cortex (area
10). Philosophical Transactions of the Royal Society B: Biological Sciences, 362
(1481), 887–899. doi:10.1098/rstb.2007.2095
Burgess, P. W., Simons, J. S., Dumontheil, I., & Gilbert, S. J. (2005). The gateway hypothesis of rostral
prefrontal cortex (area 10) function. In J. Duncan, L. Phillips, & P. McLeod (Eds.), Measuring the mind:
Speed, control and age (pp. 217–248). New York: Oxford University Press.
Davis, J. M., & Chen, N. (2004). Dose response and dose equivalence of antipsychotics. Journal of
Clinical Psychopharmacology, 24(2), 192–208. doi:10.1097/01.jcp.0000117422.05703.ae
Dickinson, D., Ragland, J. D., Gold, J. M., & Gur, R. C. (2008). General and specific cognitive
deficits in schizophrenia: Goliath defeats David? Biological Psychiatry, 64(9), 823–827.
doi:10.1016/j. biopsych.2008.04.005
Dickinson, D., Ramsey, M. E., & Gold, J. M. (2007). Overlooking the obvious: A meta-analytic
com-parison of digit symbol coding tasks and other cognitive measures in schizophrenia.
Archives of General Psychiatry, 64(5), 532–542. doi:10.1001/archpsyc.64.5.532
Favrod, J., Rexhaj, S., Ferrari, P., Bardy, S., Hayoz, C., Morandi, S., … Giuliani, F. (2012). French
version validation of the psychotic symptom rating scales (PSYRATS) for outpatients with per-
sistent psychotic symptoms. BMC Psychiatry, 12(1), 1–7. doi:10.1186/1471-244X-12-161
Gardner, D. M., Murphy, A. L., O’Donnell, H., Centorrino, F., & Baldessarini, R. J. (2010).
International consensus study of antipsychotic dosing. American Journal of Psychiatry,
167(6), 686–693. doi:10.1176/appi.ajp.2009.09060802
Gilbert, S. J., Frith, C. D., & Burgess, P. W. (2005). Involvement of rostral prefrontal cortex in
selec-tion between stimulus-oriented and stimulus-independent thought. European Journal of
Neuroscience, 21(5), 1423–1431. doi:10.1111/j.1460-9568.2005.03981.x
Haddock, G., McCarron, J., Tarrier, N., & Faragher, E. B. (1999). Scales to measure dimensions
of hallucinations and delusions: The psychotic symptom rating scales (PSYRATS).
Psychological Medicine, 29(4), 879–889.
Kaarsemaker, L., & van Wijngaarden, A. (1953). Tables for use in rank correlation. Statistica
Neerlandica, 7(1), 41–54.
COGNITIVE NEUROPSYCHIATRY 15

Levaux, M.-N., Larøi, F., Offerlin-Meyer, I., Danion, J. M., & Van der Linden, M. (2011). The
effec-tiveness of the attention training technique in reducing intrusive thoughts in
schizophrenia. Clinical Case Studies, 10(6), 466–484. doi:10.1177/1534650111435696
Levaux, M.-N., Van der Linden, M., Larøi, F., & Danion, J.-M. (2012). Caractérisation des difficultés
dans la vie quotidienne de personnes souffrant de schizophrénie en rapport avec les facteurs cog-
nitifs et cliniques. ALTER – European Journal of Disability Research / Revue Européenne de
Recherche sur le Handicap, 6(4), 267–278. doi:10.1016/j.alter.2012.08.003
Mittal, P. K., Mehta, S., Solanki, R. K., & Swami, M. K. (2014). A comparative study of cognitive
flexibility among first episode and multi-episode young schizophrenia patients. German Journal of
Psychiatry, 16(4), 130–136. Retrieved from http://www.gjpsy.uni-goettingen.de/
Orellana, G., & Slachevsky, A. (2013). Executive functioning in schizophrenia. Frontiers in
Psychiatry, 4, 35. doi:10.3389/fpsyt.2013.00035
Schyns, T., & Poncelet, M. (2002). Cognitive processing speed task. Unpublished manuscript.
Taylor, D., Paton, C., & Kapur, S. (2009). The maudsley prescribing guidelines (10th ed). London:
Informa Healthcare.
Thoma, P., Wiebel, B., & Daum, I. (2007). Response inhibition and cognitive flexibility in schizo-
phrenia with and without comorbid substance use disorder. Schizophrenia Research, 92(1–
3), 168–180. doi:10.1016/j.schres.2007.02.004
Verhaegen, C., & Poncelet, M. (2013). Changes in naming and semantic abilities with aging from
50 to 90 years. Journal of the International Neuropsychological Society, 19(2), 119–126.
doi:10.1017/ s1355617712001178
Waters, F., Woodward, T., Allen, P., Aleman, A., & Sommer, I. (2012). Self-recognition deficits in
schizophrenia patients with auditory hallucinations: A meta-analysis of the literature.
Schizophrenia Bulletin, 38(4), 741–750. doi:10.1093/schbul/sbq144
Wells, A. (1990). Panic disorder in association with relaxation induced anxiety: An attentional
training approach to treatment. Behavior Therapy, 21(3), 273–280. doi:10.1016/S0005-7894
(05)80330-2
Wells, A. (2006). Detached mindfulness in cognitive therapy: A metacognitive analysis and ten
techniques. Journal of Rational-Emotive and Cognitive-Behavior Therapy, 23(4), 337–
355. doi:10.1007/s10942-005-0018-6
Wells, A., & Matthews, G. (1994). Attention and emotion: A clinical perspective. Hove, UK:
Erlbaum.
Zimmermann, P., & Fimm, B. (2010). Tests d’évaluation de l’attention version 2.3 (TAP).
Herzogenrath: Psytest.

Вам также может понравиться