Cognitive Neuropsychiatry, 2015 Vol. 20, No. 1, 41–52, http://dx.doi.org/10.1080/13546805.2014.957380
Is conceptual implicit memory impaired in schizophrenia? Evidence from lexical decision and category verification Valéria R.S. Marquesa,b, Pietro Spataroa, Vincenzo Cestaria,c, Antonio Sciarrettad, Francesca Iannarellia and Clelia Rossi-Arnauda* a
Department of Psychology, Sapienza University of Rome, Via dei Marsi 78, 00185 Rome, Italy; CAPES Foundation, Ministry of Education of Brazil, Setor Bancário Norte, Quadra 2, Bloco L, Lote 06, CEP 70040-020 - Brasília, DF, Brazil; cCell Biology and Neurobiology Institute, C.N.R National Research Council of Italy, Via del Fosso di Fiorano 64/65, 00143 Rome, Italy; dAcute Psychiatric Care Unit, Department of Mental Health RM-G, San Giovanni Evangelista Hospital, Via Antonio Parrozzani 3, 00019 Tivoli, Italy
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(Received 20 February 2014; accepted 15 August 2014) Introduction. Implicit memory tasks differ along two orthogonal dimensions, tapping the relative involvement of perceptual/conceptual and identification/production processes. Previous studies have documented a dissociation between perceptual (spared) and conceptual (impaired) implicit memory, using in the latter case a production task (category exemplar generation), in which there is high response competition during the retrieval phase. The present study sought to determine whether the perceptual/ conceptual dissociation held when comparing two identification tasks, in which there is no response competition at retrieval. Methods. In two experiments, repetition priming was assessed in 44 schizophrenic patients and 46 healthy controls in lexical decision (a test based on perceptual identification processes) and category verification (a test based on conceptual identification processes). Results. Schizophrenic patients achieved a priming as high as that of controls in the lexical decision task. In contrast, only controls exhibited significant priming in the category verification task. Conclusions. It is concluded that schizophrenia is associated with a specific deficit in conceptual implicit memory, irrespective of the degree of response competition in the test phase. Keywords: implicit memory; repetition priming; conceptual priming; schizophrenia
Memory impairment represents one of the most essential neurocognitive features of schizophrenia (Stone & Hsi, 2011). Significant deficits have been reported in episodic memory (Aleman, Hijman, de Haan, & Kahn, 1999), as well as in verbal and visuospatial working memory (Forbes, Carrick, McIntosh, & Lawrie, 2009). However, the extent to which this impairment generalises to implicit memory is less well understood. Implicit memory refers to the unintentional retrieval of information encoded during the study phase and is typically investigated through repetition priming tasks, in which memory is demonstrated by changes in the speed and/or accuracy in the processing of previously experienced stimuli, relative to an appropriate baseline (Mulligan & Besken, *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
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2011). For instance, in word-fragment completion, participants are presented with words at encoding (e.g., scissor) and are later asked to complete unique-solution fragments (e.g., s _ _ ss _ r) with the first words that come to mind. Repetition priming is indicated by higher completion rates for fragments corresponding to previously processed (old) words than for fragments corresponding to previously unprocessed (new) words (Spataro, Mulligan, & Rossi-Arnaud, 2010). Following the Transfer-Appropriate-Processing theory (Franks, Bilbrey, Guat Lien, & McNamara, 2000), a broad distinction has been drawn between perceptually driven implicit tests (e.g., lexical decision), that rely on perceptual processes, and conceptually driven implicit tests (e.g., category exemplar generation), that rely on semantic processes based on the analysis of meaning. Priming in perceptual implicit tasks is reduced following study-test changes in the modality of stimulus presentation (from visual to auditory or vice versa), whereas it is substantially unaffected by semantic versus nonsemantic encoding and by divided attention in the study phase; priming in conceptual tasks, on the other hand, show the opposite pattern of results – it is enhanced by semantic encoding, reduced by divided attention and unaffected by modality changes (Mulligan, 2008; Spataro, Cestari, & Rossi-Arnaud, 2011). Despite its success in explaining a wide range of behavioural and neuropsychological findings, the perceptual/conceptual distinction has been challenged by a series of results first reported by Vaidya et al. (1997) and Gabrieli et al. (1999); see also Prull (2004). Vaidya et al. (1997) found that conceptual elaboration in the study phase enhanced repetition priming in word association (only for weakly associated words) and category exemplar generation, but had no effect on category verification and abstract/concrete classification. A later study by Gabrieli et al. (1999) showed that Alzheimer’s disease patients had impaired priming in word-stem completion and category exemplar generation but intact priming in picture naming and category verification; moreover, in young adults, the same pattern of results was obtained by dividing attention during the encoding phase, which reduced repetition priming in word-stem completion and category exemplar generation, but not in picture naming and category verification. To account for these findings, the authors proposed that perceptual and conceptual implicit tasks can be dissociated in two subclasses, on the basis of the presence or the absence of competition among alternative responses during the retrieval phase. Identification tests such as lexical decision or category verification are those in which the retrieval cues directly guide participants towards unique solutions (low-response competition). For instance, when participants in a lexical decision task are presented with the word judge (or the non-word ludge) and instructed to decide as rapidly as possible whether each item represents a legal word or a non-word, the identification of the stimulus is sufficient to determine the unique correct response (word or non-word). In contrast, production tasks such as wordstem completion or category exemplar generation are those in which the retrieval cues admit multiple legitimate solutions (high-response competition). For example, when participants are presented with a word-stem like pre__ and told to produce the first word that comes to mind, they can choice between multiple correct responses, including premise, present, pressure, preview and prejudice. According to Vaidya et al. (1997) and Gabrieli et al. (1999), the achievement of full priming (i.e., greater-than-zero) would require the allocation of a greater amount of study-phase attentional resources in production than in identification tasks. This is because only in production tests the target stimuli must be selected among numerous competing solutions: in such a circumstance, the retrieval of the encoded items depends on some external assistance,
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such as study-phase elaboration. On the other hand, identification tasks lack response competition because the to-be-remembered stimuli are provided during the test phase: in such a circumstance, any study-phase retrieval of the items in response to an encoding task results in significant priming, and semantic elaboration does not add anything to this direct priming (Gabrieli et al., 1999; Vaidya et al., 1997). When considered in light of the earlier two distinctions, the results of previous studies examining implicit memory in schizophrenia are mixed. Overall, there is good evidence indicating that perceptual identification tasks are spared in schizophrenic patients, since they have been reported to achieve levels of repetition priming comparable to those of healthy controls in lexical decision (Sponheim, Steele, & McGuire, 2004), perceptual identification (Schwartz, Rosse, & Deutsch, 1993) and word-fragment completion with unique solutions (Ruiz, Soler, Fuentes, & Tomás, 2007; Soler, Ruiz, Vargas, Daśi, & Fuentes, 2011). On the other hand, data concerning the perceptual production task of word-stem completion are equivocal, with studies showing both impaired priming (Kern, Hartzell, Izaguirre, & Hamilton, 2010; Randolph, Gold, Carpenter, Goldberg, & Weinberger, 1993) and intact priming (Clare, McKenna, Mortimer, & Baddeley, 1993; Kazes et al., 1999; Perry, Light, Davis, & Braff, 2000). With regard to conceptual implicit memory, available findings indicate that schizophrenic patients obtain lower levels of repetition priming in the production task of category exemplar generation (Ruiz et al., 2007; Soler, Ruiz, Fuentes, & Tomás, 2007; but see Schwartz et al., 1993). To our knowledge, the performance of this clinical population has not been previously examined in the conceptual identification task of category verification (Mulligan & Peterson, 2008), although Rossell and David (2006) found that schizophrenics were significantly less accurate than controls in deciding whether a given exemplar belonged to a category or not. However, no encoding phase was included in the latter study, implying that the exemplars were not primed. In the present study, we sought to ascertain whether schizophrenic patients show a dissociation between perceptual and conceptual implicit memory, when both tasks are based on identification processes and therefore do not involve response competition. As briefly reviewed earlier, evidence in support of a deficit in conceptual implicit memory in schizophrenia primarily comes from reduced repetition priming in category exemplar generation (Ruiz et al., 2007; Soler et al., 2007), a task which is heavily based on production processes (Gabrieli et al., 1999). This suggests the alternative possibility that the impairment in schizophrenic patients might not be caused by the conceptual nature of the category exemplar generation task, but rather by the necessity to select the encoded items among multiple competitors at the time of retrieval (i.e., by the production nature of the task). The latter proposal is supported by the fact that the only other implicit test in which SC patients have been found to perform worse than healthy controls is word-stem completion (Kern et al., 2010; Randolph et al., 1993; but see Clare et al., 1993, Kazes et al., 1999 and Perry et al., 2000, for different results), which is also classified as a production task (Gabrieli et al., 1999). To ascertain whether the perceptual/conceptual distinction held also when using two non-competitive identification tests, we compared repetition priming in schizophrenic patients and age-matched healthy controls in lexical decision (a perceptual identification task) and category verification (a conceptual identification task). Experiment 1 Experiment 1 aimed at confirming previous evidence indicating that schizophrenic patients exhibit intact repetition priming in the lexical decision task (Sponheim et al., 2004).
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Method Participants Twenty-two schizophrenic patients (11 females) and 24 healthy controls (15 females) participated in Experiment 1. There were no differences between the two groups in terms of age, M(schizophrenics) = 43.6 vs. M(controls) = 38.2, t(44) = 1.26, p = .21, and the ratio of males to females, χ(1)2 = 1.02, p = .31. However, healthy controls had a higher number of years of formal education, compared to schizophrenic patients, M(schizophrenics) = 14.0 vs. M(controls) = 16.1, t(44) = −2.01, p = .05. As a consequence, the latter variable was included as a covariate in the following statistical analyses. Patients were recruited from the Acute Psychiatric Care Unit of the “San Giovanni Evangelista” Hospital (Tivoli, Italy), after approval from the local Research Ethics Board. All of them met the standard diagnostic criteria for schizophrenia, as determined by the Structured Clinical Interview of Diagnostic and Statistical Manual of Mental Disorders (DSM-IV, 4th ed., American Psychiatric Association, 1994), medical history and the joint consensus of the senior psychiatrists of the research team. Exclusion criteria were as follows: no history of substance abuse, traumatic brain injury, epilepsy or other adverse neurological conditions. Schizophrenic patients were stabilised by at least one week at the time of testing and treated with antipsychotic neuroleptics at clinically determined dosages – atypical only: N = 13; typical only: N = 6; both: N = 3. The mean daily oral dose was 538 chlorpromazine equivalents. Symptom severity indexes, as assessed with the Positive and Negative Syndrome Scale for Schizophrenia (PANSS: Kay, Opler, & Lindenmayer, 1988), were 17.35 (positive scale), 22.64 (negative scale) and 35.42 (general psychopathology). Control participants were recruited from a variety of sources, including university employees, hospital staff and random search from people attending a community centre near the Hospital “San Giovanni Evangelista” (Tivoli, Rome). All of them denied a history of psychiatric disorders or other neuropsychological diseases, including alcohol and substance abuse. Written informed consent was obtained from all participants, after a brief explanation of the study procedures. Materials They were represented by 30 critical words selected from the LexVar database (http:// www.istc.cnr.it/it/grouppage/lexvar), and previously employed by Spataro, Longobardi, Saraulli, and Rossi-Arnaud (2013). This original set was divided in two lists of 15 words each (A–B), matched as closely as possible for length in letters (M = 7.60–7.73), written frequency (M = 74.47–79.33; taken from the CoLFIS vocabulary: http://www.istc.cnr.it/ grouppage/colfis), familiarity (M = 6.01–6.13), imageability (M = 5.42–5.22) and concreteness (M = 6.08–5.88). Twenty non-critical words, with similar properties, were also selected from the earlier database, to be used as practice items. Finally, 35 legal pronounceable non-words were created for the purposes of test, by randomly changing one letter into real words (see Spataro et al., 2013, for examples). Procedure During the encoding phase, participants were presented with a total of 40 items, including 15 critical words, 15 filler words and 10 practice words. Each trial comprised a fixation point for 1,000 ms, a word for 2,000 ms and a pause for 1,500 ms. All words appeared centrally on the computer screen and were displayed in white against a black background. Half of the participants were presented with the words of List A, whereas the words of
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List B were used only during the test phase to compute the baseline reaction times; for the other half of the sample, the assignment of the lists was reversed. Participants were simply instructed to read the words aloud (to ensure correct identification: Mulligan & Peterson, 2008). Learning was incidental, since participants were not told to remember the words. After a brief interval (2–3 minutes of free-flowing conversation), the lexical decision task was administered. Participants were presented with a total of 70 items, including 30 critical words (15 old and 15 new), 30 legal pronounceable non-words and 10 practice words (five words and five non-words). Each trial comprised: (1) a fixation point for 1,000 ms; (2) a test item (either a word or a non-word), which remained on the screen until participants’ response and (3) a pause for 1,500 ms. The instructions were to decide as rapidly and accurately as possible whether each letter string represented a real Italian word or a non-word, by pressing two different keys of a response pad (RB-834 Model, Cedrus Corporation TM). No mention was made about the relationship with the encoding phase. Results Errors and reaction times (RTs) >2.5 SD from the overall mean of each participant were excluded (2.2% of the data). Only the RTs to “word” responses were taken into account in the primary analysis (Mulligan & Peterson, 2008). A 2 (item type: old vs. new words) × 2 (group: schizophrenics vs. controls) analysis of covariance (ANCOVA), considering item type as a within-subjects variable, group as a between-subjects variable and the number of years of education as a covariate, revealed: (1) a significant main effect of item type, F(1, 43) = 5.08, MSE = 10,847, p < .05, indicating that lexical decisions were faster to old than new words, M = 1,104 vs. M = 1,172 ms; and (2) a significant main effect of group, F(1, 43) = 6.51, MSE = 388,273, p ≤ .01, indicating that the responses of schizophrenic patients were slower than those of healthy controls, M = 1,311 vs. M = 965 ms. However, the interaction between item type and group did not reach the significance level, F(1, 43) = 0.36, MSE = 10,847, suggesting that the two groups exhibited comparable effects of item type. In agreement, a series of independent t-tests showed that repetition priming, computed as the difference between the RTs to new words minus the RTs to old words, shortened lexical decision latencies to the same extent in healthy controls and schizophrenic patients, M = 45 vs. M = 93 ms, t (44) = 1.09, p = .28 (see Figure 1), and that both priming scores were significantly >0, t
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Figure 1. Experiment 1: Mean reaction times in the lexical decision task, as a function of item type (old vs. new exemplars) and group (schizophrenics vs. controls). Bars represent standard errors.
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(23) = 3.25, p < .01and t(21) = 2.13, p < .05, respectively. No significant correlations were found between repetition priming and the PANSS scores of schizophrenic patients: −0.29 < r(22) < 0.09, p > .24. Priming was also uncorrelated with the participants’ years of education, r(46) = −0.14, p = .36. The same ANCOVA as mentioned earlier found that accuracy (i.e., the percentages of correct “word” responses) did not vary as a function of item type, M(old) = 98% vs. M(new) = 97%, F(1, 43) = 0.01, MSE = 0.001, or group, M(schizophrenics) = 98% vs. M(controls) = 97%, F(1, 43) = 0.60, MSE = 0.003. Moreover, the two variables did not interact, F(1, 43) = 0.66, MSE = 0.001. In summary, Experiment 1 showed that, in a lexical decision task, schizophrenic patients benefited from repetition priming to the same extent as healthy controls. Such a finding replicates the results reported by Sponheim et al. (2004) and, more generally, is in line with the hypothesis that perceptual implicit memory is intact in schizophrenia (Ruiz et al., 2007; Soler et al., 2007).
Experiment 2 Experiment 2 extended our investigation to a conceptual implicit task based on identification processes, namely, category verification (Mulligan & Peterson, 2008). The latter task does not meet the standard requirements of a conceptual implicit task – as indicated by non-significant effects of levels-of-processing and divided attention in the study phase (Gabrieli et al., 1999; Vaidya et al., 1997). However, there is no doubt that it is based on the retrieval of semantic representations because the repetition of encoded exemplars produces strong deactivations in the left prefrontal areas typically involved in the processing of conceptual information (Henson & Rugg, 2003) and priming is not reduced by changes in presentation modality between the study and test phases (Light, Prull, & Kennison, 2000; Vaidya et al., 1997). Method Participants A different sample of 22 schizophrenic patients (9 females) and 22 controls (14 females) participated in Experiment 2. There were no differences between the two groups in terms of age, M(schizophrenics) = 37.2 vs. M(controls) = 38.4, t(44) = −0.27, p = .79, and the ratio of males to females, χ(1)2 = 2.28, p = .13. However, healthy controls reported a higher number of years of formal education, M = 11.50 vs. M = 15.14 years, t(42) = −3.85, p < .001. Because of this difference, the latter variable was included as a covariate in the following statistical analyses. Schizophrenic patients and control participants were recruited following the same general strategy and exclusion criteria described in Experiment 1. Of the schizophrenic patients, 12 were treated with atypical neuroleptics and 10 with typical neuroleptics. The mean daily oral dose was 526 chlorpromazine equivalents. PANSS symptom severity indexes were 17.11 (positive scale), 22.50 (negative scale) and 35.06 (general psychopathology scale). Materials Ninety-six critical words (8 exemplars from 12 categories), from 5 to 11 letters in length, were selected from the category production database compiled by Boccardi and Cappa
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(1997). Such a database reports, in descending order of taxonomic frequency, all the exemplars spontaneously produced by 200 Italian university students in response to a category name. The items chosen for the present experiment did not rank in the five most frequent instances. The critical exemplars were divided into two study lists of 48 items (4 instances from each of the 12 categories), which were counterbalanced across the old and new conditions. The two lists were equated as closely as possible for taxonomic frequency (M = 33.58–36.04) and written frequency (M = 15.50–15.53; taken from the CoLFIS Vocabulary). Each study list was further divided into half, to counterbalance the assignment of the old exemplars to the “yes” and “no” responses. An additional set of 12 exemplars were selected from the same database (four instances from three categories), to be used as practice items during the test phase. Procedure At encoding, 48 critical exemplars were presented individually in the middle of the computer screen. They were shown in white against a black background. Each trial comprised a fixation point for 1,000 ms, a word for 2,000 ms and a pause for 1,500 ms. The general procedure and the instructions were similar to those illustrated in Experiment 1: participants were again asked to read each word aloud, to secure correct identification (Mulligan & Peterson, 2008). Words in the study blocks were randomly ordered subject to the constraint that no more than two exemplars from the same category could appear in a row. After a brief interval (2–3 minutes of free-flowing conversation), the category verification task was administered. Participants were presented with a total of 96 category exemplar pairs, including 48 old exemplars (24 requiring a “yes” response and 24 requiring a “no” response) and 48 new exemplars (again, 24 requiring a “yes” response and 24 requiring a “no” response). Each trial began with a fixation point for 1,000 ms. Then, a category name (e.g., FRUIT) was presented in uppercase letters about 2 cm above the fixation point, for 2,000 ms. Whereas the category name remained visible on the screen, an exemplar (which could be congruent or incongruent with the cued category: pineapple vs. leopard) was presented in lowercase letters about 2 cm below the fixation point, until the participants’ response. A pause of 1,500 ms was interposed between two subsequent trials. Participants were instructed to decide, as rapidly and accurately as possible, whether each exemplar belonged or not to the associated category, by pressing two different keys of a response pad (RB-834 Model, Cedrus Corporation TM). No mention was made about the relationship with the study phase. Results Errors and RTs >2.5 SD from the overall mean of each participant were excluded (2.6% of the data). Only the RTs corresponding to “yes” responses were taken into account in the primary analysis (Mulligan & Peterson, 2008). A 2 (item type: old vs. new exemplars) × 2 (group: schizophrenics vs. controls) ANCOVA, considering item type as a within-subjects variable, group as a betweensubjects variable and number of years of education as a covariate, revealed: (1) a significant main effect of item type, F(1, 41) = 8.05, MSE = 3,186, p < .01, indicating that semantic decisions were faster to old than to new exemplars, M = 1,206 vs. M = 1,258 ms; (2) a significant main effect of group, F(1, 41) = 4.55, MSE = 291,754,
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Figure 2. Experiment 2: Mean reaction times in the category verification task, as a function of item type (old vs. new exemplars) and group (schizophrenics vs. controls). Bars represent standard errors.
p < .05, indicating that schizophrenic patients responded more slowly than healthy controls, M = 1,375 vs. M = 1,089 ms; and (3) a significant interaction between item type and group, F(1, 41) = 8.25, MSE = 3,186, p < .01. A follow-up analysis of simple effects, using the Bonferroni adjustment for multiple comparisons showed that the effect of item type was significant for healthy controls, F(1, 41) = 24.89, p < .001, but not for schizophrenic patients, F(1, 41) = 0.40, p = .53. As illustrated in Figure 2, this interaction indicates that repetition priming, computed as the difference between the RTs to new exemplars minus the RTs to old exemplars, was significantly >0 for healthy controls, M = 78 ms, t(21) = 5.62, p < .001, whereas it did not differ from null priming for schizophrenic patients, M = 25 ms, t(21) = 1.24, p = .23. No significant correlations were found between repetition priming and the PANSS scores of schizophrenic patients: r(22) < 0.23, p > .37. Like in Experiment 1, priming scores were not significantly correlated with the participants’ number of education years: r(44) = 0.12, p = .37. A 2 (item type: old vs. new) × 2 (Group: schizophrenics vs. controls) ANCOVA was also applied to accuracy data (i.e., the percentages of correct “yes” responses). However, this analysis found neither significant main effects – for item type: M(old) = 95% vs. M(new) = 94%, F(1, 41) = 0.61, MSE = 0.002; for group: M(schizophrenics) = 94% vs. M(controls) = 96%, F(1, 41) = 0.33, MSE = 0.007 – nor a two-way interaction between item type and group, F(1, 41) = 0.764, MSE = 0.002. In summary, Experiment 2 extended to a semantic identification task previous findings indicating that conceptually driven implicit memory is significantly impaired in schizophrenia (Ruiz et al., 2007; Soler et al., 2007). On the other hand, we did not replicate the finding that schizophrenic patients are less accurate than controls in making semantic decisions to category exemplar pairs (Rossell & David, 2006). This incongruence might be ascribed to methodological differences: in particular, in the study by Rossell and David (2006), the exemplars were presented for 200 ms, whereas in our experiment, they remained visible until the participant’s response. Discussion The present two experiments sought to establish whether schizophrenic patients showed a dissociation between perceptual and conceptual implicit memory, when both types of memory were measured with tasks based on identification processes and therefore did not
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involve competition between multiple solutions at the time of test (Gabrieli et al., 1999; Vaidya et al., 1997). As mentioned in the Introduction, Ruiz et al. (2007) and Soler et al. (2007) found that repetition priming in schizophrenic patients was comparable to that of healthy controls in the word-fragment completion task, but significantly reduced in the category exemplar generation task. These findings suggest that schizophrenia may be associated with a specific deficit in conceptually driven implicit memory. However, besides the perceptual/ conceptual distinction, the aforementioned tasks also differ in the involvement of identification/production processes. Word-fragment completion is primarily based on identification processes because in most studies (including those by Ruiz et al., 2007, and Soler et al., 2007), the to-be-solved fragments have unique solutions, implying small or no competition during the retrieval phase (Spataro et al., 2010). In contrast, the category generation task is heavily based on production processes (Gabrieli et al., 1999; Vaidya et al., 1997) because participants are instructed to produce the first instances that come to mind in response to a category label: in these conditions, the encoded exemplars must be selected among multiple competing responses. Because of this critical difference, it was deemed important to ascertain whether schizophrenic patients continue to show a dissociation between perceptual and conceptual implicit memory when the tasks are based on non-competitive identification processes. The data obtained in the present experiments provide a clear answer to the above question. Schizophrenic patients and healthy controls reached comparable levels of repetition priming in the perceptual identification task of lexical decision. In contrast, only controls achieved reliable (i.e., non-zero) priming in the conceptual identification task of category verification; schizophrenic patients did not show any facilitation in this test. Therefore, our results extend previous findings showing that schizophrenic patients have reduced priming in the category exemplar generation task (Ruiz et al., 2007; Soler et al., 2007). Furthermore, they suggest that the dissociations between perceptual and conceptual memory observed in these studies were not confounded by the productive nature of category exemplar generation; rather, they reflected a specific deficit in the use of conceptually driven implicit processes, which is independent of the degree of response competition during the retrieval phase. The absence of significant priming in the category verification task raises the question of what mechanisms are impaired in the semantic memory of schizophrenic patients. One plausible explanation for our data is that schizophrenia is associated with an impairment in the ability to use contextual information for biasing conceptual decisions (Cohen & Servan-Schreiber, 1992). Such a hypothesis has two different, but related, implications. The first is that, during the test phase of the category verification task, schizophrenic patients might be less efficient in exploiting the category names to activate related exemplars and inhibit unrelated exemplars. Kiang and Kutas (2005) recorded the N400 component of event-related brain potentials from healthy adults during an unprimed category verification task. The N400 is a well-known negativity whose amplitude is reduced (i.e., less negative) after presentation of a target stimulus conceptually related to a prime. Kiang and Kutas (2005) found that individuals high in schizotypy showed larger (i.e., more negative) N400s to both high- and low-typicality exemplars, suggesting lower than normal activation of stimuli semantically related to the preceding category names; they also found smaller (i.e., less negative) N400s to non-exemplars, indicating higher than normal activation of unrelated items. The second aspect of the contextual deficit hypothesis is that schizophrenic patients might be less able to utilise semantic information
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from the previous encoding phase to modify the latency of their responses to repeated stimuli (Guillem et al., 2001; Jeong & Kubicki, 2010; Matsuoka et al., 1999). For example, the schizophrenic patients tested by Matsuoka and colleagues (1999) did not show significant changes in the amplitude of the N400s associated with repeated words in a semantic categorisation task. Taken together, these two lines of evidence have striking consequences for the interpretation of the results of our second experiment. For healthy controls, the initial presentation of the critical exemplars during the encoding phase increased the activation of the corresponding semantic representations. Then, when the exemplars were re-presented in the category verification task, the combined effects of semantic relatedness and stimulus repetition led to a substantial saving of processing resources, which revealed itself as a shortening of decision times to previously processed exemplars (as compared to new exemplars). On the other hand, in schizophrenic patients both the effects of semantic relatedness and stimulus repetition were loosened, resulting in a non-significant shortening of decision times to old exemplars. Conclusions and limitations To summarise, the present two experiments (1) confirmed that schizophrenic patients have intact priming in the perceptually driven implicit task of lexical decision (Sponheim et al., 2004), and (2) extended to the identification task of category verification previous evidence suggesting that schizophrenia involves a deficit in conceptual implicit memory (Ruiz et al., 2007; Soler et al., 2007). At the same, there are a number of potential limitations that must be taken into account. First, we compared perceptual and conceptual implicit tasks across different samples of schizophrenic patients and healthy controls, whereas the best way to prove dissociations between tasks/processes is to compare different tasks under the same experimental conditions using the same participants (Schacter, Bowers, & Booker, 1989). Related to this problem, the schizophrenic patients in our Experiment 2 (category verification) were slightly less educated than those in Experiment 1 (lexical decision). However, there was no hint that priming scores in the lexical decision and category verification tasks were correlated with the participants’ number of years of education. A second limitation is that we did not employ a post-test questionnaire to assess the awareness and/or the retrieval intentionality of our participants (Mulligan & Peterson, 2008). When using identification tasks based on RTs, the potential for retrieval intentionality is severely limited because the to-be-remembered stimuli are re-presented during the test phase and the decisions are speeded (Perfect, Moulin, Conway, & Perry, 2002). However, the possibility for participants to become aware of the repetition of the studies words in the retrieval phase remains (Mulligan & Peterson, 2008). Test awareness might have contaminated the results, by inflating the performance of healthy controls in the category verification task. Although we cannot rule out this possibility, it should be noted that in the study by Mulligan and Peterson (2008), the results never changed when aware participants were eliminated from analyses. Lastly, our encoding task (read aloud visually presented words) might have favoured the analysis of the perceptual properties of the stimuli, to the detriment of conceptual priming. In many previous studies, the dissociation between perceptual and conceptual priming has been successfully obtained using the same procedure (e.g., Gabrieli et al., 1999). Indeed, the fact that significant priming obtained in the category verification task suggests that at least part of the semantic information associated with the encoded words
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was activated during the encoding phase. Nonetheless, it remains to be determined whether schizophrenic patients show the same conceptual priming deficit after a deep encoding task (Ragland et al., 2003). Funding This study was supported by a grant from Sapienza University awarded to C. Rossi-Arnaud (Ateneo 2011; project n. C26A11RESK).
References Aleman, A., Hijman, R., de Haan, E., & Kahn, R. (1999). Memory impairment in schizophrenia: A meta-analysis. The American Journal of Psychiatry, 156, 1358–1366. Boccardi, M., & Cappa, S. F. (1997). Valori normativi di produzione categoriale per la lingua italiana. [Normative values of categorical production for the Italian language]. Giornale Italiano Di Psicologia, 24, 425–436. Clare, L., McKenna, P. J., Mortimer, A. M., & Baddeley, A. D. (1993). Memory in schizophrenia: What is impaired and what is preserved? Neuropsychologia, 31, 1225–1241. doi:10.1016/00283932(93)90070-G Cohen, J. D., & Servan-Schreiber, D. (1992). Context, cortex and dopamine: A connectionist approach to behavior and biology in schizophrenia. Psychological Review, 99, 45–77. doi:10.1037/0033-295X.99.1.45 Forbes, N., Carrick, L., McIntosh, A., & Lawrie, S. (2009). Working memory in schizophrenia: A meta-analysis. Psychological Medicine, 39, 889–905. doi:10.1017/S0033291708004558 Franks, J. J., Bilbrey, C. W., Guat L. K., & McNamara, T. P. (2000). Transfer-appropriate processing (TAP). Memory and Cognition, 28, 1140–1151. doi:10.3758/BF03211815 Gabrieli, J. D. E., Vaidya, C. J., Stone, M., Francis W. S., Thompson-Schill, S. L., Fleischman, D. A., … Wilson, R. S. (1999). Convergent behavioral and neuropsychological evidence for a distinction between identification and production forms of repetition priming. Journal of Experimental Psychology: General, 128, 479–498. doi:10.1037/0096-3445.128.4.479 Guillem, F., Bicu, M., Hooper, R., Bloom, D., Wolf, M. A., Messier, J., … Debruille, J. (2001). Memory impairment in schizophrenia: A study using event-related potentials in implicit and explicit tasks. Psychiatry Research, 104, 157–173. doi:10.1016/S0165-1781(01)00305-5 Henson, R. A., & Rugg, M. D. (2003). Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia, 41, 263–270. doi:10.1016/S0028-3932(02) 00159-8 Jeong, B., & Kubicki, M. (2010). Reduced task-related suppression during semantic repetition priming in schizophrenia. Psychiatry Research, 181, 114–120. doi:10.1016/j.pscychresns.2009. 09.005 Kay, S. R., Opler, L. A., & Lindenmayer, J. (1988). Reliability and validity of the positive and negative syndrome scale for schizophrenics. Psychiatry Research, 23, 99–110. doi:10.1016/ 0165-1781(88)90038-8 Kazes, M., Berthet, L., Danion, J. M., Amado, I., Willard, D., Robert, P., & Poirier, M. F. (1999). Impairment of consciously controlled use of memory in schizophrenia. Neuropsychology, 13, 54– 61. doi:10.1037/0894-4105.13.1.54 Kern, R., Hartzell, A., Izaguirre, B., & Hamilton, A. (2010). Declarative and nondeclarative memory in schizophrenia: What is impaired? What is spared? Journal of Clinical and Experimental Neuropsychology, 32, 1017–1027. doi:10.1080/13803391003671166 Kiang, M., & Kutas, M. (2005). Association of schizotypy with semantic processing differences: An event-related potential brain study. Schizophrenia Research, 77, 329–342. doi:10.1016/j. schres.2005.03.021 Light, L. L., Prull, M. W., & Kennison, R. F. (2000). Divided attention, aging, and priming in exemplar generation and category verification. Memory & Cognition, 28, 856–872. doi:10.3758/ BF03198421 Matsuoka, H., Matsumoto, K., Yamazaki, H., Sakai, H., Miwa, S., Yoshida, S., … Sato, M. (1999). Lack of repetition priming effect on visual event-related potentials in schizophrenia. Biological Psychiatry, 46, 137–140. doi:10.1016/S0006-3223(98)00330-8
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Mulligan, N. W. (2008). Implicit memory. London: Psychology Press. Mulligan, N. W., & Besken, M. (2011). Implicit memory. In D. Reisberg (Ed.), Oxford handbook of cognitive psychology (pp. 220–231). Oxford: Oxford University Press. Mulligan, N. W., & Peterson, D. (2008). Attention and implicit memory in the category verification and lexical decision tasks. Journal of Experimental Psychology: Learning, Memory and Cognition, 34, 662–679. doi:10.1037/0278-7393.34.3.662 Perfect, T. J., Moulin, C. J. A., Conway, M. A., & Perry, E. (2002). Assessing the inhibitory account of retrieval-induced forgetting with implicit-memory tests. Journal of Experimental Psychology: Learning, Memory, and Cognition, 28, 1111–1119. doi:10.1037/0278-7393.28.6.1111 Perry, W., Light, G. A., Davis, H., & Braff, D. L. (2000). Schizophrenia patients demonstrate a dissociation on declarative and non-declarative memory tests. Schizophrenia Research, 46, 167– 174. doi:10.1016/S0920-9964(99)00229-7 Prull, M. W. (2004). Exploring the identification-production hypothesis of repetition priming in young and older adults. Psychology and Aging, 19, 108–124. doi:10.1037/0882-7974.19.1.108 Ragland, J. D., Moelter, S. T., McGrath, C., Hill, S. K., Gur, R. E., Bilker, W. B., … Gur, R. C. (2003). Levels-of-processing effect on word recognition in schizophrenia. Biological Psychiatry, 54, 1154–1161. doi:10.1016/S0006-3223(03)00235-X Randolph, C., Gold, J. M., Carpenter, C. J., Goldberg, T. E., & Weinberger, D. R. (1993). Implicit memory in patients with schizophrenia and normal controls: Effects of task demands on susceptibility to priming. Journal of Clinical and Experimental Neuropsychology, 15, 853–866. doi:10.1080/01688639308402603 Rossell, S. L., & David, A. S. (2006). Are deficits in schizophrenia due to problems with access or storage? Schizophrenia Research, 82, 121–134. doi:10.1016/j.schres.2005.11.001 Ruiz, J., Soler, M., Fuentes, I., & Tomás, P. (2007). Intellectual functioning and memory deficits in schizophrenia. Comprehensive Psychiatry, 48, 276–282. doi:10.1016/j.comppsych.2006.11.002 Schacter, D. L., Bowers, J., & Booker, J. (1989). Intention, awareness, and implicit memory: The retrieval intentionality criterion. In S. Lewandowsky, J. C. Dunn, & K. Kirsner (Eds.), Implicit memory: Theoretical issues (pp. 47–65). Hillsdale, NJ: Lawrence Erlbaum. Schwartz, B., Rosse, R., & Deutsch, S. (1993). Limits of the processing view in accounting for dissociations among memory measures in a clinical population. Memory & Cognition, 21, 63–72. doi:10.3758/BF03211165 Soler, M. J., Ruiz, J. C., Fuentes, I., & Tomás, P. (2007). A comparison of implicit memory tests in schizophrenic patients and normal controls. The Spanish Journal of Psychology, 10, 423–429. doi:10.1017/S1138741600006685 Soler, M., Ruiz, J., Vargas, M., Dasi, C., & Fuentes, I. (2011). Perceptual priming in schizophrenia evaluated by word fragment and word stem completion. Psychiatry Research, 190, 167–171. doi:10.1016/j.psychres.2011.08.008 Spataro, P., Cestari, V., & Rossi-Arnaud, C. (2011). The relationship between divided attention and implicit memory: A meta-analysis. Acta Psychologica, 136, 329–339. doi:10.1016/j.actpsy.2010. 12.007 Spataro, P., Longobardi, E., Saraulli, D., & Rossi-Arnaud, C. (2013). Interactive effects of age-ofacquisition and repetition priming in the lexical decision task: A multiple loci account. Experimental Psychology, 19, 1–8. doi:10.1027/1618-3169/a000192 Spataro, P., Mulligan, N., & Rossi-Arnaud, C. (2010). Effects of divided attention in the wordfragment completion task with unique and multiple solutions. European Journal of Cognitive Psychology, 22, 18–45. doi:10.1080/09541440802685979 Sponheim, S., Steele, V., & McGuire, K. (2004). Verbal memory processes in schizophrenia patients and biological relatives of schizophrenia patients: Intact implicit memory impaired explicit recollection. Schizophrenia Research, 71, 339–348. doi:10.1016/j.schres.2004.04.008 Stone, W., & Hsi, X. (2011). Declarative memory deficits and schizophrenia: Problems and prospects. Neurobiology of Learning and Memory, 96, 544–552. doi:10.1016/j.nlm.2011.04.006 Vaidya, C. J., Gabrieli, J. D. E., Keane, M. M., Monti, L. A., Gutierrez-Rivas, H., & Zarella, M. M. (1997). Evidence for multiple mechanisms of conceptual priming on implicit memory tests. Journal of Experimental Psychology: Learning, Memory, and Cognition, 23, 1324–1343. doi:10.1037/0278-7393.23.6.1324
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Is conceptual implicit memory impaired in schizophrenia? Evidence from lexical decision and category verification Valéria R.S. Marquesa,b, Pietro Spataroa, Vincenzo Cestaria,c, Antonio Sciarrettad, Francesca Iannarellia and Clelia Rossi-Arnauda* a
Department of Psychology, Sapienza University of Rome, Via dei Marsi 78, 00185 Rome, Italy; CAPES Foundation, Ministry of Education of Brazil, Setor Bancário Norte, Quadra 2, Bloco L, Lote 06, CEP 70040-020 - Brasília, DF, Brazil; cCell Biology and Neurobiology Institute, C.N.R National Research Council of Italy, Via del Fosso di Fiorano 64/65, 00143 Rome, Italy; dAcute Psychiatric Care Unit, Department of Mental Health RM-G, San Giovanni Evangelista Hospital, Via Antonio Parrozzani 3, 00019 Tivoli, Italy
b
(Received 20 February 2014; accepted 15 August 2014) Introduction. Implicit memory tasks differ along two orthogonal dimensions, tapping the relative involvement of perceptual/conceptual and identification/production processes. Previous studies have documented a dissociation between perceptual (spared) and conceptual (impaired) implicit memory, using in the latter case a production task (category exemplar generation), in which there is high response competition during the retrieval phase. The present study sought to determine whether the perceptual/ conceptual dissociation held when comparing two identification tasks, in which there is no response competition at retrieval. Methods. In two experiments, repetition priming was assessed in 44 schizophrenic patients and 46 healthy controls in lexical decision (a test based on perceptual identification processes) and category verification (a test based on conceptual identification processes). Results. Schizophrenic patients achieved a priming as high as that of controls in the lexical decision task. In contrast, only controls exhibited significant priming in the category verification task. Conclusions. It is concluded that schizophrenia is associated with a specific deficit in conceptual implicit memory, irrespective of the degree of response competition in the test phase. Keywords: implicit memory; repetition priming; conceptual priming; schizophrenia
Memory impairment represents one of the most essential neurocognitive features of schizophrenia (Stone & Hsi, 2011). Significant deficits have been reported in episodic memory (Aleman, Hijman, de Haan, & Kahn, 1999), as well as in verbal and visuospatial working memory (Forbes, Carrick, McIntosh, & Lawrie, 2009). However, the extent to which this impairment generalises to implicit memory is less well understood. Implicit memory refers to the unintentional retrieval of information encoded during the study phase and is typically investigated through repetition priming tasks, in which memory is demonstrated by changes in the speed and/or accuracy in the processing of previously experienced stimuli, relative to an appropriate baseline (Mulligan & Besken, *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
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2011). For instance, in word-fragment completion, participants are presented with words at encoding (e.g., scissor) and are later asked to complete unique-solution fragments (e.g., s _ _ ss _ r) with the first words that come to mind. Repetition priming is indicated by higher completion rates for fragments corresponding to previously processed (old) words than for fragments corresponding to previously unprocessed (new) words (Spataro, Mulligan, & Rossi-Arnaud, 2010). Following the Transfer-Appropriate-Processing theory (Franks, Bilbrey, Guat Lien, & McNamara, 2000), a broad distinction has been drawn between perceptually driven implicit tests (e.g., lexical decision), that rely on perceptual processes, and conceptually driven implicit tests (e.g., category exemplar generation), that rely on semantic processes based on the analysis of meaning. Priming in perceptual implicit tasks is reduced following study-test changes in the modality of stimulus presentation (from visual to auditory or vice versa), whereas it is substantially unaffected by semantic versus nonsemantic encoding and by divided attention in the study phase; priming in conceptual tasks, on the other hand, show the opposite pattern of results – it is enhanced by semantic encoding, reduced by divided attention and unaffected by modality changes (Mulligan, 2008; Spataro, Cestari, & Rossi-Arnaud, 2011). Despite its success in explaining a wide range of behavioural and neuropsychological findings, the perceptual/conceptual distinction has been challenged by a series of results first reported by Vaidya et al. (1997) and Gabrieli et al. (1999); see also Prull (2004). Vaidya et al. (1997) found that conceptual elaboration in the study phase enhanced repetition priming in word association (only for weakly associated words) and category exemplar generation, but had no effect on category verification and abstract/concrete classification. A later study by Gabrieli et al. (1999) showed that Alzheimer’s disease patients had impaired priming in word-stem completion and category exemplar generation but intact priming in picture naming and category verification; moreover, in young adults, the same pattern of results was obtained by dividing attention during the encoding phase, which reduced repetition priming in word-stem completion and category exemplar generation, but not in picture naming and category verification. To account for these findings, the authors proposed that perceptual and conceptual implicit tasks can be dissociated in two subclasses, on the basis of the presence or the absence of competition among alternative responses during the retrieval phase. Identification tests such as lexical decision or category verification are those in which the retrieval cues directly guide participants towards unique solutions (low-response competition). For instance, when participants in a lexical decision task are presented with the word judge (or the non-word ludge) and instructed to decide as rapidly as possible whether each item represents a legal word or a non-word, the identification of the stimulus is sufficient to determine the unique correct response (word or non-word). In contrast, production tasks such as wordstem completion or category exemplar generation are those in which the retrieval cues admit multiple legitimate solutions (high-response competition). For example, when participants are presented with a word-stem like pre__ and told to produce the first word that comes to mind, they can choice between multiple correct responses, including premise, present, pressure, preview and prejudice. According to Vaidya et al. (1997) and Gabrieli et al. (1999), the achievement of full priming (i.e., greater-than-zero) would require the allocation of a greater amount of study-phase attentional resources in production than in identification tasks. This is because only in production tests the target stimuli must be selected among numerous competing solutions: in such a circumstance, the retrieval of the encoded items depends on some external assistance,
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such as study-phase elaboration. On the other hand, identification tasks lack response competition because the to-be-remembered stimuli are provided during the test phase: in such a circumstance, any study-phase retrieval of the items in response to an encoding task results in significant priming, and semantic elaboration does not add anything to this direct priming (Gabrieli et al., 1999; Vaidya et al., 1997). When considered in light of the earlier two distinctions, the results of previous studies examining implicit memory in schizophrenia are mixed. Overall, there is good evidence indicating that perceptual identification tasks are spared in schizophrenic patients, since they have been reported to achieve levels of repetition priming comparable to those of healthy controls in lexical decision (Sponheim, Steele, & McGuire, 2004), perceptual identification (Schwartz, Rosse, & Deutsch, 1993) and word-fragment completion with unique solutions (Ruiz, Soler, Fuentes, & Tomás, 2007; Soler, Ruiz, Vargas, Daśi, & Fuentes, 2011). On the other hand, data concerning the perceptual production task of word-stem completion are equivocal, with studies showing both impaired priming (Kern, Hartzell, Izaguirre, & Hamilton, 2010; Randolph, Gold, Carpenter, Goldberg, & Weinberger, 1993) and intact priming (Clare, McKenna, Mortimer, & Baddeley, 1993; Kazes et al., 1999; Perry, Light, Davis, & Braff, 2000). With regard to conceptual implicit memory, available findings indicate that schizophrenic patients obtain lower levels of repetition priming in the production task of category exemplar generation (Ruiz et al., 2007; Soler, Ruiz, Fuentes, & Tomás, 2007; but see Schwartz et al., 1993). To our knowledge, the performance of this clinical population has not been previously examined in the conceptual identification task of category verification (Mulligan & Peterson, 2008), although Rossell and David (2006) found that schizophrenics were significantly less accurate than controls in deciding whether a given exemplar belonged to a category or not. However, no encoding phase was included in the latter study, implying that the exemplars were not primed. In the present study, we sought to ascertain whether schizophrenic patients show a dissociation between perceptual and conceptual implicit memory, when both tasks are based on identification processes and therefore do not involve response competition. As briefly reviewed earlier, evidence in support of a deficit in conceptual implicit memory in schizophrenia primarily comes from reduced repetition priming in category exemplar generation (Ruiz et al., 2007; Soler et al., 2007), a task which is heavily based on production processes (Gabrieli et al., 1999). This suggests the alternative possibility that the impairment in schizophrenic patients might not be caused by the conceptual nature of the category exemplar generation task, but rather by the necessity to select the encoded items among multiple competitors at the time of retrieval (i.e., by the production nature of the task). The latter proposal is supported by the fact that the only other implicit test in which SC patients have been found to perform worse than healthy controls is word-stem completion (Kern et al., 2010; Randolph et al., 1993; but see Clare et al., 1993, Kazes et al., 1999 and Perry et al., 2000, for different results), which is also classified as a production task (Gabrieli et al., 1999). To ascertain whether the perceptual/conceptual distinction held also when using two non-competitive identification tests, we compared repetition priming in schizophrenic patients and age-matched healthy controls in lexical decision (a perceptual identification task) and category verification (a conceptual identification task). Experiment 1 Experiment 1 aimed at confirming previous evidence indicating that schizophrenic patients exhibit intact repetition priming in the lexical decision task (Sponheim et al., 2004).
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Method Participants Twenty-two schizophrenic patients (11 females) and 24 healthy controls (15 females) participated in Experiment 1. There were no differences between the two groups in terms of age, M(schizophrenics) = 43.6 vs. M(controls) = 38.2, t(44) = 1.26, p = .21, and the ratio of males to females, χ(1)2 = 1.02, p = .31. However, healthy controls had a higher number of years of formal education, compared to schizophrenic patients, M(schizophrenics) = 14.0 vs. M(controls) = 16.1, t(44) = −2.01, p = .05. As a consequence, the latter variable was included as a covariate in the following statistical analyses. Patients were recruited from the Acute Psychiatric Care Unit of the “San Giovanni Evangelista” Hospital (Tivoli, Italy), after approval from the local Research Ethics Board. All of them met the standard diagnostic criteria for schizophrenia, as determined by the Structured Clinical Interview of Diagnostic and Statistical Manual of Mental Disorders (DSM-IV, 4th ed., American Psychiatric Association, 1994), medical history and the joint consensus of the senior psychiatrists of the research team. Exclusion criteria were as follows: no history of substance abuse, traumatic brain injury, epilepsy or other adverse neurological conditions. Schizophrenic patients were stabilised by at least one week at the time of testing and treated with antipsychotic neuroleptics at clinically determined dosages – atypical only: N = 13; typical only: N = 6; both: N = 3. The mean daily oral dose was 538 chlorpromazine equivalents. Symptom severity indexes, as assessed with the Positive and Negative Syndrome Scale for Schizophrenia (PANSS: Kay, Opler, & Lindenmayer, 1988), were 17.35 (positive scale), 22.64 (negative scale) and 35.42 (general psychopathology). Control participants were recruited from a variety of sources, including university employees, hospital staff and random search from people attending a community centre near the Hospital “San Giovanni Evangelista” (Tivoli, Rome). All of them denied a history of psychiatric disorders or other neuropsychological diseases, including alcohol and substance abuse. Written informed consent was obtained from all participants, after a brief explanation of the study procedures. Materials They were represented by 30 critical words selected from the LexVar database (http:// www.istc.cnr.it/it/grouppage/lexvar), and previously employed by Spataro, Longobardi, Saraulli, and Rossi-Arnaud (2013). This original set was divided in two lists of 15 words each (A–B), matched as closely as possible for length in letters (M = 7.60–7.73), written frequency (M = 74.47–79.33; taken from the CoLFIS vocabulary: http://www.istc.cnr.it/ grouppage/colfis), familiarity (M = 6.01–6.13), imageability (M = 5.42–5.22) and concreteness (M = 6.08–5.88). Twenty non-critical words, with similar properties, were also selected from the earlier database, to be used as practice items. Finally, 35 legal pronounceable non-words were created for the purposes of test, by randomly changing one letter into real words (see Spataro et al., 2013, for examples). Procedure During the encoding phase, participants were presented with a total of 40 items, including 15 critical words, 15 filler words and 10 practice words. Each trial comprised a fixation point for 1,000 ms, a word for 2,000 ms and a pause for 1,500 ms. All words appeared centrally on the computer screen and were displayed in white against a black background. Half of the participants were presented with the words of List A, whereas the words of
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List B were used only during the test phase to compute the baseline reaction times; for the other half of the sample, the assignment of the lists was reversed. Participants were simply instructed to read the words aloud (to ensure correct identification: Mulligan & Peterson, 2008). Learning was incidental, since participants were not told to remember the words. After a brief interval (2–3 minutes of free-flowing conversation), the lexical decision task was administered. Participants were presented with a total of 70 items, including 30 critical words (15 old and 15 new), 30 legal pronounceable non-words and 10 practice words (five words and five non-words). Each trial comprised: (1) a fixation point for 1,000 ms; (2) a test item (either a word or a non-word), which remained on the screen until participants’ response and (3) a pause for 1,500 ms. The instructions were to decide as rapidly and accurately as possible whether each letter string represented a real Italian word or a non-word, by pressing two different keys of a response pad (RB-834 Model, Cedrus Corporation TM). No mention was made about the relationship with the encoding phase. Results Errors and reaction times (RTs) >2.5 SD from the overall mean of each participant were excluded (2.2% of the data). Only the RTs to “word” responses were taken into account in the primary analysis (Mulligan & Peterson, 2008). A 2 (item type: old vs. new words) × 2 (group: schizophrenics vs. controls) analysis of covariance (ANCOVA), considering item type as a within-subjects variable, group as a between-subjects variable and the number of years of education as a covariate, revealed: (1) a significant main effect of item type, F(1, 43) = 5.08, MSE = 10,847, p < .05, indicating that lexical decisions were faster to old than new words, M = 1,104 vs. M = 1,172 ms; and (2) a significant main effect of group, F(1, 43) = 6.51, MSE = 388,273, p ≤ .01, indicating that the responses of schizophrenic patients were slower than those of healthy controls, M = 1,311 vs. M = 965 ms. However, the interaction between item type and group did not reach the significance level, F(1, 43) = 0.36, MSE = 10,847, suggesting that the two groups exhibited comparable effects of item type. In agreement, a series of independent t-tests showed that repetition priming, computed as the difference between the RTs to new words minus the RTs to old words, shortened lexical decision latencies to the same extent in healthy controls and schizophrenic patients, M = 45 vs. M = 93 ms, t (44) = 1.09, p = .28 (see Figure 1), and that both priming scores were significantly >0, t
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Figure 1. Experiment 1: Mean reaction times in the lexical decision task, as a function of item type (old vs. new exemplars) and group (schizophrenics vs. controls). Bars represent standard errors.
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(23) = 3.25, p < .01and t(21) = 2.13, p < .05, respectively. No significant correlations were found between repetition priming and the PANSS scores of schizophrenic patients: −0.29 < r(22) < 0.09, p > .24. Priming was also uncorrelated with the participants’ years of education, r(46) = −0.14, p = .36. The same ANCOVA as mentioned earlier found that accuracy (i.e., the percentages of correct “word” responses) did not vary as a function of item type, M(old) = 98% vs. M(new) = 97%, F(1, 43) = 0.01, MSE = 0.001, or group, M(schizophrenics) = 98% vs. M(controls) = 97%, F(1, 43) = 0.60, MSE = 0.003. Moreover, the two variables did not interact, F(1, 43) = 0.66, MSE = 0.001. In summary, Experiment 1 showed that, in a lexical decision task, schizophrenic patients benefited from repetition priming to the same extent as healthy controls. Such a finding replicates the results reported by Sponheim et al. (2004) and, more generally, is in line with the hypothesis that perceptual implicit memory is intact in schizophrenia (Ruiz et al., 2007; Soler et al., 2007).
Experiment 2 Experiment 2 extended our investigation to a conceptual implicit task based on identification processes, namely, category verification (Mulligan & Peterson, 2008). The latter task does not meet the standard requirements of a conceptual implicit task – as indicated by non-significant effects of levels-of-processing and divided attention in the study phase (Gabrieli et al., 1999; Vaidya et al., 1997). However, there is no doubt that it is based on the retrieval of semantic representations because the repetition of encoded exemplars produces strong deactivations in the left prefrontal areas typically involved in the processing of conceptual information (Henson & Rugg, 2003) and priming is not reduced by changes in presentation modality between the study and test phases (Light, Prull, & Kennison, 2000; Vaidya et al., 1997). Method Participants A different sample of 22 schizophrenic patients (9 females) and 22 controls (14 females) participated in Experiment 2. There were no differences between the two groups in terms of age, M(schizophrenics) = 37.2 vs. M(controls) = 38.4, t(44) = −0.27, p = .79, and the ratio of males to females, χ(1)2 = 2.28, p = .13. However, healthy controls reported a higher number of years of formal education, M = 11.50 vs. M = 15.14 years, t(42) = −3.85, p < .001. Because of this difference, the latter variable was included as a covariate in the following statistical analyses. Schizophrenic patients and control participants were recruited following the same general strategy and exclusion criteria described in Experiment 1. Of the schizophrenic patients, 12 were treated with atypical neuroleptics and 10 with typical neuroleptics. The mean daily oral dose was 526 chlorpromazine equivalents. PANSS symptom severity indexes were 17.11 (positive scale), 22.50 (negative scale) and 35.06 (general psychopathology scale). Materials Ninety-six critical words (8 exemplars from 12 categories), from 5 to 11 letters in length, were selected from the category production database compiled by Boccardi and Cappa
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(1997). Such a database reports, in descending order of taxonomic frequency, all the exemplars spontaneously produced by 200 Italian university students in response to a category name. The items chosen for the present experiment did not rank in the five most frequent instances. The critical exemplars were divided into two study lists of 48 items (4 instances from each of the 12 categories), which were counterbalanced across the old and new conditions. The two lists were equated as closely as possible for taxonomic frequency (M = 33.58–36.04) and written frequency (M = 15.50–15.53; taken from the CoLFIS Vocabulary). Each study list was further divided into half, to counterbalance the assignment of the old exemplars to the “yes” and “no” responses. An additional set of 12 exemplars were selected from the same database (four instances from three categories), to be used as practice items during the test phase. Procedure At encoding, 48 critical exemplars were presented individually in the middle of the computer screen. They were shown in white against a black background. Each trial comprised a fixation point for 1,000 ms, a word for 2,000 ms and a pause for 1,500 ms. The general procedure and the instructions were similar to those illustrated in Experiment 1: participants were again asked to read each word aloud, to secure correct identification (Mulligan & Peterson, 2008). Words in the study blocks were randomly ordered subject to the constraint that no more than two exemplars from the same category could appear in a row. After a brief interval (2–3 minutes of free-flowing conversation), the category verification task was administered. Participants were presented with a total of 96 category exemplar pairs, including 48 old exemplars (24 requiring a “yes” response and 24 requiring a “no” response) and 48 new exemplars (again, 24 requiring a “yes” response and 24 requiring a “no” response). Each trial began with a fixation point for 1,000 ms. Then, a category name (e.g., FRUIT) was presented in uppercase letters about 2 cm above the fixation point, for 2,000 ms. Whereas the category name remained visible on the screen, an exemplar (which could be congruent or incongruent with the cued category: pineapple vs. leopard) was presented in lowercase letters about 2 cm below the fixation point, until the participants’ response. A pause of 1,500 ms was interposed between two subsequent trials. Participants were instructed to decide, as rapidly and accurately as possible, whether each exemplar belonged or not to the associated category, by pressing two different keys of a response pad (RB-834 Model, Cedrus Corporation TM). No mention was made about the relationship with the study phase. Results Errors and RTs >2.5 SD from the overall mean of each participant were excluded (2.6% of the data). Only the RTs corresponding to “yes” responses were taken into account in the primary analysis (Mulligan & Peterson, 2008). A 2 (item type: old vs. new exemplars) × 2 (group: schizophrenics vs. controls) ANCOVA, considering item type as a within-subjects variable, group as a betweensubjects variable and number of years of education as a covariate, revealed: (1) a significant main effect of item type, F(1, 41) = 8.05, MSE = 3,186, p < .01, indicating that semantic decisions were faster to old than to new exemplars, M = 1,206 vs. M = 1,258 ms; (2) a significant main effect of group, F(1, 41) = 4.55, MSE = 291,754,
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Old words
Figure 2. Experiment 2: Mean reaction times in the category verification task, as a function of item type (old vs. new exemplars) and group (schizophrenics vs. controls). Bars represent standard errors.
p < .05, indicating that schizophrenic patients responded more slowly than healthy controls, M = 1,375 vs. M = 1,089 ms; and (3) a significant interaction between item type and group, F(1, 41) = 8.25, MSE = 3,186, p < .01. A follow-up analysis of simple effects, using the Bonferroni adjustment for multiple comparisons showed that the effect of item type was significant for healthy controls, F(1, 41) = 24.89, p < .001, but not for schizophrenic patients, F(1, 41) = 0.40, p = .53. As illustrated in Figure 2, this interaction indicates that repetition priming, computed as the difference between the RTs to new exemplars minus the RTs to old exemplars, was significantly >0 for healthy controls, M = 78 ms, t(21) = 5.62, p < .001, whereas it did not differ from null priming for schizophrenic patients, M = 25 ms, t(21) = 1.24, p = .23. No significant correlations were found between repetition priming and the PANSS scores of schizophrenic patients: r(22) < 0.23, p > .37. Like in Experiment 1, priming scores were not significantly correlated with the participants’ number of education years: r(44) = 0.12, p = .37. A 2 (item type: old vs. new) × 2 (Group: schizophrenics vs. controls) ANCOVA was also applied to accuracy data (i.e., the percentages of correct “yes” responses). However, this analysis found neither significant main effects – for item type: M(old) = 95% vs. M(new) = 94%, F(1, 41) = 0.61, MSE = 0.002; for group: M(schizophrenics) = 94% vs. M(controls) = 96%, F(1, 41) = 0.33, MSE = 0.007 – nor a two-way interaction between item type and group, F(1, 41) = 0.764, MSE = 0.002. In summary, Experiment 2 extended to a semantic identification task previous findings indicating that conceptually driven implicit memory is significantly impaired in schizophrenia (Ruiz et al., 2007; Soler et al., 2007). On the other hand, we did not replicate the finding that schizophrenic patients are less accurate than controls in making semantic decisions to category exemplar pairs (Rossell & David, 2006). This incongruence might be ascribed to methodological differences: in particular, in the study by Rossell and David (2006), the exemplars were presented for 200 ms, whereas in our experiment, they remained visible until the participant’s response. Discussion The present two experiments sought to establish whether schizophrenic patients showed a dissociation between perceptual and conceptual implicit memory, when both types of memory were measured with tasks based on identification processes and therefore did not
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involve competition between multiple solutions at the time of test (Gabrieli et al., 1999; Vaidya et al., 1997). As mentioned in the Introduction, Ruiz et al. (2007) and Soler et al. (2007) found that repetition priming in schizophrenic patients was comparable to that of healthy controls in the word-fragment completion task, but significantly reduced in the category exemplar generation task. These findings suggest that schizophrenia may be associated with a specific deficit in conceptually driven implicit memory. However, besides the perceptual/ conceptual distinction, the aforementioned tasks also differ in the involvement of identification/production processes. Word-fragment completion is primarily based on identification processes because in most studies (including those by Ruiz et al., 2007, and Soler et al., 2007), the to-be-solved fragments have unique solutions, implying small or no competition during the retrieval phase (Spataro et al., 2010). In contrast, the category generation task is heavily based on production processes (Gabrieli et al., 1999; Vaidya et al., 1997) because participants are instructed to produce the first instances that come to mind in response to a category label: in these conditions, the encoded exemplars must be selected among multiple competing responses. Because of this critical difference, it was deemed important to ascertain whether schizophrenic patients continue to show a dissociation between perceptual and conceptual implicit memory when the tasks are based on non-competitive identification processes. The data obtained in the present experiments provide a clear answer to the above question. Schizophrenic patients and healthy controls reached comparable levels of repetition priming in the perceptual identification task of lexical decision. In contrast, only controls achieved reliable (i.e., non-zero) priming in the conceptual identification task of category verification; schizophrenic patients did not show any facilitation in this test. Therefore, our results extend previous findings showing that schizophrenic patients have reduced priming in the category exemplar generation task (Ruiz et al., 2007; Soler et al., 2007). Furthermore, they suggest that the dissociations between perceptual and conceptual memory observed in these studies were not confounded by the productive nature of category exemplar generation; rather, they reflected a specific deficit in the use of conceptually driven implicit processes, which is independent of the degree of response competition during the retrieval phase. The absence of significant priming in the category verification task raises the question of what mechanisms are impaired in the semantic memory of schizophrenic patients. One plausible explanation for our data is that schizophrenia is associated with an impairment in the ability to use contextual information for biasing conceptual decisions (Cohen & Servan-Schreiber, 1992). Such a hypothesis has two different, but related, implications. The first is that, during the test phase of the category verification task, schizophrenic patients might be less efficient in exploiting the category names to activate related exemplars and inhibit unrelated exemplars. Kiang and Kutas (2005) recorded the N400 component of event-related brain potentials from healthy adults during an unprimed category verification task. The N400 is a well-known negativity whose amplitude is reduced (i.e., less negative) after presentation of a target stimulus conceptually related to a prime. Kiang and Kutas (2005) found that individuals high in schizotypy showed larger (i.e., more negative) N400s to both high- and low-typicality exemplars, suggesting lower than normal activation of stimuli semantically related to the preceding category names; they also found smaller (i.e., less negative) N400s to non-exemplars, indicating higher than normal activation of unrelated items. The second aspect of the contextual deficit hypothesis is that schizophrenic patients might be less able to utilise semantic information
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from the previous encoding phase to modify the latency of their responses to repeated stimuli (Guillem et al., 2001; Jeong & Kubicki, 2010; Matsuoka et al., 1999). For example, the schizophrenic patients tested by Matsuoka and colleagues (1999) did not show significant changes in the amplitude of the N400s associated with repeated words in a semantic categorisation task. Taken together, these two lines of evidence have striking consequences for the interpretation of the results of our second experiment. For healthy controls, the initial presentation of the critical exemplars during the encoding phase increased the activation of the corresponding semantic representations. Then, when the exemplars were re-presented in the category verification task, the combined effects of semantic relatedness and stimulus repetition led to a substantial saving of processing resources, which revealed itself as a shortening of decision times to previously processed exemplars (as compared to new exemplars). On the other hand, in schizophrenic patients both the effects of semantic relatedness and stimulus repetition were loosened, resulting in a non-significant shortening of decision times to old exemplars. Conclusions and limitations To summarise, the present two experiments (1) confirmed that schizophrenic patients have intact priming in the perceptually driven implicit task of lexical decision (Sponheim et al., 2004), and (2) extended to the identification task of category verification previous evidence suggesting that schizophrenia involves a deficit in conceptual implicit memory (Ruiz et al., 2007; Soler et al., 2007). At the same, there are a number of potential limitations that must be taken into account. First, we compared perceptual and conceptual implicit tasks across different samples of schizophrenic patients and healthy controls, whereas the best way to prove dissociations between tasks/processes is to compare different tasks under the same experimental conditions using the same participants (Schacter, Bowers, & Booker, 1989). Related to this problem, the schizophrenic patients in our Experiment 2 (category verification) were slightly less educated than those in Experiment 1 (lexical decision). However, there was no hint that priming scores in the lexical decision and category verification tasks were correlated with the participants’ number of years of education. A second limitation is that we did not employ a post-test questionnaire to assess the awareness and/or the retrieval intentionality of our participants (Mulligan & Peterson, 2008). When using identification tasks based on RTs, the potential for retrieval intentionality is severely limited because the to-be-remembered stimuli are re-presented during the test phase and the decisions are speeded (Perfect, Moulin, Conway, & Perry, 2002). However, the possibility for participants to become aware of the repetition of the studies words in the retrieval phase remains (Mulligan & Peterson, 2008). Test awareness might have contaminated the results, by inflating the performance of healthy controls in the category verification task. Although we cannot rule out this possibility, it should be noted that in the study by Mulligan and Peterson (2008), the results never changed when aware participants were eliminated from analyses. Lastly, our encoding task (read aloud visually presented words) might have favoured the analysis of the perceptual properties of the stimuli, to the detriment of conceptual priming. In many previous studies, the dissociation between perceptual and conceptual priming has been successfully obtained using the same procedure (e.g., Gabrieli et al., 1999). Indeed, the fact that significant priming obtained in the category verification task suggests that at least part of the semantic information associated with the encoded words
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was activated during the encoding phase. Nonetheless, it remains to be determined whether schizophrenic patients show the same conceptual priming deficit after a deep encoding task (Ragland et al., 2003). Funding This study was supported by a grant from Sapienza University awarded to C. Rossi-Arnaud (Ateneo 2011; project n. C26A11RESK).
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