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Comprehensive Psyc

Intellectual functioning and memory deficits in schizophrenia

Juan Carlos Ruiza,4, Marıa Jose Solerb, Inma Fuentesc, Pilar Tomasd

aDepartment of Methodology, Facultad de Psicologıa, University of Valencia, 46010 Valencia, SpainbDepartment of Basic Psychology, University of Valencia, 46010 Valencia, Spain

cDepartment of Personality, Evaluation, and Psychological Treatments, University of Valencia, 46010 Valencia, SpaindCenter for Rehabilitation and Social Integration, Department of Social Welfare of the Regional Government of Valencia, 46001 Valencia, Spain

Abstract

Background: There is converging evidence about the existence of different subgroups of patients with schizophrenia in

relation to intellectual ability (intelligence quotient [IQ]). Studying cognitive deficits in such patients in relation to IQ, and more

specifically to memory, could help determine the patterns of preserved and impaired functioning in cognitive abilities in association with

patterns of preserved and compromised intellect. This information could serve to delimit the possibilities of treatment and rehabilitation in

those patients.

Methods: A total of 44 patients with schizophrenia completed a cognitive battery that included executive functioning, attention,

speed of information processing, working memory, explicit memory, implicit memory, and everyday memory. Their IQ was also measured

to identify 2 subgroups with an IQ of 85 as the cutoff point. Then, differences between the groups in the neurocognitive measures

were studied.

Results: Performance in executive functioning, attention, working memory, and everyday memory, but not that in speed of infor-

mation processing, explicit memory, and implicit memory, was associated with intellectual functioning. Patients performed at the same level

in perceptual implicit memory but at a lower level in conceptual implicit memory as did healthy control subjects.

Discussion: Cognitive deficits in schizophrenia are associated with intellectual functioning. Implicit memory should not be considered as a

unique entity. It is suggested that conceptual implicit memory deficit may be a core feature of schizophrenia.

D 2007 Elsevier Inc. All rights reserved.

1. Introduction

Memory deficits have been considered as a specific

dysfunction in schizophrenia [1,2]. Most empirical evidence

on such deficits come from studies that compared the

performance of patients with schizophrenia with that of

healthy control subjects in explicit verbal and nonverbal

recall and recognition, working memory, and semantic

memory. Their neural mechanisms have also been estab-

lished [3]. More recently, a specific pattern of dissociations

in schizophrenic memory functioning has been found with

impairment in episodic long-term memory and working

memory coupled with preservation in areas such as short-

term memory, especially verbal short-term memory, and

procedural memory [2,4].

However, the literature has given less attention to the

study of everyday memory impairment and implicit memory

deficits in these patients.

0010-440X/$ – see front matter D 2007 Elsevier Inc. All rights reserved.

doi:10.1016/j.comppsych.2006.11.002

4 Corresponding author. Tel.: +34 963 864 414; fax: +34 963 864 697.

E-mail address: jcruiz@uv.es (J.C. Ruiz).

According to McKenna et al [4], poor performance in

some memory forms could reflect the schizophrenic

tendency to general intellectual impairment. In fact, memory

deficits in schizophrenia commonly occur within some

degree of general intellectual impairment when intelligence

is measured using traditional psychometric instruments (ie,

an intelligence quotient [IQ] test). Consequently, the scores

on all cognitive tests could be depressed to some extent and

the memory performance pattern could be obscured.

However, results about the magnitude of intellectual

deficit in patients with schizophrenia do not show a clear

pattern. Some studies have reported that patients with

schizophrenia have a lower IQ in comparison with healthy

control subjects, whereas other studies have shown that

intellectual decline after the onset of schizophrenia is not

general and that a relevant proportion of patients have a

normal IQ [5,6]. For example, in a cognitive evaluation of

221 patients with schizophrenia, Goldstein and Shemansky

[7] observed that 26% of the sample showed a normal IQ.

Similarly, Weickert et al [8] reported that, of 11 patients with

hiatry 48 (2007) 276–282

able 1

ociodemographic characteristics of all patients

IQ b85 (n = 23) IQ z85 (n = 21)

ex (male/female) 20:3 20:1

(mean F SD) 73.09 F 8.92 98.38 F 10.14

ge (y; mean F SD) 34.30 F 7.84 41.00 F 8.07

ducation (y; mean F SD) 6.57 F 4.91 9.95 F 4.72

uration of illness

(y; mean F SD)

15.39 F 8.71 19.33 F 8.38

J.C. Ruiz et al. / Comprehensive Psychiatry 48 (2007) 276–282 277

schizophrenia consecutively admitted to a mental health

center, 24.8% had an IQ within normal limits. More

recently, in a sample of 109 patients, Badcock et al [9]

found that 41% had preserved intellectual functioning.

Parallel literature had also shown that patients with a

normal IQ also have substantial cognitive deficits [10],

although results do not always coincide. For example,

Rund et al [11] found that a high intellectually functioning

group of patients with schizophrenia who have IQ scores

between 100 and 125 scored lower than did control

subjects in executive functioning, visual memory, and

verbal memory. However, Weickert et al [8] only observed

bmild impairment in executive function and, possibly,

attention and encoding.QThe heterogeneity of results observed in the general

intellectual functioning of patients has been afforded

through 2 strategies. The first strategy involves controlling

the influence of IQ on memory impairments using only

subjects with intact cognitive functions. Although this

strategy helps eliminate the effect of intellectual function-

ing on different cognitive functions, it does not indicate

how memory deficits are related to intellectual deficit in

schizophrenia [10,11]. The second strategy is establishing

different subgroups of subjects using IQ level as the

criterion. This procedure could help elaborate the role that

intellectual functioning plays in cognitive functioning and

particularly in memory impairments [11]. If memory

performance is related to IQ, then we can expect different

scores on memory tests from patients who have a low IQ

and from those with a normal IQ. Studying these differ-

ences could make determining which memory aspects are

jointly impaired and which are uniquely affected for each

IQ group possible.

To draw more firm conclusions regarding the magnitude

and specificity of memory dysfunction in schizophrenia, we

analyzed the role of IQ in these deficits, assessing a wide

range of memory areas and the cognitive domains of

executive functioning, attention, and speed of information

processing. We examined the profile of the performance of

patients with schizophrenia evaluating different forms of

explicit and implicit memory. A battery of memory tasks

was administered, including explicit tests on working

memory capacity, recall and recognition tasks, implicit

memory tests such as word-fragment completion and word

production from semantic categories, and a memory test to

detect and monitor everyday memory problems.

The general intellectual functioning of patients was also

measured using the Wechsler Adult Intelligence Scale

(WAIS-III). The IQ scores were used to classify subjects

in 2 groups: patients who were intellectually intact by

having IQ levels within 1 SD of the population mean

(IQ scores z85) and those who were intellectually impaired

by having IQ levels lower than 85. To determine the

possible influence of IQ on memory performance, we

compared the patterns of results of both patient groups on

the different cognitive and memory measures.

2. Subjects and methods

2.1. Participants

Forty-four outpatients from the Center for Rehabilitation

and Social Integration in Valencia, Spain, participated in the

study. They had a diagnosis of schizophrenia according to

Diagnostic and Statistical Manual of Mental Disorders,

Fourth Edition criteria. All the subjects provided written

informed consent before participating in the study. The

demographic and clinical characteristics of the patients are

shown in Table 1. All the patients were treated with typical

or atypical antipsychotic medication. A short form of the

Spanish version of the WAIS-III with documented psycho-

metric properties was administered to estimate their current

IQ level. This short form [12] includes the following

subtests of the full scale: information, block design,

arithmetic, and digit symbols. Two groups were formed

according to the participants’ IQ; an IQ of 85 was used as

the cutoff point. Twenty-three subjects scored lower than

this point (mean IQ = 73.09; SD = 8.92), and 21 scored

higher than it (mean IQ = 98.38; SD = 10.14).

2.2. Cognitive assessment

All the participants completed a battery of neuropsycho-

logic tests that had been selected to assess executive

functioning, attention capacity, speed of information pro-

cessing, working memory, explicit and implicit memory,

and everyday memory. All these tests were administered and

scored by trained psychologists.

The Wisconsin Card Sorting Test (WCST) [13] was

administered as a test of executive function. The variables

analyzed from this test were the number of categories

achieved, total trials to resolve the task, total errors, and

perseverative errors. Attention and speed of information

processing were assessed using the digit symbol substitution

and picture completion subtests of the WAIS-III. These

tasks require some level of attention, motor coordination,

and visual tracking.

The arithmetic calculation and digit span (forward and

backward) subtests of the WAIS-III were administered as

tests of working memory.

Explicit memory was measured with tests that assess

acquisition, storage, and retrieval deficits. The acquisition

mechanism was assessed with a general learning paradigm

(the immediate and delayed free recall of a short story) using

the immediate and delayed subtests of the Rivermead

T

S

S

IQ

A

E

D

Table 2

Patients’ test scores in the neurocognitive measures and results of comparisons between the whole group, the low IQ subgroup (IQ b85), and the high IQ

subgroup (IQ z85) with normative data mean values

Normative data Whole group Low IQ subgroup (IQ b85) High IQ subgroup (IQ z85)

Mean Mean F SD t P Mean F SD t P Mean F SD t P P4

Executive functioning

WCST categories 5.57 3.84 F 2.11 5.37 .001 3.00 F 1.98 6.10 .001 4.71 F 1.93 2.04 .055 .006

WCST number

of trials

84.22 113.40 F 21.48 8.91 .001 123.45 F 11.55 15.93 .001 102.86 F 24.51 3.48 .002 .002

WCST total errors 17.05 45.16 F 26.32 7.01 .001 54.00 F 20.47 8.47 .001 35.90 F 28.95 2.98 .007 .024

WCST perseverative

errors

8.78 25.86 F 18.85 5.94 .001 30.77 F 14.41 7.16 .001 20.71 F 21.76 2.51 .021 .080

Attention and speed of information processing

WAIS-III picture

completion

10.7 8.00 F 3.18 5.64 .001 6.43 F 2.59 7.90 .001 9.76 F 2.68 1.60 .125 .005

WAIS-III digit

symbol substitution

10.6 6.75 F 2.19 11.66 .001 5.52 F 1.95 12.48 .001 7.76 F 2.02 6.43 .001 .001

Working memory

WAIS-III arithmetic

calculation

10.4 7.98 F 2.88 5.59 .001 6.30 F 1.69 11.62 .001 9.57 F 2.50 1.52 .145 .003

WAIS-III digits

(forward and backward)

10.3 8.82 F 3.00 3.27 .002 7.17 F 2.33 6.44 .001 10.57 F 2.84 0.44 .666 .001

Explicit memory

RBMT immediate

verbal recall

1.81 1.67 F 0.65 1.43 .161 1.52 F 0.73 1.89 .072 1.84 F 0.50 0.28 .783 .179

RBMT delayed

verbal recall

1.88 1.79 F 0.47 1.30 .201 1.70 F 0.47 1.88 .074 1.89 F 0.46 0.14 .890 .020

RBMT immediate

nonverbal recognition

1.90 1.86 F 0.35 0.78 .440 1.83 F 0.49 0.72 .478 1.84 F 0.37 0.67 .509 .529

WAIS-III information 10.5 9.70 F 3.22 1.64 .108 7.43 F 2.23 6.59 .001 12.00 F 2.45 2.81 .011 .001

Implicit memorya

WFCT studied

word fragments

62.18 57.14 F 18.14 1.57 .121 53.91 F 18.55 1.92 .066 60.90 F 17.92 0.29 .772 .234

WFCT nonstudied

word fragments

32.14 27.44 F 12.23 1.72 .090 22.28 F 10.47 3.23 .002 32.33 F 11.87 0.06 .955 .007

WFCT priming 30.04 29.70 F 15.18 0.10 .919 31.63 F 15.00 0.42 .679 28.57 F 15.39 0.37 .713 .528

WPSCT exemplars

from old categories

20.42 10.16 F 9.20 4.82 .001 9.30 F 7.19 4.55 .001 11.25 F 11.31 3.17 .002 .515

WPSCT exemplars

from new categories

4.70 1.58 F 3.68 2.26 .028 0.79 F 2.51 2.86 .006 2.53 F 4.61 1.32 .191 .156

WPSCT priming 15.72 8.58 F 8.04 3.66 .001 8.51 F 7.85 3.00 .004 8.72 F 8.65 2.74 .008 .936

Everyday memory

RBMT total

profile score

22.19 18.47 F 4.11 5.99 .001 17.39 F 3.73 5.67 .001 19.53 F 4.39 2.65 .016 .102

RBMT orientation 1.88 1.47 F 0.83 3.33 .002 1.09 F 0.95 4.01 .001 1.89 F 0.32 0.20 .841 .006

WFCT indicates word-fragment completion test; WPSCT, word production from semantic categories test.a Normative data from a previous experiment presented at the VII International Symposium on Schizophrenia (March 17-18, 2005; Bern, Switzerland;

Soler MJ, Ruiz JC, Fuentes I, Tomas P. Implicit memory in patients with schizophrenia) comparing patients with schizophrenia (n = 29) and control subjects

(n = 34).

4 Between the subgroups.

J.C. Ruiz et al. / Comprehensive Psychiatry 48 (2007) 276–282278

Behavioral Memory Test (RBMT) [14]. The storage

mechanism was assessed using the information subtest of

the WAIS-III. This subtest is a recall test of information

learned over a delayed period. Finally, the retrieval

mechanism was measured using the immediate nonverbal

recognition task of the RBMT.

Implicit memory was assessed using a perceptual test

(word-fragment completion) and a conceptual test (word

production from semantic categories). In these tasks,

participants have to process a stimulus called a prime (eg,

to judge the familiarity of a list of words using a scale).

Then, they are told to perform another task (eg, to complete

word fragments or to generate words belonging to a specific

category) that makes no reference to the first phase of the

test. The variables of interest in those memory tasks were

the proportion of correctly answered stimuli that are seen in

the first phase and the proportion of correctly answered

stimuli that are not seen in the first phase. The difference

between these 2 proportions is the priming score, which

reflects implicit memory.

Finally, everyday memory aspects were measured with

the RBMT. Performance on this test yields a total profile

score (range = 0-24), which weights each subtest equally in

relation to the others to provide comparable scores across

J.C. Ruiz et al. / Comprehensive Psychiatry 48 (2007) 276–282 279

the battery of tests. The total profile score and the scores on

the subtest of orientation of the RBMT (this subtest is a

battery of 10 questions that make reference to aspects such

as the date of the day, the name of the patient, or the age of

the patient) were used to give objective measures of

everyday memory.

able 3

orrelations between IQ and neuropsychologic measures in the 2 subgroups

f patients with schizophrenia and in the whole group

IQ b85 IQ z85 All patients

r P r P r P

xecutive functioning

WCST categories �0.03 .885 0.51 .017 0.47 .002

WCST number of trials �0.11 .638 �0.63 .002 �0.63 .001

WCST total errors �0.09 .695 �0.63 .002 �0.51 .001

WCST perseverative errors �0.27 .228 �0.57 .007 �0.47 .001

ttention and speed of information processing

WAIS-III picture

completion

0.62 .002 0.34 .136 0.67 .001

WAIS-III digit

symbol substitution

0.62 .002 0.24 .287 0.62 .001

orking memory

WAIS-III arithmetic

calculation

0.48 .021 0.79 .001 0.81 .001

WAIS-III digits

(forward and backward)

0.60 .002 0.49 .024 0.72 .001

xplicit memory

RBMT immediate

verbal recall

�0.11 .634 0.26 .285 0.22 .164

RBMT delayed

verbal recall

0.10 .672 0.31 .202 0.28 .070

RBMT immediate

nonverbal recognition

�0.32 .139 0.18 .473 �0.05 .732

WAIS-III information 0.71 .001 0.62 .003 0.85 .001

plicit memory

WFCT studied

word fragments

0.11 .652 0.29 .230 0.27 .090

WFCT nonstudied

word fragments

0.26 .261 0.51 .025 0.55 .001

WFCT priming �0.05 .830 �0.06 .812 �0.12 .481

WPSCT exemplars

from old categories

�0.14 .547 �0.08 .767 0.03 .872

WPSCT exemplars

from new categories

�0.36 .107 �0.11 .662 0.08 .629

WPSCT priming �0.01 .958 0.04 .864 0.01 .970

veryday memory

RBMT total profile score 0.03 .906 0.37 .117 0.33 .036

RBMT orientation �0.10 .649 0.26 .279 0.34 .028

3. Results

Analyses were conducted using the SPSS statistical

package for Windows (version 11, SPSS, Chicago, Ill).

All statistical analyses were based on 2-tailed tests of

significance. The Bonferroni method was applied to control

for multiple comparisons; thus, the adjusted critical P value

was .008 (.05/6), because implicit memory was scored using

6 measures, with the cognitive domain having the greater

number of measures.

The 2 groups of patients with schizophrenia showed

significant differences in age (t = 2.79; P = .008) and

intelligence (t = 8.80; P = .001). There was no statistically

significant difference between the 2 groups in length of

illness and level of education (Table 1). Because the 2 groups

differed in age, this variable was entered as a covariate in

the analysis of between-group differences in scores on the

neurocognitive tests.

Test scores on the various cognitive tasks for the whole

group of patients are presented in Table 2. These scores

were compared with general population norms provided that

such normative data exist using t tests. As expected, the

results revealed that, in most of the measures, patients with

schizophrenia show performance levels lower than the

normative mean values for the same age group; this was

the case for the executive function, attention, speed of

information processing, working memory performance and

capacity, conceptual implicit memory (word production

from semantic categories test), and everyday memory total

scores and orientation subtest score. There was no differ-

ence in the explicit memory tasks of immediate and delayed

verbal recall, immediate nonverbal recognition, general

information, and perceptual implicit memory task (word-

fragment completion test).

3.1. Group comparisons

Once the general neurocognitive profile of the group of

patients was established, data were analyzed looking for

differences within the group associated with IQ. The 2 IQ

groups were compared with the normative data and with one

another on the different measures using the v2 test or t testsdepending on the nature of the variable measured or using

analyses of covariance when age was correlated with the

dependent measure considered. The mean values and

standard deviations for the 2 groups on the various cognitive

measures are presented in Table 2. The low intellectually

functioning group performed at levels lower than normative

data in the executive functioning (P = .001), attention and

speed of information processing (P = .001), working

memory (P = .001), WAIS-III information measure (P =

.001), conceptual implicit memory (P = .004), and

everyday memory (P = .001) scores. The high intellectually

functioning group showed significant differences in the

number of trials (P = .002) and total errors (P = .007) of

the WCST, in the digit symbol substitution (P = .001) of

the WAIS-III, and in the conceptual implicit memory

measure (P = .008).

When both groups were compared, significant differ-

ences appeared in the 4 subscales of the WAIS-III that were

used to evaluate working memory performance and capac-

ity, attention, and speed of information processing (P V.005). In 2 WCST scores, differences between the groups

were significant: the number of categories achieved (P =

.006) and the number of trials (P = .002). The comparison

in explicit memory measures only showed differences in the

WAIS-III information score (P = .001). Both groups

performed at the same level in the 2 implicit memory tasks,

T

C

o

E

A

W

E

Im

E

J.C. Ruiz et al. / Comprehensive Psychiatry 48 (2007) 276–282280

except in one measure, the proportion of nonstudied word

fragments completed in the perceptual implicit memory task

(P = .007). The patterns of results were quite similar

in everyday memory. Differences only appeared in the

orientation scale when it was measured using profile scores

(P = .006).

3.2. Correlations between IQ and cognitive measures

Pearson’s correlations were calculated between IQ and

the cognitive measures for the whole group of patients

(Table 3). The results showed that IQ was related to all

WCST scores: categories (r = 0.47; P = .002); number of

trials (r = �0.63; P b .001); total errors (r = �0.51; P =

.001); and perseverative errors (r = �0.47; P = .001). Level

of IQ and the attention measures correlated significantly:

WAIS-III picture completion scores (r = 0.67; P = .001)

and WAIS-III digit symbol substitution scores (r = 0.62;

P = .001). The same pattern of results was observed in the

working memory measures: WAIS-III arithmetic calculation

(r = 0.81; P = .001) and digits (forward and backward;

r = 0.72; P = .001). In the case of explicit memory, IQ was

correlated with WAIS-III information scores (r = 0.85;

P = .001). Implicit memory did not correlate significantly

with IQ. Two of the measures used to explore everyday mem-

ory also correlated significantly with IQ: orientation (r =

0.34; P = .028) and total profile score (r = 0.33; P = .036).

Pearson’s correlation coefficients were also computed to

explore the relationship between IQ and the cognitive

measures in each patient group (Table 3). There was no

difference between the correlations obtained in both groups

when the correlations were compared using a Z test. The

absence of differences between groups in the correlations

obtained could probably be a result of the small sample size

of the groups.

4. Discussion

Schizophrenia and memory dysfunction are significantly

associated. Numerous studies have demonstrated that

memory deficits are core features of schizophrenia. The

evidence is so clear that the MATRICS group included

memory deficit among the 7 separable fundamental dimen-

sions of cognitive deficit in schizophrenia [15]. In contrast,

the nature of the disorder with respect to general intellectual

functioning is more heterogeneous. Patients with schizo-

phrenia could show intact, mild, moderate, or severe

intellectual impairment. As a consequence, many studies

have been conducted to clarify the profile of cognitive

deficits associated with the different intellectual impairment

levels shown by patients with schizophrenia. In general,

results show that even intellectually intact patients have

deteriorated performance in some cognitive areas: executive

functioning, attention, speed of processing, and memory.

Specifically, in the neurocognitive memory domain,

although memory is globally described as impaired in the

literature, results are heterogeneous probably because of the

different aspects or types of memory that can be measured

and because of the great number of different tasks used. In

this study, we focused on the evaluation of 4 dimensions of

memory using different tasks for each one with the aim of

clarifying which aspects of memory are and which are not

deteriorated in schizophrenia. Then, the aim was to analyze

how patterns of memory function differ in relation to

intellectual functioning.

Standard intelligence tests place a relatively heavy

emphasis on measures of memory, including semantic

memory, episodic memory, and working memory. It is then

expected that IQ will correlate with these memory measures,

and the literature confirms this statement. Even in the case

of everyday memory, a measure not included in intelligence

tests, the correlation is significant [14]. In the case of

implicit memory, not much is known about its relation with

IQ. Precisely, one of the main interests of our study was to

clarify this relation.

In the whole sample of patients, we found evidence for

distinct patterns of memory dysfunction in schizophrenia.

With respect to working memory, the patients with

schizophrenia performed at significantly lower levels as

compared with normative control subjects. Many of the

studies in this area have found impairment in schizophrenia,

although few patients have shown normal function or only a

trend toward a poorer performance [4]. The studies that show

this result of preserved working memory tend to include

control subjects who are matched for IQ, age, or education;

however, there are some studies that have found a working

memory impairment using well-controlled designs [16].

Results showed preserved explicit memory in the group.

Globally, these results are not in line with some previous

results. Studies that have used explicit tests such as free and

cued recall, verbal fluency tests, and semantic processing

tests have reported that the performance of patients with

schizophrenia is impaired [1,17,18]. However, previous

work had demonstrated heterogeneity in the results dis-

played in schizophrenia in the wide variety of tasks used to

measure memory [19,20].

Implicit memory appeared to be preserved when percep-

tual implicit memory was measured but appeared to be

impaired when the task was conceptual. Literature always

presents implicit memory as a normal cognitive function in

schizophrenia [4]. However, differences within implicit

memory should be considered. In a previous study, we

found a dissociation in priming between healthy and patient

groups depending on the task. In the word-fragment test,

priming was similar in the 2 groups. However, in the word

production test, the priming obtained from patients with

schizophrenia was lower than that obtained from healthy

control subjects. These results could be explained because

there are obvious differences in task demands posed by

different kinds of tests. Dissociations between implicit

memory tests can be accounted for by postulating a

continuum of tests, from those requiring more perceptual

information (data-driven tests) to those requiring knowledge

J.C. Ruiz et al. / Comprehensive Psychiatry 48 (2007) 276–282 281

of meaning (conceptually driven tests) [21-23]. Word-

fragment completion is a data-driven task in which the

fragments evoke the perceptual identification record of the

target. In this test, the stimulus presented during the study

phase is shown in a perceptually related form, albeit

partially. The letters in the fragment, which are drawn

randomly from the word, are poor cues for locating words in

the lexicon. Thus, perceptual overlap between study and test

stimuli is sufficient to produce priming [24].

Our data show equal priming in healthy control subjects

and patients with schizophrenia (see the meta-analysis of

implicit memory tasks with nonclinical populations in

Reference [25]), which suggests that perceptual comparison

processes are apparently not affected by the cognitive

deficits of schizophrenia.

In contrast, word production from semantic categories is

a conceptually driven task in which the information

provided in the test phase is semantically related to the

information studied and requires a response based on the

meaning of the stimulus. This task involves an elaborative

processing that is predominantly conceptual and, therefore,

seems to be more affected by the cognitive deficits present

in schizophrenia.

Everyday memory was also impaired. The distribution of

profile scores for patients on the RBMT ranges from 17 to

21. This means that patients with schizophrenia have a poor

everyday memory and that their performance is poorer than

that of healthy normative control subjects of a comparable

age range [26]. Previous studies with healthy control subjects

have obtained a slight correlation between the RBMT and

intelligence, although this does not account for more than

approximately 10% of the variance in performance on the

RBMT. The results of our study with patients with

schizophrenia show that, although there was a significant

correlation between intelligence and everyday memory, there

was no significant difference in this form of memory when

the 2 IQ groups were compared. The 2 IQ groups obtained

significant differences only in the orientation subtest.

Finally, results in executive functioning were similar to

the findings of a recent study by Hughes et al [27] with

62 patients. They found differences between the perfor-

mance of patients with schizophrenia and that of control

subjects in the number of categories achieved and the

number of perseverative errors on the WCST (see also the

review of Laws [28]). The patterns of attention and speed of

information processing deficits in the whole group were also

similar to those obtained in another study [8]. Patients with

schizophrenia perform worse than do healthy control

subjects. Taken together, these results are in line with those

of authors who argue that executive deficits constitute a

necessary dysfunction in schizophrenia [8,9]. Nonetheless,

this statement should be taken with caution because, as our

results show, executive functioning deficits appear to be

associated with IQ. These results are not new, and, as

Landro et al [19] indicated, significant differences between

patients with schizophrenia and healthy control subjects, on

the number of categories achieved and on the perseveration

index of the WCST, disappear when the patients are selected

with normal general intellectual function.

When the profile of memory data was analyzed

separately in the 2 IQ subgroups of patients with schizo-

phrenia, the pattern of results changed. The low intellectu-

ally functioning group performed at lower levels as

compared with the healthy control subjects, and the high

intellectually functioning group performed at the same level

in working memory. Both groups did not show differences

in comparison with normative data and with one another in

explicit memory, except in the information scale of the

WAIS-III. The low IQ group, but not the high IQ group,

showed differences with normative data. Results in the

implicit memory tasks replicated those of the whole group.

Preserved perceptual implicit memory and compromised

conceptual implicit memory patterns were similar in both

groups. However, the patterns were different in everyday

memory. The high intellectually functioning group showed a

performance level similar to that of the healthy control

subjects, but the performance in the low intellectually

functioning group was deteriorated.

In summary, patients with an IQ higher than 85 (mean

IQ = 98) perform at a standard level in working memory,

explicit memory, everyday memory, and implicit memory

when their performance is measured with a perceptual task.

They only perform at lower-than-standard levels in implicit

memory when their performance is measured using a

conceptual task. The profile of results changes when the

patients’ IQ is lower than 85 (mean IQ = 73). They show

deficits in working memory, everyday memory, and explicit

memory when their performance is measured using the

information scale of the WAIS-III and in implicit memory

when their performance is measured with a conceptual task.

These mean that, although intellectual functioning appears

to be related to working memory and everyday memory, it is

not associated with explicit and implicit memory.

Despite the fact that patients with schizophrenia have key

cognitive deficits, such as executive functioning, attention,

andmemory, their IQ seems to be related to all of them but not

globally to memory. Within the memory domain, there are

differences associated with the explicit-implicit dichotomy

and with the specific measure used to assess memory. Our

results are in line with the hypothesis of Reber et al [29], who

considered that the implicit systems operate largely indepen-

dently of standard measures of cognitive capability, such as

intelligence. In fact, Wagner and Sternberg [30] differentiated

between tacit and explicit intelligence. Although tacit

knowledge is practical, informal, and usually acquired

indirectly or implicitly, explicit intelligence is evaluated

primarily by tasks usually found on mental ability tests.

5. Conclusions

This study presents relevant data in relation to implicit

memory and everyday memory impairment in schizophrenia

J.C. Ruiz et al. / Comprehensive Psychiatry 48 (2007) 276–282282

and its relation to IQ: (1) the type of implicit memory

measured determines the presence or absence of a deficit;

(2) perceptual implicit memory is preserved in schizophre-

nia independently of the intellectual functioning level of the

patients; and (3) conceptual priming is deteriorated even in

intellectually preserved patients. These findings suggest

that, for its complete evaluation, implicit memory should be

assessed with different tasks because it is not a unique

entity. Everyday memory is also impaired in association

with IQ. It only appears to be impaired in patients with

deteriorated intellectual function.

Overall, our results have important implications for

identifying suitable treatment and rehabilitation interven-

tions. These interventions should focus on the assessment of

individual cognitive functions and on the memory capacities

demanded of patients.

Acknowledgment

This study was supported by a grant from the Ministry

of Education and Science of Spain (No. SEJ2006-07055/

PSIC).

References

[1] Aleman A, Hijman R, de Haan EHF, Kahn RS. Memory impairment in

schizophrenia: a meta-analysis. Am J Psychiatry 1999;156:1358 -66.

[2] McKenna PJ, Clare L, Baddeley AD. Schizophrenia. In: Baddeley AD,

Wilson BA, Watts FN, editors. The handbook of memory disorders.

New York7 John Wiley and Sons; 1995. p. 271 -92.

[3] Kuperberg G, Heckers S. Schizophrenia and cognitive function. Curr

Opin Neurobiol 2000;10:205 -10.

[4] McKenna PJ, Ornstein T, Baddeley AD. Schizophrenia. In: Baddeley

AD, Kopelman MD, Wilson BA, editors. The handbook of mem-

ory disorders. 2nd ed. West Sussex (UK)7 John Wiley and Sons; 2002.

p. 413 -35.

[5] Keri J, Kanka Z. Critical evaluation of cognitive dysfunctions as

endophenotypes of schizophrenia. Acta Psychiatr Scand 2004;110:

83 -91.

[6] Palmer BW, Heaton RK, Paulsen JS, Kuck J, Braff D, Harris MJ, et al.

Is it possible to be schizophrenic yet neuropsychologically normal?

Neuropsychology 1997;11:437-46.

[7] Goldstein G, Shemansky WJ. Influences on cognitive heterogeneity in

schizophrenia. Schizophr Res 1995;18:59 -69.

[8] Weickert TW, Goldberg TE, Gold JM, Bigelow LB, Egan MF,

Weinberger DR. Cognitive impairment in patients with schizophrenia

displaying preserved and compromised intellect. Arch Gen Psychiatry

2000;57:907-13.

[9] Badcock JC, Dragovic M, Waters AV, Jablensky A. Dimensions

of intelligence in schizophrenia: evidence from patients with

preserved, deteriorated and compromised intellect. J Psychiatr Res

2005;39:11 -9.

[10] Kremen WS, Seidman LJ, Farone SV, Tsuang MT. Intelligence

quotient and neuropsychological profiles in patients with schizophre-

nia and in normal volunteers. Biol Psychiatry 2001;50:453-62.

[11] Rund BR, Sundet K, Asbjorsen A, Egeland J, Landro NI, Lund A,

et al. Neuropsychological test profiles in schizophrenia and non-

psychotic depression. Acta Psychiatr Scand 2005;111:1 -10.

[12] Blyler CR, Gold JM, Iannone VN, Buchanan RW. Short form of the

WAIS-III for use with patients with schizophrenia. Schizophr Res

2000;46:209-15.

[13] Heaton RK, Chelune CJ, Talley JL, Kay GC, Curtiss G. Wisconsin

Card Sorting Test manual—revised and expanded. Odessa (Tex)7

Psychological Assessment Resources; 1993.

[14] Wilson BA, Cockburn JM, Baddeley AD, Hiorns R. The Rivermead

Behavioural Memory Test: supplement two. 2nd ed. Bury St Edmunds

(UK)7 Thames Valley Test Co; 1991.

[15] Marder SR, Fenton W. Measurement and treatment research to

improve cognition in schizophrenia: NIMH MATRICS initiative to

support the development of agents for improving cognition in

schizophrenia. Schizophr Res 2004;72:5 -9.

[16] Iddon J, McKenna PJ, Sahakian BJ, Robbins TW. Impaired generation

and use of strategy in schizophrenia: evidence from visuospatial and

verbal tasks. Psychol Med 1998;28:1049-62.

[17] Duffy L, O’Carroll R. Memory impairment in schizophrenia—

a comparison with that observed in the alcoholic Korsakoff syndrome.

Psychol Med 1994;24:155-65.

[18] Elvevag B, Weinstock DM, Akil M, Kleinman JE, Goldberg TE.

A comparison of verbal fluency tasks in schizophrenic patients and

normal controls. Schizophr Res 2001;51:119 -26.

[19] Landro NI, Pape-Ellefsen E, Hagland KO, Odland T. Memory deficits

in young schizophrenics with normal general intellectual function.

Scand J Psychol 2001;42:459-66.

[20] Rushe TM, Woodruff PWR, Murray RM, Morris RG. Episodic

memory and learning in patients with chronic schizophrenia.

Schizophr Res 1999;35:85 -96.

[21] Brebion G, Smith M, Gorman J, Malaspina D, Sharif Z, Amador X.

Memory and schizophrenia: differential link of processing speed and

selective attention with two levels of encoding. J Psychiatr Res 2000;

34:121-7.

[22] Brebion G, Gorman JM, Malaspina D, Amador X. A model of verbal

memory impairments in schizophrenia: two systems and their

associations with underlying cognitive processes and clinical symp-

toms. Psychol Med 2004;35:133 -42.

[23] Roediger HL, Blaxton TA. Retrieval modes produce dissociations in

memory for surface information. In: Gorfein D, Hoffman RR, editors.

Memory and cognitive processes: the Ebbinghaus Centennial Con-

ference. Hillsdale (NJ)7 Erlbaum; 1987. p. 349 -79.

[24] Fay S, Isingrini M, Clarys D. Effects of depth-of-processing and

ageing on word-stem and word-fragment implicit memory tasks: test

of the lexical-processing hypothesis. Eur J Cogn Psychol 2005;17:

785 -802.

[25] Light LL, Prull MW, La Voile DJ, Healy MR. Dual-process theories of

memory in old age. In: Perfect TJ, Maylor EA, editors. Models of

cognitive aging. New York7 Oxford University Press; 2000. p. 238-300.

[26] McKenna PJ, Tamlyn D, Lund CE, Mortimer AM, Hammond S,

Baddeley AD. Amnesic syndrome in schizophrenia. Psychol Med

1990;20:967-72.

[27] Hughes C, Kumari V, Soni W, Das M, Binneman B, Drozd S, et al.

Longitudinal study of symptoms and cognitive function in chronic

schizophrenia. Schizophr Res 2002;59:137 -46.

[28] Laws KR. A meta-analytic review of Wisconsin Card Sort studies in

schizophrenia: general intellectual deficit in disguise? Cogn Neuro-

psychiatry 1999;4:1 -35.

[29] Reber AS, Walkenfeld FF, Hernstadt R. Implicit and explicit learning:

individual differences and IQ. J Exp Psychol Learn Mem Cogn 1991;

17:888-96.

[30] Wagner RK, Sternberg RJ. Tacit knowledge and intelligence in

everyday word. In: Sternberg RJ, Wagner RK, editors. Practical

intelligence: nature and origins of competence in the everyday word.

Cambridge (UK)7 Cambridge University Press; 1986. p. 51 -83.