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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
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.
Hallucinations are very common in patients with schizophrenia. verbal hallucinations have been associated with disturbance in self-
They have been linked to deficits in the cognitive processes enabling monitoring of language (Allen, Aleman, & McGuire, 2007;
reality discrimination, reality monitoring, self-monitoring, and source Brébion, David, Bressan, Ohlsen, & Pilowsky, 2009; Ditman &
monitoring (Bentall, 1990; Brookwell, Bentall, & Varese, 2013; Frith, Kuperberg, 2005; Jones, 2010; Moseley, Fernyhough, & Ellison,
1992; Johnson, Hashtroudi, & Lindsay, 1993; Larøi & Woodward, 2013; Shergill, Bullmore, Simmons, Murray, & McGuire, 2000),
2007; Woodward & Menon, 2011). More specifically, auditory- 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
Gildas Brébion, Unit of Research and Development, Parc Sanitari Sant Joan temporal (Brébion, David, Jones, Ohlsen, & Pilowsky, 2007; Wa-
de Déu and Centro de Investigación Biomédica en Red de Salud Mental, ters, Badcock, Michie, & Maybery, 2006) and spatial (Brébion,
Barcelona, Spain; Christian Stephan-Otto, Unit of Research and Development, David, Ohlsen, Jones, & Pilowsky, 2007) sources of events, and
Parc Sanitari Sant Joan de Déu and Centro de Investigación Biomédica en Red
with faulty mechanisms of intentional inhibition (Badcock, Wa-
de Salud Mental, Barcelona, Spain, and Fundació Sant Joan de Déu, Barce-
lona, Spain; Judith Usall, Elena Huerta-Ramos, Mireia Perez del Olmo, Jorge
ters, Maybery, & Michie, 2005; Soriano, Jiménez, Román, & Bajo,
Cuevas-Esteban, Josep Maria Haro, and Susana Ochoa, Unit of Research and 2009; Waters, Badcock, Maybery, & Michie, 2003).
Development, Parc Sanitari Sant Joan de Déu and Centro de Investigación Visual hallucinations, which are less prevalent in schizophrenia,
Biomédica en Red de Salud Mental, Barcelona, Spain. have been the object of much scantier investigation. Collerton et
We thank Dr Mercedes Roca and Ms Montserrat Contel for helping with al. (2005) emphasized the role of perceptual and attentional im-
the recruitment of patients. This study was funded by a Miguel Servet pairment in recurrent complex visual hallucinations occurring un-
contract at CIBERSAM and a grant from the Fondo de Investigación
der various conditions. We observed in a previous schizophrenia
Sanitaria, Spanish Ministry of Health (PI10/02479), to Gildas Brébion.
Correspondence concerning this article should be addressed to Gildas
sample that visual hallucinations were associated with confusion
Brébion, Unit of Research and Development, PSSJD, C/ Doctor Antoni between mental images and perception (Brébion, Ohlsen, Pi-
Pujadas 42, 08830 Sant Boi de Llobregat (Barcelona) Spain. E-mail: lowsky, & David, 2008), as well as with reduced use of verbal
gildas.brebion@pssjd.org strategies in the learning of lists of words (Brébion, Ohlsen,
1
2 BRÉBION ET AL.
Pilowsky, & David, 2011). This latter finding suggests increased automatic processes (Ellis, 1990). We contrasted immediate and
use of a visual imagery strategy in these patients. delayed recognition conditions to ascertain that the alleged effect
In previous research on visual memory in schizophrenia of auditory-verbal hallucinations occurred at the encoding stage—
(Brébion, David, Ohlsen, et al., 2007), we presented mixed black- reflected by immediate recognition performance— because both
and-white (b/w) and color pictures at different locations, with each hypotheses that we propose postulate impaired encoding of the
location indicated by a small image that constituted the visuospa- color pictures. A working-memory task was administered as well.
tial context. We unexpectedly observed that auditory hallucina- Following on from our previous finding, we hypothesized that
tions were associated with subsequent impairment in recognizing auditory-verbal hallucinations were associated with impaired rec-
the color pictures among similar distracters after a delay of a few ognition of color, but not b/w, pictures. The specific pattern of
minutes. This suggests that patients with auditory hallucinations associations with each visual encoding condition was expected to
had not properly encoded these color pictures during the presen- illuminate the mechanism involved. If the association between
tation phase, or were impaired in maintaining them in memory auditory hallucinations and impaired recognition of color pictures
over the delay. No association with the recognition of the b/w stemmed from difficulty in conducting effortful processing as a
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pictures emerged. Although the use of visual material might have consequence of decreased working-memory capacity, we should
This document is copyrighted by the American Psychological Association or one of its allied publishers.
facilitated the emergence of potential associations with visual expect the following pattern: (a) auditory-verbal hallucinations
hallucinations, no such association was uncovered. would be inversely associated with working-memory span, (b) the
The inverse association between auditory hallucinations and association between picture recognition and auditory-verbal hallu-
recognition of the color pictures was challenging. Indeed, positive cinations would pertain to the color pictures presented under the
symptoms of schizophrenia have generally been found to be fairly “association” condition rather than those presented under the “lo-
independent of cognitive efficiency (Dibben, Rice, Laws, & Mc- cation” condition, and (c) controlling for the working-memory
Kenna, 2009; Ventura, Thames, Wood, Guzik, & Hellemann, span would abolish this association. Alternatively, if patients with
2010). Patients with auditory hallucinations might be abnormally auditory-verbal hallucinations are cognitively hampered by the
distracted by chromatic information, and hence disregard the other very chromatic properties of the color pictures regardless of task
characteristics of the stimuli. This would lead to incomplete en- difficulty, the association between auditory-verbal hallucinations
coding of the color pictures. Alternatively, the crux might be that and color picture recognition should be equally observed for both
the color pictures contain richer and more complex information conditions of visual encoding, and it should be unaffected by
than do the b/w pictures, and therefore they require deeper pro- statistical control of working-memory span.
cessing. Patients with auditory hallucinations might be generally A second objective of our study was to investigate the associ-
impaired in conducting deep/effortful processing. Indeed, ations of picture recognition with visual hallucinations. Our sam-
auditory-verbal hallucinations have been associated with impair- ple presented a greater prevalence of hallucinations than in our
ment in working memory (Bruder et al., 2011; Gisselgård et al., previous study, especially with respect to visual hallucinations,
2014), a cognitive system allegedly involved in complex cognitive and therefore associations with this clinical symptom were more
operations (Baddeley, 2012). We previously reported that the likely to be disclosed. However, given the lack of previous data
encoding of color pictures was constrained by working-memory concerning any relationship between visual memory and visual
capacity, whereas the encoding of b/w pictures was not (Brébion, hallucinations, potential associations were studied in an explor-
Bressan, Pilowsky, & David, 2011), and that this association with ative way.
working memory was significant only when the encoding of the
color pictures was effortful (Brébion et al., 2014). A reduced Method
working-memory span in patients with auditory hallucinations
might lead them to ineffective encoding of the pictures that require
the most effortful processing. Subjects
The first objective of the current study was to replicate and Fifty in-patients with schizophrenia (per DSM–IV criteria; APA,
attempt to clarify our previous unexpected finding of an inverse 1994) were recruited from various units for chronic and acute
association between auditory hallucinations and recognition of pathology within the Parc Sanitari Sant Joan de Déu network of
color pictures, because an understanding of this association might mental health services in Barcelona, Spain: 34 men, 16 women;
shed new light on the nature of auditory hallucinations. We mod- aged M ⫽ 47.3, SD ⫽ 10.2; education level1: M ⫽ 3.2, SD ⫽ 1.4;
ified our visual memory task so that the procedure would presum- verbal IQ (Test de Acentuación de Palabras; TAP; Gomar et al.,
ably enable us to determine whether it was the color itself that 2011)2: M ⫽ 16.2, SD ⫽ 5.6; illness duration: M ⫽ 19.9 years,
impeded efficient picture encoding in patients with auditory hal- SD ⫽ 12.2. The exclusion criteria were alcohol or drug abuse (per
lucinations, or if the impairment resulted from the greater com- DSM–IV criteria) within the previous 6 months, organic mental
plexity of the stimuli to be processed. B/w and color pictures were disorders, intellectual disability (IQ ⬍ 70), history of brain injury,
presented separately so as to isolate the effect of color. The visual dementia, and current severe physical disease. All patients were
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 1
The scale used was: 1 ⫽ no studies; 2 ⫽ uncompleted primary studies;
association with a small image. These two encoding conditions 3 ⫽ completed primary studies; 4 ⫽ high school uncompleted; 5 ⫽ high
school completed; 6 ⫽ undergraduate studies; 7 ⫽ bachelor’s or master’s
corresponded to two levels of complexity. It was assumed that degree; 8 ⫽ doctorate.
encoding two associated visual stimuli was especially demanding, 2
The equivalent estimated verbal IQs are 16.2 ⫽ 89 and 20.4 ⫽ 97
whereas encoding the spatial location of stimuli relied on more (Gomar et al., 2011).
HALLUCINATIONS AND RECOGNITION OF COLOR PICTURES 3
receiving antipsychotic medication and were clinically stable— Procedure. The 16 target pictures from the first set were
that is, were at a stabilized dose of medication—at the time of displayed on the table in trials of four b/w or four color pictures.
testing. In the “location” context condition they were placed at one of four
Forty-five healthy control participants were recruited from the different locations (top left, top right, bottom left, bottom right). In
community: 27 men, 18 women aged M ⫽ 45.1, SD ⫽ 9.1; the “association” context condition they were displayed in the
education level1: M ⫽ 4.8, SD ⫽ 1.2; verbal IQ (TAP)2: M ⫽ 20.4, center, each beneath one of four small schematic color images that
SD ⫽ 4.7. They were screened by telephone interview to rule out constituted the visual context. The subjects were presented with
current or recent alcohol abuse, drug abuse, and psychiatric dis- four b/w location pictures, four color location pictures, four b/w
ease, as well as severe current nonpsychiatric disease. The two association pictures, and four color association pictures, in a coun-
groups were not significantly different in age or sex distribution. terbalanced order (see Figure 1 for an example). They were in-
However, the level of education was significantly higher in the structed to commit to memory not only the pictures themselves,
control group, as was the score on the vocabulary test (TAP), a but also where these pictures were located or with which image
Spanish equivalent of the National Adult Reading Test (NART; each was associated. The exposure duration was 20 s for each trial
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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.
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-
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Table 2
Regression Analyses in the 50 Schizophrenia Patients
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
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sented in association disappeared. The positive association be- equivalent to the healthy participants in the recognition of the color
tween visual hallucinations and recognition of the color pictures pictures (estimated marginal means: 3.32 vs. 3.30, F near 0).
presented in location was unaltered.
Discussion
Positive Effect of Visual Hallucinations
Studies concerned with the cognitive underpinnings of halluci-
To further investigate the finding that visual hallucinations were nations in patients with schizophrenia have uncovered various
associated with enhanced recognition of the color pictures pre- correlates of auditory-verbal hallucinations, mostly related to
sented at different locations, we compared the 45 healthy control source memory and inhibition processes (Badcock & Hugdahl,
participants with the 17 patients presenting visual hallucinations 2012; de Leede-Smith & Barkus, 2013; Waters, Allen, et al.,
(score ⬎ 1) and with the 26 patients without visual hallucinations 2012). Our previous work unexpectedly revealed that auditory
(score ⫽ 0). The seven patients scoring 1 on the visual hallucina- hallucinations were associated with impairment in the recognition
tion item were excluded from these analyses. Analyses of variance of color pictures, whereas they were not significantly related to the
were conducted on the number of recognized pictures in the recognition of the b/w pictures (Brébion, David, Ohlsen, et al.,
location context condition of immediate recognition, with group 2007). In the current study we attempted to determine, through
(patients– healthy controls) as a between-subjects factor, and type manipulation of the encoding conditions, whether this impairment
of picture (b/w pictures– color pictures) as a within-subjects factor. was due to the chromatic properties themselves of the color pic-
Br indices, education level, and verbal IQ were controlled. tures, or rather to the fact that the encoding of color pictures
When the patients without visual hallucinations were compared requires more cognitive effort than b/w pictures.
to the healthy participants, the effect of group was significant, F(1, Results showed that the association between auditory-verbal
65) ⫽ 9.36, p ⬍ .005, without any interaction with type of picture hallucinations and poor recognition of the color pictures was again
(F ⬍ 1). This indicates that these patients were equally impaired in observed, and that it was significant only for immediate recogni-
the recognition of b/w and color pictures. In contrast, when the tion. Because the recognition format eliminates the retrieval re-
patients with visual hallucinations were compared to the healthy quirements of memory processes, and because a recognition test
participants, the effect of group was significant, F(1, 56) ⫽ 4.92, immediately following the encoding of the information eliminates
p ⬍ .05, with a significant interaction with type of picture, F(1, the maintenance requirements, the observed association suggests
56) ⫽ 6.65, p ⬍ .015. Follow-up univariate tests revealed that the that the effect of auditory-verbal hallucinations pertains to picture
patients with visual hallucinations were highly significantly im- encoding processes, as expected. Separate analyses of each type of
paired in the recognition of the b/w pictures (estimated marginal visuospatial context indicate that the association between auditory-
means: 2.48 vs. 3.46, F(1, 56) ⫽ 14.4, p ⬍ .0001), but they were verbal hallucinations and impaired recognition of the color pic-
Table 3
Regression Analyses in the 50 Schizophrenia Patients
Table 4
Regression Analyses in the 50 Schizophrenia Patients.
tures only emerged when those color pictures were aggregated with Very few cognitive correlates of visual hallucinations have been
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another visual stimulus at the presentation phase, a condition which established so far in patients with schizophrenia. In our data, in
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required more effortful encoding than when the pictures were contrast to auditory-verbal hallucinations, visual hallucinations
presented alone. Moreover, auditory-verbal hallucinations were were associated with enhanced recognition of the color pictures.
significantly associated with decreased working-memory span. This dissociation between the effects of auditory-verbal and visual
This latter observation corroborates Gisselgård et al. (2014), who hallucinations is striking because scores in these two types of
also obtained a significant correlation between auditory-verbal hallucinations were positively intercorrelated. A specific analysis
hallucination scores and letter–number spans in patients with first- of the visuospatial encoding conditions indicated that visual hal-
episode psychosis. In our data, the association between auditory- lucinations were selectively associated with enhanced recognition
verbal hallucinations and poor recognition of the associated color of the color pictures presented alone at different locations. In
pictures appears to have been entirely mediated by working- addition, the patients who suffered visual hallucinations were
memory impairment, because it no longer existed when working- equivalent to the healthy participants in the recognition of these
memory span was controlled. Thus, the pattern of findings sug- color pictures, whereas they were highly significantly impaired in
gests that it was not the color, per se, that impeded picture the recognition of the b/w pictures presented in the same location
encoding in patients with auditory hallucinations, but rather the condition. In contrast, the patients without visual hallucinations
cognitive effort required to encode the stimuli that included the were equally impaired relative to the healthy participants in the
richest and most complex visual information (color attributes recognition of both types of pictures. We found it interesting that
combined with visual association). This association with impaired Barnes and Boubert (2011) reported that Parkinson’s disease pa-
encoding of the color pictures is specific to auditory-verbal hallu- tients with visual hallucinations were poorer than their nonhallu-
cinations, because no inverse association emerged with either cinating counterparts in the recognition of b/w pictures, but they
visual or olfactory/tactile hallucinations. Dealing with auditory were equivalent to them in the recognition of color pictures. Visual
hallucinations might draw from the limited pool of cognitive hallucinations might possibly facilitate the encoding of visual
resources available in working memory, thereby impeding the stimuli displayed in natural colors. This hypothesis could be tested
processing of the upcoming information that exceeds residual by means of pictures presented in natural versus unnatural colors
system capacity. In the same vein, Hugdahl et al. (2013) recently (e.g., yellow sea and blue sun), or pictures of abstract versus
demonstrated that auditory-verbal hallucinations, by drawing at- figurative color stimuli. Our procedure did not enable us to deter-
tention inward, interfere with the ability to attend to external mine whether the fact that the pictures were displayed at different
stimuli. Alternatively, working-memory dysfunction might be one locations provided a cue to the visually hallucinating patients that
factor involved in the genesis of auditory-verbal hallucinations. In helped visual encoding, or whether these patients merely had an
any case, decreased working-memory span seems to be a stable advantage in processing color pictures as long as the encoding
trait of patients suffering from auditory-verbal hallucinations, be- conditions were not exceedingly taxing. Patients with visual hal-
cause these patients were not necessarily hallucinating at the time lucinations might present enhanced activation of brain areas that
of the testing in our study or in those mentioned above. enable visual perception. Indeed, brain studies have shown that
Although cognitive performance has generally been found to be visual hallucinations are associated with activation of visual areas
unrelated to hallucinations in schizophrenia patients, specific as- (Ffytche et al., 1998; Oertel et al., 2007). Further, similar brain
sociations with auditory-verbal hallucinations might have been areas seem to be activated during visual perception and visual
masked by the use of a global hallucination score. Working- imagery (Ganis, Thompson, & Kosslyn, 2004). The alleged
memory span might mediate associations between auditory-verbal excessive visual imagery in visually hallucinating patients
hallucinations and other types of cognitive impairment. Indeed, might lead them to improved perception, and thereby deeper
performance in a variety of neuropsychological domains seems to encoding, of external pictures. Visual hallucinations might al-
be constrained by working-memory-span decrement in this popu- ternatively be associated with specific abilities in the perception
lation (Silver, Feldman, Bilker, & Gur, 2003), and this seems to of colors. It has been suggested that enhanced color-perception
apply mostly to effortful processes (Bagner, Melinder, & Barch, abilities in nonpsychiatric populations are associated with en-
2003; Brébion et al., 2011; Stone, Gabrieli, Stebbins, & Sullivan, hanced visual memory for color stimuli (Pritchard, Rothen,
1998). Alleviating verbal hallucinations might indirectly improve Coolbear, & Ward, 2013). Conversely, patients with strong
certain cognitive functions by reducing the burden on working color-perception abilities might be more likely to suffer hallu-
memory. cinations in the visual modality.
HALLUCINATIONS AND RECOGNITION OF COLOR PICTURES 7
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