Neuropsychology

Association of Auditory-Verbal and Visual Hallucinations

With Impaired and Improved Recognition of Colored
Pictures
Gildas Brébion, Christian Stephan-Otto, Judith Usall, Elena Huerta-Ramos, Mireia Perez del
Olmo, Jorge Cuevas-Esteban, Josep Maria Haro, and Susana Ochoa
Online First Publication, January 26, 2015. http://dx.doi.org/10.1037/neu0000169

CITATION
Brébion, G., Stephan-Otto, C., Usall, J., Huerta-Ramos, E., Perez del Olmo, M.,
Cuevas-Esteban, J., Haro, J. M., & Ochoa, S. (2015, January 26). Association of
Auditory-Verbal and Visual Hallucinations With Impaired and Improved Recognition of
Colored Pictures. Neuropsychology. Advance online publication.
http://dx.doi.org/10.1037/neu0000169
 Neuropsychology © 2015 American Psychological Association
2015, Vol. 28, No. 6, 000 0894-4105/15/$12.00 http://dx.doi.org/10.1037/neu0000169

Association of Auditory-Verbal and Visual Hallucinations With Impaired

and Improved Recognition of Colored Pictures

Gildas Brébion Christian Stephan-Otto

Parc Sanitari Sant Joan de Déu and Centro de Investigación Fundació Sant Joan de Déu, Barcelona, Spain
Biomédica en Red de Salud Mental, Barcelona, Spain

Judith Usall, Elena Huerta-Ramos, Mireia Perez del Olmo, Jorge Cuevas-Esteban, Josep Maria Haro,
and Susana Ochoa
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

Parc Sanitari Sant Joan de Déu and Centro de Investigación Biomédica en Red de Salud Mental, Barcelona, Spain
This document is copyrighted by the American Psychological Association or one of its allied publishers.

Objective: A number of cognitive underpinnings of auditory hallucinations have been established in

schizophrenia patients, but few have, as yet, been uncovered for visual hallucinations. In previous
research, we unexpectedly observed that auditory hallucinations were associated with poor recognition
of color, but not black-and-white (b/w), pictures. In this study, we attempted to replicate and explain this
finding. Potential associations with visual hallucinations were explored. Method: B/w and color pictures
were presented to 50 schizophrenia patients and 45 healthy individuals under 2 conditions of visual
context presentation corresponding to 2 levels of visual encoding complexity. Then, participants had to
recognize the target pictures among distractors. Results: Auditory-verbal hallucinations were inversely
associated with the recognition of the color pictures presented under the most effortful encoding
condition. This association was fully mediated by working-memory span. Visual hallucinations were
associated with improved recognition of the color pictures presented under the less effortful condition.
Patients suffering from visual hallucinations were not impaired, relative to the healthy participants, in the
recognition of these pictures. Conclusion: Decreased working-memory span in patients with auditory-
verbal hallucinations might impede the effortful encoding of stimuli. Visual hallucinations might be
associated with facilitation in the visual encoding of natural scenes, or with enhanced color perception
abilities.

Keywords: hallucinations, visual memory, schizophrenia

Hallucinations are very common in patients with schizophrenia.
They have been linked to deficits in the cognitive processes enabling
reality discrimination, reality monitoring, self-monitoring, and source
monitoring (Bentall, 1990; Brookwell, Bentall, & Varese, 2013; Frith,
1992; Johnson, Hashtroudi, & Lindsay, 1993; Larøi & Woodward,
2007; Woodward & Menon, 2011). More specifically, auditory-
Gildas Brébion, Unit of Research and Development, Parc Sanitari Sant Joan
de Déu and Centro de Investigación Biomédica en Red de Salud Mental,
Barcelona, Spain; Christian Stephan-Otto, Unit of Research and Development,
Parc Sanitari Sant Joan de Déu and Centro de Investigación Biomédica en Red
de Salud Mental, Barcelona, Spain, and Fundació Sant Joan de Déu, Barce-
lona, Spain; Judith Usall, Elena Huerta-Ramos, Mireia Perez del Olmo, Jorge
Cuevas-Esteban, Josep Maria Haro, and Susana Ochoa, Unit of Research and
Development, Parc Sanitari Sant Joan de Déu and Centro de Investigación
Biomédica en Red de Salud Mental, Barcelona, Spain.
We thank Dr Mercedes Roca and Ms Montserrat Contel for helping with
the recruitment of patients. This study was funded by a Miguel Servet
contract at CIBERSAM and a grant from the Fondo de Investigación
Sanitaria, Spanish Ministry of Health (PI10/02479), to Gildas Brébion.
Correspondence concerning this article should be addressed to Gildas
Brébion, Unit of Research and Development, PSSJD, C/ Doctor Antoni
Pujadas 42, 08830 Sant Boi de Llobregat (Barcelona) Spain. E-mail:
gildas.brebion@pssjd.org
1
verbal hallucinations have been associated with disturbance in self-
monitoring of language (Allen, Aleman, & McGuire, 2007;
Brébion, David, Bressan, Ohlsen, & Pilowsky, 2009; Ditman &
Kuperberg, 2005; Jones, 2010; Moseley, Fernyhough, & Ellison,
2013; Shergill, Bullmore, Simmons, Murray, & McGuire, 2000),
self-monitoring of actions (Gaweda, Woodward, Moritz, & Koko-
szka, 2013), and self-recognition of one’s own productions or
actions (Waters, Woodward, Allen, Aleman, & Sommer, 2012).
They have also been associated with deficits in remembering the
temporal (Brébion, David, Jones, Ohlsen, & Pilowsky, 2007; Wa-
ters, Badcock, Michie, & Maybery, 2006) and spatial (Brébion,
David, Ohlsen, Jones, & Pilowsky, 2007) sources of events, and
with faulty mechanisms of intentional inhibition (Badcock, Wa-
ters, Maybery, & Michie, 2005; Soriano, Jiménez, Román, & Bajo,
2009; Waters, Badcock, Maybery, & Michie, 2003).
Visual hallucinations, which are less prevalent in schizophrenia,
have been the object of much scantier investigation. Collerton et
al. (2005) emphasized the role of perceptual and attentional im-
pairment in recurrent complex visual hallucinations occurring un-
der various conditions. We observed in a previous schizophrenia
sample that visual hallucinations were associated with confusion
between mental images and perception (Brébion, Ohlsen, Pi-
lowsky, & David, 2008), as well as with reduced use of verbal
strategies in the learning of lists of words (Brébion, Ohlsen,
 2 BRÉBION ET AL.
Pilowsky, & David, 2011). This latter finding suggests increased
use of a visual imagery strategy in these patients.
In previous research on visual memory in schizophrenia
(Brébion, David, Ohlsen, et al., 2007), we presented mixed black-
and-white (b/w) and color pictures at different locations, with each
location indicated by a small image that constituted the visuospa-
tial context. We unexpectedly observed that auditory hallucina-
tions were associated with subsequent impairment in recognizing
the color pictures among similar distracters after a delay of a few
minutes. This suggests that patients with auditory hallucinations
had not properly encoded these color pictures during the presen-
tation phase, or were impaired in maintaining them in memory
over the delay. No association with the recognition of the b/w
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
pictures emerged. Although the use of visual material might have
This document is copyrighted by the American Psychological Association or one of its allied publishers.
facilitated the emergence of potential associations with visual
hallucinations, no such association was uncovered.
The inverse association between auditory hallucinations and
recognition of the color pictures was challenging. Indeed, positive
symptoms of schizophrenia have generally been found to be fairly
independent of cognitive efficiency (Dibben, Rice, Laws, & Mc-
Kenna, 2009; Ventura, Thames, Wood, Guzik, & Hellemann,
2010). Patients with auditory hallucinations might be abnormally
distracted by chromatic information, and hence disregard the other
characteristics of the stimuli. This would lead to incomplete en-
coding of the color pictures. Alternatively, the crux might be that
the color pictures contain richer and more complex information
than do the b/w pictures, and therefore they require deeper pro-
cessing. Patients with auditory hallucinations might be generally
impaired in conducting deep/effortful processing. Indeed,
auditory-verbal hallucinations have been associated with impair-
ment in working memory (Bruder et al., 2011; Gisselgård et al.,
2014), a cognitive system allegedly involved in complex cognitive
operations (Baddeley, 2012). We previously reported that the
encoding of color pictures was constrained by working-memory
capacity, whereas the encoding of b/w pictures was not (Brébion,
Bressan, Pilowsky, & David, 2011), and that this association with
working memory was significant only when the encoding of the
color pictures was effortful (Brébion et al., 2014). A reduced
working-memory span in patients with auditory hallucinations
might lead them to ineffective encoding of the pictures that require
the most effortful processing.
The first objective of the current study was to replicate and
attempt to clarify our previous unexpected finding of an inverse
association between auditory hallucinations and recognition of
color pictures, because an understanding of this association might
shed new light on the nature of auditory hallucinations. We mod-
ified our visual memory task so that the procedure would presum-
ably enable us to determine whether it was the color itself that
impeded efficient picture encoding in patients with auditory hal-
lucinations, or if the impairment resulted from the greater com-
plexity of the stimuli to be processed. B/w and color pictures were
presented separately so as to isolate the effect of color. The visual
context used in our previous study (small images displayed at
different locations) was decomposed into its two aspects: pictures
were presented either at different locations, or centrally, but in
association with a small image. These two encoding conditions
corresponded to two levels of complexity. It was assumed that
encoding two associated visual stimuli was especially demanding,
whereas encoding the spatial location of stimuli relied on more
automatic processes (Ellis, 1990). We contrasted immediate and
delayed recognition conditions to ascertain that the alleged effect
of auditory-verbal hallucinations occurred at the encoding stage—
reflected by immediate recognition performance— because both
hypotheses that we propose postulate impaired encoding of the
color pictures. A working-memory task was administered as well.
Following on from our previous finding, we hypothesized that
auditory-verbal hallucinations were associated with impaired rec-
ognition of color, but not b/w, pictures. The specific pattern of
associations with each visual encoding condition was expected to
illuminate the mechanism involved. If the association between
auditory hallucinations and impaired recognition of color pictures
stemmed from difficulty in conducting effortful processing as a
consequence of decreased working-memory capacity, we should
expect the following pattern: (a) auditory-verbal hallucinations
would be inversely associated with working-memory span, (b) the
association between picture recognition and auditory-verbal hallu-
cinations would pertain to the color pictures presented under the
“association” condition rather than those presented under the “lo-
cation” condition, and (c) controlling for the working-memory
span would abolish this association. Alternatively, if patients with
auditory-verbal hallucinations are cognitively hampered by the
very chromatic properties of the color pictures regardless of task
difficulty, the association between auditory-verbal hallucinations
and color picture recognition should be equally observed for both
conditions of visual encoding, and it should be unaffected by
statistical control of working-memory span.
A second objective of our study was to investigate the associ-
ations of picture recognition with visual hallucinations. Our sam-
ple presented a greater prevalence of hallucinations than in our
previous study, especially with respect to visual hallucinations,
and therefore associations with this clinical symptom were more
likely to be disclosed. However, given the lack of previous data
concerning any relationship between visual memory and visual
hallucinations, potential associations were studied in an explor-
ative way.
Method
Subjects
Fifty in-patients with schizophrenia (per DSM–IV criteria; APA,
1994) were recruited from various units for chronic and acute
pathology within the Parc Sanitari Sant Joan de Déu network of
mental health services in Barcelona, Spain: 34 men, 16 women;
aged M ⫽ 47.3, SD ⫽ 10.2; education level1: M ⫽ 3.2, SD ⫽ 1.4;
verbal IQ (Test de Acentuación de Palabras; TAP; Gomar et al.,
2011)2: M ⫽ 16.2, SD ⫽ 5.6; illness duration: M ⫽ 19.9 years,
SD ⫽ 12.2. The exclusion criteria were alcohol or drug abuse (per
DSM–IV criteria) within the previous 6 months, organic mental
disorders, intellectual disability (IQ ⬍ 70), history of brain injury,
dementia, and current severe physical disease. All patients were
1
The scale used was: 1 ⫽ no studies; 2 ⫽ uncompleted primary studies;
3 ⫽ completed primary studies; 4 ⫽ high school uncompleted; 5 ⫽ high
school completed; 6 ⫽ undergraduate studies; 7 ⫽ bachelor’s or master’s
degree; 8 ⫽ doctorate.
2
The equivalent estimated verbal IQs are 16.2 ⫽ 89 and 20.4 ⫽ 97
(Gomar et al., 2011).
 HALLUCINATIONS AND RECOGNITION OF COLOR PICTURES 3

receiving antipsychotic medication and were clinically stable—
that is, were at a stabilized dose of medication—at the time of
testing.
Forty-five healthy control participants were recruited from the
community: 27 men, 18 women aged M ⫽ 45.1, SD ⫽ 9.1;
education level1: M ⫽ 4.8, SD ⫽ 1.2; verbal IQ (TAP)2: M ⫽ 20.4,
SD ⫽ 4.7. They were screened by telephone interview to rule out
current or recent alcohol abuse, drug abuse, and psychiatric dis-
ease, as well as severe current nonpsychiatric disease. The two
groups were not significantly different in age or sex distribution.
However, the level of education was significantly higher in the
control group, as was the score on the vocabulary test (TAP), a
Spanish equivalent of the National Adult Reading Test (NART;
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Procedure. The 16 target pictures from the first set were
displayed on the table in trials of four b/w or four color pictures.
In the “location” context condition they were placed at one of four
different locations (top left, top right, bottom left, bottom right). In
the “association” context condition they were displayed in the
center, each beneath one of four small schematic color images that
constituted the visual context. The subjects were presented with
four b/w location pictures, four color location pictures, four b/w
association pictures, and four color association pictures, in a coun-
terbalanced order (see Figure 1 for an example). They were in-
structed to commit to memory not only the pictures themselves,
but also where these pictures were located or with which image
each was associated. The exposure duration was 20 s for each trial

Nelson, 1982), used to assess verbal IQ. of four pictures.

This document is copyrighted by the American Psychological Association or one of its allied publishers.

Ethical approval for the study was obtained from the Parc
Sanitari Sant Joan de Déu Research and Ethics Committee. After
a full explanation of the study, subjects provided written informed
consent.

Clinical Ratings
Hallucinations were assessed by means of the Spanish version
of the Scale for the Assessment of Positive Symptoms (Peralta &
Cuesta, 1999). An auditory-verbal hallucination score was com-
puted by adding up the scores obtained on the first, second, and
third items of the hallucination subscale (auditory hallucinations,
voices commenting, and voices conversing; M ⫽ 4.8, SD ⫽ 3.4,
range ⫽ 0 –12). The score obtained on the visual hallucinations
item was tallied (M ⫽ 1.0, SD ⫽ 1.3, range ⫽ 0 – 4). An olfactory/
tactile hallucination score was computed by adding up the scores
on the two items pertaining to these types of hallucinations (M ⫽
1.5, SD ⫽ 1.8, range ⫽ 0 – 6). Forty-one patients presented
auditory-verbal hallucinations (score ⬎ 1); 17 patients presented
visual hallucinations (score ⬎ 1; all of them except one also
presented auditory-verbal hallucinations); 21 patients presented
olfactory/tactile hallucinations (similarly, all of them except one
also presented auditory-verbal hallucinations); seven patients did
not present hallucinations of any kind. Clinical assessment was
conducted shortly after the completion of the task by a trained
clinical psychologist who was blinded to the study hypotheses.

Material and Procedure

Working-memory span. The letter–number span from the
Wechsler Adult Intelligence Scale-III (WAIS-III; Wechsler, 1997)
was administered. Increasingly long series of mixed letters and
digits were read aloud by the experimenter. The participants had to
repeat the series in a reorganized order, first putting the digits in
ascending order, and then the letters in alphabetical order. The
total number of correct trials was used as a measure of working-
memory capacity.
Picture recognition.
Material. Two sets of 32 representational pictures from art
galleries were prepared, one for immediate and one for delayed
recognition. Each set comprised 16 pictures (eight b/w and eight
color) to be used as targets, and 16 pictures (eight b/w and eight
color) to be used as distractors. The use of each picture in its b/w Figure 1. Example of the picture-presentation procedure in the experi-
or color version, as target or distractor, in the immediate or delayed mental condition “location– color, location– black/white, association–
recognition condition, and within each type of visuospatial con- color, association– black/white. See the online article for the color version
text, was counterbalanced among subjects. of this figure.
 4 BRÉBION ET AL.

The presentation of the pictures was followed by a delay of Associations Between Picture Recognition
approximately 20 min, during which time unrelated verbal tasks and Hallucinations
were completed. The 16 target pictures were then mixed with the
16 distractor pictures from the set. These 32 pictures were pre- A correlational analysis indicated that the three hallucination
sented one by one in random order. The subjects were required to scores were significantly and positively intercorrelated (auditory-
verbal and visual hallucination scores: r ⫽ .42, p ⬍ .002; auditory-
indicate whether the picture had been previously presented or was
verbal and olfactory/tactile hallucination scores: r ⫽ .44, p ⬍ .001;
new. The number of correct recognitions of target pictures, and
visual and olfactory/tactile hallucination scores: r ⫽ .48, p ⬍
false recognitions of new pictures, was tallied for the b/w and color
.0001). Regression analyses were conducted in patients on the
pictures. The Pr index, reflecting ability to discriminate the targets
recognition indices (Pr) from each condition, with auditory-verbal
from the distractors (Corwin, 1994), was computed for each type
and visual hallucination scores as predictors. The olfactory and
of picture (Pr-b/w delayed recognition, and Pr-color delayed rec-
tactile hallucination score was also entered to demonstrate the
ognition). The corresponding Br indices reflecting the propensity specificity of potential associations with auditory-verbal and visual
to make false recognitions of nontarget pictures in case of uncer-
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

hallucinations. Last, sex was entered because it was found to have

tainty were computed as well. We also tallied the number of
This document is copyrighted by the American Psychological Association or one of its allied publishers.

an effect on recognition accuracy. Results are presented in Table 2.

correct recognitions as a function of the visuospatial context in As expected, the auditory-verbal hallucination score was associ-
which the pictures were presented (correct recognitions of pictures ated with impaired recognition of the color pictures. This inverse
presented in location, and correct recognitions of pictures pre- association was significant for immediate recognition and was
sented in association). only observed at a trend level of significance for delayed
A break of a few minutes followed the recognition of the recognition. The visual hallucination score was marginally sig-
pictures from the first set. Then the second set of pictures was nificantly associated with improved immediate recognition of
used. The subjects were informed that they were going to be the color pictures. No association with olfactory/tactile hallu-
administered the visual memory task a second time, with different cinations emerged.
pictures. The procedure was similar to that for the first set, except
that no delay intervened between the presentation of the 16 target
pictures and the recognition phase. Again, the Pr index was Effects of Visuospatial Encoding Context
computed for each type of picture (Pr-b/w immediate recognition, To investigate the effect of encoding complexity on these
and Pr-color immediate recognition), as were the corresponding Br associations, we then studied the immediate recognition of
indices; the number of correctly recognized pictures in each visu- pictures according to their visuospatial encoding context con-
ospatial context of presentation (location and association) was dition. Regression analyses were conducted on the number of
tallied. recognized b/w and color pictures presented in association with
an image, and the number of recognized b/w and color pictures
presented alone at different locations. The Br index from im-
Results mediate recognition was entered among the predictors to con-
The numbers of correctly recognized target pictures in schizo- trol for the propensity to make false recognitions of nonpre-
phrenia patients and healthy participants as a function of the type sented pictures. The olfactory/tactile hallucination score was
of picture (b/w or color) and visuospatial context encoding condi- removed because it was found to be unrelated to the Pr indices.
tion (association or location) in immediate and delayed recognition Results are presented in Table 3. Auditory-verbal hallucinations
were significantly associated with poor recognition of the color
are reported in Table 1.
pictures presented in association with another visual stimulus,
but not with poor recognition of the color pictures presented at
different locations. Visual hallucinations, in contrast, were pos-
Table 1 itively associated with recognition of the color pictures pre-
Number of Correctly Recognized Target Pictures (Max ⫽ 8) as sented at different locations.
a Function of the Type of Picture (B/W or Color), and as a
Function of the Visuospatial Context Encoding Condition
(“Association” or “Location”) in Immediate and Delayed
Mediating Effect of Working-Memory Span
Recognition in 50 Schizophrenia Patients and 45 Healthy Correlational analyses indicated that the auditory-verbal hal-
Control Participants: Ms and SDs) lucination score was inversely associated with the working-
memory span (r ⫽ ⫺.40, p ⬍ .005), but the visual hallucination
Type of Type of picture and its Schizophrenia Healthy score was unrelated to it (r ⫽ ⫺.09, ns). We tested the poten-
recognition context patients controls
tially mediating effect of working-memory span on the ob-
Immediate B/W pictures 4.9 (2.0) 6.5 (1.2) served association between auditory-verbal hallucinations and
recognition Color pictures 5.0 (1.9) 6.6 (1.5) impaired recognition of the color pictures. The regression anal-
Pictures in “association” 4.6 (2.0) 6.4 (1.6)
Pictures in “location” 5.3 (1.9) 6.7 (1.3) yses on the number of recognized color pictures in each visu-
Delayed B/W pictures 5.1 (1.7) 5.7 (1.7) ospatial context condition were computed again, this time add-
recognition Color pictures 5.1 (1.9) 5.7 (1.5) ing the working-memory span to the predictors. Results are
Pictures in “association” 4.6 (1.7) 5.3 (1.8) presented in Table 4. The inverse association between auditory-
Pictures in “location” 5.6 (1.6) 6.1 (1.7)
verbal hallucinations and recognition of the color pictures pre-
 HALLUCINATIONS AND RECOGNITION OF COLOR PICTURES 5

Table 2
Regression Analyses in the 50 Schizophrenia Patients

Recognition Auditory-verbal Visual Olfactory/tactile

parameter hallucinations hallucinations hallucinations Sex R2 F test p value

Pr-b/w
immediate ⫺.17 .09 ⫺.03 .34ⴱ .13 1.69 ns
Pr-color
immediate ⫺.40ⴱⴱ .30$ ⫺.15 .40ⴱⴱⴱ .30 4.89 .002
Pr-b/w
ⴱⴱⴱ
delayed .13 ⫺.21 ⫺.15 .42 .20 2.81 .04
Pr-color
delayed ⫺.27& ⫺.06 .02 .31ⴱ .17 2.37 .07
Note. Associations of three types of hallucinations with picture recognition of b/w and color pictures in
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

immediate and delayed recognition conditions (␤ coefficient).

$
p ⫽ .052. & p ⬍ .10. ⴱ p ⬍ .05. ⴱⴱ p ⬍ .01. ⴱⴱⴱ p ⬍ .005.
This document is copyrighted by the American Psychological Association or one of its allied publishers.

sented in association disappeared. The positive association be-
tween visual hallucinations and recognition of the color pictures
presented in location was unaltered.
Positive Effect of Visual Hallucinations
To further investigate the finding that visual hallucinations were
associated with enhanced recognition of the color pictures pre-
sented at different locations, we compared the 45 healthy control
participants with the 17 patients presenting visual hallucinations
(score ⬎ 1) and with the 26 patients without visual hallucinations
(score ⫽ 0). The seven patients scoring 1 on the visual hallucina-
tion item were excluded from these analyses. Analyses of variance
were conducted on the number of recognized pictures in the
location context condition of immediate recognition, with group
(patients– healthy controls) as a between-subjects factor, and type
of picture (b/w pictures– color pictures) as a within-subjects factor.
Br indices, education level, and verbal IQ were controlled.
When the patients without visual hallucinations were compared
to the healthy participants, the effect of group was significant, F(1,
65) ⫽ 9.36, p ⬍ .005, without any interaction with type of picture
(F ⬍ 1). This indicates that these patients were equally impaired in
the recognition of b/w and color pictures. In contrast, when the
patients with visual hallucinations were compared to the healthy
participants, the effect of group was significant, F(1, 56) ⫽ 4.92,
p ⬍ .05, with a significant interaction with type of picture, F(1,
56) ⫽ 6.65, p ⬍ .015. Follow-up univariate tests revealed that the
patients with visual hallucinations were highly significantly im-
paired in the recognition of the b/w pictures (estimated marginal
means: 2.48 vs. 3.46, F(1, 56) ⫽ 14.4, p ⬍ .0001), but they were
equivalent to the healthy participants in the recognition of the color
pictures (estimated marginal means: 3.32 vs. 3.30, F near 0).
Discussion
Studies concerned with the cognitive underpinnings of halluci-
nations in patients with schizophrenia have uncovered various
correlates of auditory-verbal hallucinations, mostly related to
source memory and inhibition processes (Badcock & Hugdahl,
2012; de Leede-Smith & Barkus, 2013; Waters, Allen, et al.,
2012). Our previous work unexpectedly revealed that auditory
hallucinations were associated with impairment in the recognition
of color pictures, whereas they were not significantly related to the
recognition of the b/w pictures (Brébion, David, Ohlsen, et al.,
2007). In the current study we attempted to determine, through
manipulation of the encoding conditions, whether this impairment
was due to the chromatic properties themselves of the color pic-
tures, or rather to the fact that the encoding of color pictures
requires more cognitive effort than b/w pictures.
Results showed that the association between auditory-verbal
hallucinations and poor recognition of the color pictures was again
observed, and that it was significant only for immediate recogni-
tion. Because the recognition format eliminates the retrieval re-
quirements of memory processes, and because a recognition test
immediately following the encoding of the information eliminates
the maintenance requirements, the observed association suggests
that the effect of auditory-verbal hallucinations pertains to picture
encoding processes, as expected. Separate analyses of each type of
visuospatial context indicate that the association between auditory-
verbal hallucinations and impaired recognition of the color pic-

Table 3
Regression Analyses in the 50 Schizophrenia Patients

Number and type of recognized pictures in Auditory-verbal Visual

immediate recognition hallucinations hallucinations Sex Br index R2 F test p value
ⴱⴱⴱⴱ
B/W pictures “association” ⫺.12 .09 .17 .55 .29 4.48 .004
Color pictures “association” ⫺.31ⴱ .04 .37ⴱⴱ .47ⴱⴱⴱ .33 5.58 .001
B/W pictures “location” ⫺.11 .06 .33ⴱ .57ⴱⴱⴱⴱ .32 5.22 .002
Color pictures “location” ⫺.19 .38ⴱⴱ .15 .39ⴱⴱ .28 4.40 .004
Note. Associations of auditory-verbal and visual hallucinations with the number of recognized black-and-white and color pictures in the immediate-
recognition condition, according to the visuospatial encoding context condition: “association” or “location” (␤ coefficient).
ⴱ
p ⬍ .025. ⴱⴱ p ⬍ .01. ⴱⴱⴱ p ⬍ .001. ⴱⴱⴱⴱ p ⬍ .0001.
 6 BRÉBION ET AL.
Table 4
Regression Analyses in the 50 Schizophrenia Patients.
Number of recognized pictures Auditory-verbal Visual
(immediate recognition) hallucinations hallucinations
Color pictures “association” ⫺.09 .01
Color pictures “location” ⫺.02 .36ⴱⴱ
Note. Associations of auditory-verbal and visual hallucinations with the number of recognized color pictures (immediate recognition) in “association” and
“location” visuospatial encoding context conditions, after adding working memory span to the predictors (␤ coefficient).
ⴱ
p ⬍ .05. ⴱⴱ p ⬍ .01. ⴱⴱⴱ p ⬍ .005. ⴱⴱⴱⴱ p ⬍ .0001.
tures only emerged when those color pictures were aggregated with
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
another visual stimulus at the presentation phase, a condition which
This document is copyrighted by the American Psychological Association or one of its allied publishers.
required more effortful encoding than when the pictures were
presented alone. Moreover, auditory-verbal hallucinations were
significantly associated with decreased working-memory span.
This latter observation corroborates Gisselgård et al. (2014), who
also obtained a significant correlation between auditory-verbal
hallucination scores and letter–number spans in patients with first-
episode psychosis. In our data, the association between auditory-
verbal hallucinations and poor recognition of the associated color
pictures appears to have been entirely mediated by working-
memory impairment, because it no longer existed when working-
memory span was controlled. Thus, the pattern of findings sug-
gests that it was not the color, per se, that impeded picture
encoding in patients with auditory hallucinations, but rather the
cognitive effort required to encode the stimuli that included the
richest and most complex visual information (color attributes
combined with visual association). This association with impaired
encoding of the color pictures is specific to auditory-verbal hallu-
cinations, because no inverse association emerged with either
visual or olfactory/tactile hallucinations. Dealing with auditory
hallucinations might draw from the limited pool of cognitive
resources available in working memory, thereby impeding the
processing of the upcoming information that exceeds residual
system capacity. In the same vein, Hugdahl et al. (2013) recently
demonstrated that auditory-verbal hallucinations, by drawing at-
tention inward, interfere with the ability to attend to external
stimuli. Alternatively, working-memory dysfunction might be one
factor involved in the genesis of auditory-verbal hallucinations. In
any case, decreased working-memory span seems to be a stable
trait of patients suffering from auditory-verbal hallucinations, be-
cause these patients were not necessarily hallucinating at the time
of the testing in our study or in those mentioned above.
Although cognitive performance has generally been found to be
unrelated to hallucinations in schizophrenia patients, specific as-
sociations with auditory-verbal hallucinations might have been
masked by the use of a global hallucination score. Working-
memory span might mediate associations between auditory-verbal
hallucinations and other types of cognitive impairment. Indeed,
performance in a variety of neuropsychological domains seems to
be constrained by working-memory-span decrement in this popu-
lation (Silver, Feldman, Bilker, & Gur, 2003), and this seems to
apply mostly to effortful processes (Bagner, Melinder, & Barch,
2003; Brébion et al., 2011; Stone, Gabrieli, Stebbins, & Sullivan,
1998). Alleviating verbal hallucinations might indirectly improve
certain cognitive functions by reducing the burden on working
memory.
Working
memory span Sex Br index R2 F test p value
ⴱⴱⴱⴱ ⴱ ⴱⴱⴱ
.50 .26 .34 .52 9.49 .0001
.38ⴱⴱ .07 .28ⴱ .39 5.55 .0001
Very few cognitive correlates of visual hallucinations have been
established so far in patients with schizophrenia. In our data, in
contrast to auditory-verbal hallucinations, visual hallucinations
were associated with enhanced recognition of the color pictures.
This dissociation between the effects of auditory-verbal and visual
hallucinations is striking because scores in these two types of
hallucinations were positively intercorrelated. A specific analysis
of the visuospatial encoding conditions indicated that visual hal-
lucinations were selectively associated with enhanced recognition
of the color pictures presented alone at different locations. In
addition, the patients who suffered visual hallucinations were
equivalent to the healthy participants in the recognition of these
color pictures, whereas they were highly significantly impaired in
the recognition of the b/w pictures presented in the same location
condition. In contrast, the patients without visual hallucinations
were equally impaired relative to the healthy participants in the
recognition of both types of pictures. We found it interesting that
Barnes and Boubert (2011) reported that Parkinson’s disease pa-
tients with visual hallucinations were poorer than their nonhallu-
cinating counterparts in the recognition of b/w pictures, but they
were equivalent to them in the recognition of color pictures. Visual
hallucinations might possibly facilitate the encoding of visual
stimuli displayed in natural colors. This hypothesis could be tested
by means of pictures presented in natural versus unnatural colors
(e.g., yellow sea and blue sun), or pictures of abstract versus
figurative color stimuli. Our procedure did not enable us to deter-
mine whether the fact that the pictures were displayed at different
locations provided a cue to the visually hallucinating patients that
helped visual encoding, or whether these patients merely had an
advantage in processing color pictures as long as the encoding
conditions were not exceedingly taxing. Patients with visual hal-
lucinations might present enhanced activation of brain areas that
enable visual perception. Indeed, brain studies have shown that
visual hallucinations are associated with activation of visual areas
(Ffytche et al., 1998; Oertel et al., 2007). Further, similar brain
areas seem to be activated during visual perception and visual
imagery (Ganis, Thompson, & Kosslyn, 2004). The alleged
excessive visual imagery in visually hallucinating patients
might lead them to improved perception, and thereby deeper
encoding, of external pictures. Visual hallucinations might al-
ternatively be associated with specific abilities in the perception
of colors. It has been suggested that enhanced color-perception
abilities in nonpsychiatric populations are associated with en-
hanced visual memory for color stimuli (Pritchard, Rothen,
Coolbear, & Ward, 2013). Conversely, patients with strong
color-perception abilities might be more likely to suffer hallu-
cinations in the visual modality.
 HALLUCINATIONS AND RECOGNITION OF COLOR PICTURES
The main limitation of our results resides in the very novelty of
this line of research and the lack of previous data that might have
enabled us to build compelling expectations. The association be-
tween auditory-verbal hallucinations and impaired encoding of
color pictures was investigated in an attempt to explain a previous
unexpected finding, and therefore the hypotheses that drove the
study were more tentative than based on a solid theoretical back-
ground. More work is warranted to corroborate the involvement of
working memory in auditory-verbal hallucinations. With respect to
visual hallucinations, they have been the object of little cognitive
research and the dearth of data relative to this issue did not enable
us to make any specific hypothesis regarding an association with
picture recognition. The association we observed rather emerged
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
from exploratory analyses and we can only speculate on its inter-
This document is copyrighted by the American Psychological Association or one of its allied publishers.
pretation. The very paucity of data available so far, however,
makes any additional information relative to visual hallucinations
valuable. Another limitation is that working memory was assessed
only in the verbal modality. We cannot rule out the possibility that
the pattern of associations with hallucinations would have been
different if a visual working-memory test had been used. Last,
antipsychotic medication might have influenced the results. Thus,
the findings do not enable us to draw definite conclusions, but they
suggest new avenues for the investigation of auditory and visual
hallucinations.
References
Allen, P., Aleman, A., & McGuire, P. K. (2007). Inner speech models of
auditory verbal hallucinations: Evidence from behavioural and neuro-
imaging studies. International Review of Psychiatry, 19, 407– 415.
http://dx.doi.org/10.1080/09540260701486498
American Psychiatric Association. (1994). Diagnostic and statistical man-
ual of mental disorders (4th ed.). Washington, DC.
Baddeley, A. (2012). Working memory: Theories, models, and controver-
sies. Annual Review of Psychology, 63, 1–29. http://dx.doi.org/10.1146/
annurev-psych-120710-100422
Badcock, J. C., & Hugdahl, K. (2012). Cognitive mechanisms of auditory
verbal hallucinations in psychotic and non-psychotic groups. Neurosci-
ence and Biobehavioral Reviews, 36, 431– 438. http://dx.doi.org/
10.1016/j.neubiorev.2011.07.010
Badcock, J. C., Waters, F. A. V., Maybery, M. T., & Michie, P. T. (2005).
Auditory hallucinations: Failure to inhibit irrelevant memories. Cogni-
tive Neuropsychiatry, 10, 125–136. http://dx.doi.org/10.1080/
13546800344000363
Bagner, D. M., Melinder, M. R. D., & Barch, D. M. (2003). Language
comprehension and working memory deficits in patients with schizo-
phrenia. Schizophrenia Research, 60, 299 –309. http://dx.doi.org/
10.1016/S0920-9964(02)00280-3
Barnes, J., & Boubert, L. (2011). Visual memory errors in Parkinson’s
disease patient with visual hallucinations. The International Journal of
Neuroscience, 121, 159 –164. http://dx.doi.org/10.3109/00207454.2010
.539308
Bentall, R. P. (1990). The illusion of reality: A review and integration of
psychological research on hallucinations. Psychological Bulletin, 107,
82–95. http://dx.doi.org/10.1037/0033-2909.107.1.82
Brébion, G., Bressan, R. A., Pilowsky, L. S., & David, A. S. (2011).
Processing speed and working-memory span: Their differential role in
superficial and deep memory processes in schizophrenia. Journal of the
International Neuropsychological Society, 17, 485– 493. http://dx.doi
.org/10.1017/S1355617711000208
Brébion, G., David, A. S., Bressan, R. A., Ohlsen, R. I., & Pilowsky, L. S.
(2009). Hallucinations and two types of free-recall intrusion in schizo-
7
phrenia. Psychological Medicine, 39, 917–926. http://dx.doi.org/
10.1017/S0033291708004819
Brébion, G., David, A. S., Jones, H. M., Ohlsen, R., & Pilowsky, L. S.
(2007). Temporal context discrimination in patients with schizophrenia:
Associations with auditory hallucinations and negative symptoms. Neuro-
psychologia, 45, 817– 823. http://dx.doi.org/10.1016/j.neuropsychologia
.2006.08.009
Brébion, G., David, A. S., Ohlsen, R., Jones, H. M., & Pilowsky, L. S.
(2007). Visual memory errors in schizophrenic patients with auditory
and visual hallucinations. Journal of the International Neuropsycho-
logical Society, 13, 832– 838. http://dx.doi.org/10.1017/S1355617
70707107X
Brébion, G., Ohlsen, R. I., Pilowsky, L. S., & David, A. S. (2008). Visual
hallucinations in schizophrenia: Confusion between imagination and
perception. Neuropsychology, 22, 383–389. http://dx.doi.org/10.1037/
0894-4105.22.3.383
Brébion, G., Ohlsen, R. I., Pilowsky, L. S., & David, A. S. (2011). Serial
and semantic encoding of lists of words in schizophrenia patients with
visual hallucinations. Psychiatry Research, 186, 5–10. http://dx.doi.org/
10.1016/j.psychres.2010.07.053
Brébion, G., Stephan-Otto, C., Huerta-Ramos, E., Ochoa, S., Usall, J.,
Abellán-Vega, H., . . . Haro, J. M. (2014). Visual Encoding Impairment
in Patients With Schizophrenia: Contribution of Reduced Working-
memory span, Decreased Processing Speed, and Affective Symptoms.
Neuropsychology. Advance online publication.
Brookwell, M. L., Bentall, R. P., & Varese, F. (2013). Externalizing biases
and hallucinations in source-monitoring, self-monitoring and signal de-
tection studies: A meta-analytic review. Psychological Medicine, 43,
2465–2475. http://dx.doi.org/10.1017/S0033291712002760
Bruder, G. E., Alschuler, D. M., Kroppmann, C. J., Fekri, S., Gil, R. B.,
Jarskog, L. F., . . . Wexler, B. E. (2011). Heterogeneity of auditory
verbal working memory in schizophrenia. Journal of Abnormal Psychol-
ogy, 120, 88 –97. http://dx.doi.org/10.1037/a0021661
Collerton, D., Perry, E., & McKeith, I. (2005). Why people see things that
are not there: A novel Perception and Attention Deficit model for
recurrent complex visual hallucinations. Behavioral and Brain Sciences,
28, 737–757. http://dx.doi.org/10.1017/S0140525X05000130
Corwin, J. (1994). On measuring discrimination and response bias: Un-
equal numbers of targets and distractors and two classes of distractors.
Neuropsychology, 8, 110 –117. http://dx.doi.org/10.1037/0894-4105.8.1
.110
de Leede-Smith, S., & Barkus, E. (2013). A comprehensive review of
auditory verbal hallucinations: Lifetime prevalence, correlates and
mechanisms in healthy and clinical individuals. Frontiers in Human
Neuroscience, 7, 367. http://dx.doi.org/10.3389/fnhum.2013.00367
Dibben, C. R. M., Rice, C., Laws, K., & McKenna, P. J. (2009). Is
executive impairment associated with schizophrenic syndromes? A
meta-analysis. Psychological Medicine, 39, 381–392. http://dx.doi.org/
10.1017/S0033291708003887
Ditman, T., & Kuperberg, G. R. (2005). A source-monitoring account of
auditory verbal hallucinations in patients with schizophrenia. Harvard
Review of Psychiatry, 13, 280 –299. http://dx.doi.org/10.1080/
10673220500326391
Ellis, N. R. (1990). Is memory for spatial location automatically encoded?
Memory & Cognition, 18, 584 –592. http://dx.doi.org/10.3758/
BF03197101
Ffytche, D. H., Howard, R. J., Brammer, M. J., David, A., Woodruff, P., &
Williams, S. (1998). The anatomy of conscious vision: An fMRI study
of visual hallucinations. Nature Neuroscience, 1, 738 –742. http://dx.doi
.org/10.1038/3738
Frith, C. D. (1992). The cognitive neuropsychology of schizophrenia.
Hove, UK: Erlbaum.
Ganis, G., Thompson, W. L., & Kosslyn, S. M. (2004). Brain areas
underlying visual mental imagery and visual perception: An fMRI study.
 8 BRÉBION ET AL.
Cognitive Brain Research, 20, 226 –241. http://dx.doi.org/10.1016/j
.cogbrainres.2004.02.012
Gaweda, L., Woodward, T. S., Moritz, S., & Kokoszka, A. (2013). Im-
paired action self-monitoring in schizophrenia patients with auditory
hallucinations. Schizophrenia Research, 144, 72–79. http://dx.doi.org/
10.1016/j.schres.2012.12.003
Gisselgård, J., Anda, L. G., Brønnick, K., Langeveld, J., Ten Velden
Hegelstad, W., Joa, I., . . . Larsen, T. K. (2014). Verbal working memory
deficits predict levels of auditory hallucination in first-episode psycho-
sis. Schizophrenia Research, 153(1–3), 38 – 41. http://dx.doi.org/
10.1016/j.schres.2013.12.018
Gomar, J. J., Ortiz-Gil, J., McKenna, P. J., Salvador, R., Sans-Sansa, B.,
Sarró, S., . . . Pomarol-Clotet, E. (2011). Validation of the Word
Accentuation Test (TAP) as a means of estimating premorbid IQ in
This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.
Spanish speakers. Schizophrenia Research, 128, 175–176. http://dx.doi
.org/10.1016/j.schres.2010.11.016
This document is copyrighted by the American Psychological Association or one of its allied publishers.
Hugdahl, K., Nygård, M., Falkenberg, L. E., Kompus, K., Westerhausen,
R., Kroken, R., . . . Løberg, E.-M. (2013). Failure of attention focus and
cognitive control in schizophrenia patients with auditory verbal halluci-
nations: Evidence from dichotic listening. Schizophrenia Research, 147,
301–309. http://dx.doi.org/10.1016/j.schres.2013.04.005
Johnson, M. K., Hashtroudi, S., & Lindsay, D. S. (1993). Source monitor-
ing. Psychological Bulletin, 114, 3–28. http://dx.doi.org/10.1037/0033-
2909.114.1.3
Jones, S. R. (2010). Do we need multiple models of auditory verbal
hallucinations? Examining the phenomenological fit of cognitive and
neurological models. Schizophrenia Bulletin, 36, 566 –575. http://dx.doi
.org/10.1093/schbul/sbn129
Larøi, F., & Woodward, T. S. (2007). Hallucinations from a cognitive
perspective. Harvard Review of Psychiatry, 15, 109 –117. http://dx.doi
.org/10.1080/10673220701401993
Moseley, P., Fernyhough, C., & Ellison, A. (2013). Auditory verbal hal-
lucinations as atypical inner speech monitoring, and the potential of
neurostimulation as a treatment option. Neuroscience and Biobehavioral
Reviews, 37, 2794 –2805. http://dx.doi.org/10.1016/j.neubiorev.2013.10
.001
Nelson, H. E. (1982). The National Adult Reading Test (NART): Test
manual. NFER-Nelson, Windsor, UK.
Oertel, V., Rotarska-Jagiela, A., van de Ven, V. G., Haenschel, C., Maurer,
K., & Linden, D. E. J. (2007). Visual hallucinations in schizophrenia
investigated with functional magnetic resonance imaging. Psychiatry
Research: Neuroimaging, 156, 269 –273. http://dx.doi.org/10.1016/j
.pscychresns.2007.09.004
Peralta, V., & Cuesta, M. J. (1999). Dimensional structure of psychotic
symptoms: An item-level analysis of SAPS and SANS symptoms in
psychotic disorders. Schizophrenia Research, 38, 13–26. http://dx.doi
.org/10.1016/S0920-9964(99)00003-1
Pritchard, J., Rothen, N., Coolbear, D., & Ward, J. (2013). Enhanced
associative memory for colour (but not shape or location) in synaesthe-
sia. Cognition, 127, 230 –234. http://dx.doi.org/10.1016/j.cognition.2012
.12.012
Shergill, S. S., Bullmore, E., Simmons, A., Murray, R., & McGuire, P.
(2000). Functional anatomy of auditory verbal imagery in schizophrenic
patients with auditory hallucinations. The American Journal of Psychi-
atry, 157, 1691–1693. http://dx.doi.org/10.1176/appi.ajp.157.10.1691
Silver, H., Feldman, P., Bilker, W., & Gur, R. C. (2003). Working memory
deficit as a core neuropsychological dysfunction in schizophrenia. The
American Journal of Psychiatry, 160, 1809 –1816. http://dx.doi.org/
10.1176/appi.ajp.160.10.1809
Soriano, M. F., Jiménez, J. F., Román, P., & Bajo, M. T. (2009). Intentional
inhibition in memory and hallucinations: Directed forgetting and updat-
ing. Neuropsychology, 23, 61–70. http://dx.doi.org/10.1037/a0013739
Stone, M., Gabrieli, J. D., Stebbins, G. T., & Sullivan, E. V. (1998).
Working and strategic memory deficits in schizophrenia. Neuropsychol-
ogy, 12, 278 –288. http://dx.doi.org/10.1037/0894-4105.12.2.278
Ventura, J., Thames, A. D., Wood, R. C., Guzik, L. H., & Hellemann, G. S.
(2010). Disorganization and reality distortion in schizophrenia: A meta-
analysis of the relationship between positive symptoms and neurocog-
nitive deficits. Schizophrenia Research, 121, 1–14. http://dx.doi.org/
10.1016/j.schres.2010.05.033
Waters, F., Allen, P., Aleman, A., Fernyhough, C., Woodward, T. S.,
Badcock, J. C., . . . Larøi, F. (2012). Auditory hallucinations in schizo-
phrenia and nonschizophrenia populations: A review and integrated
model of cognitive mechanisms. Schizophrenia Bulletin, 38, 683– 693.
http://dx.doi.org/10.1093/schbul/sbs045
Waters, F. A. V., Badcock, J. C., Maybery, M. T., & Michie, P. T. (2003).
Inhibition in schizophrenia: Association with auditory hallucinations.
Schizophrenia Research, 62, 275–280. http://dx.doi.org/10.1016/S0920-
9964(02)00358-4
Waters, F. A. V., Badcock, J. C., Michie, P. T., & Maybery, M. T. (2006).
Auditory hallucinations in schizophrenia: Intrusive thoughts and forgot-
ten memories. Cognitive Neuropsychiatry, 11, 65– 83. http://dx.doi.org/
10.1080/13546800444000191
Waters, F., Woodward, T., Allen, P., Aleman, A., & Sommer, I. (2012).
Self-recognition deficits in schizophrenia patients with auditory hallu-
cinations: A meta-analysis of the literature. Schizophrenia Bulletin, 38,
741–750. http://dx.doi.org/10.1093/schbul/sbq144
Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). San
Antonio, TX: The Psychological Corporation.
Woodward, T. S., & Menon, M. (2011). Considerations for analysis of
source monitoring data when investigating hallucinations in schizophre-
nia research. European Archives of Psychiatry and Clinical Neurosci-
ence, 261, 157–164. http://dx.doi.org/10.1007/s00406-010-0151-9
Received June 11, 2014
Revision received October 6, 2014
Accepted October 30, 2014 䡲