Intellectual Functioning and Memory Deficits in Schizophrenia

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    Intellectual functioning and memory deficits in schizophrenia

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

    aDepartment of Methodology, Facultad de Psicologa, 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, Spain

    dCenter 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 withpatterns 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 workingmemory 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.

    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 clearpattern. 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

    0010-440X/$ see front matterD 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: [email protected] (J.C. Ruiz).

    Comprehensive Psychiatry 48 (2007) 276282

    www.elsevier.com/locate/comppsych

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    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.Q

    The 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 todetect 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 andclinical characteristics of the patients are

    shown inTable 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 administeredto 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 scoredhigher 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) usingthe immediate and delayed subtests of the Rivermead

    Table 1

    Sociodemographic characteristics of all patients

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

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

    IQ (mean F SD) 73.09 F 8.92 98.38 F 10.14

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

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

    Duration of illness

    (y; mean F SD)

    15.39 F 8.71 19.33 F 8.38

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    Behavioral Memory Test (RBMT) [14]. The storagemechanism 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 specificcategory) 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

    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 numberof 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 memoryRBMT 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.

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    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.

    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 Pvalue

    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 statisticallysignificant 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 tasksfor 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 wasthe 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 fordifferences 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 orttests

    depending 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 2groupson 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,

    Table 3

    Correlations between IQ and neuropsychologic measures in the 2 subgroups

    of patients with schizophrenia and in the whole group

    IQ b85 IQ z85 All patients

    r P r P r P

    Executive 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

    Attention and speed of information processing

    WAIS-III picture

    completion

    0.62 .002 0.34 .136 0.67 .001

    WAIS-III digitsymbol substitution

    0.62 .002 0.24 .287 0.62 .001

    Working 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

    Explicit 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

    Implicit memoryWFCT 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

    Everyday 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

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    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

    Pearsons 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).

    Pearsons 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 shownnormal 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 inthe 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, wefound 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

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    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 elaborativeprocessing 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 healthynormative 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 weresimilar 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 ofinformation 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 controlsubjects, 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,

    and memory, 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

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

    PSIC).

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