Está en la página 1de 11

Schizophrenia Research 80 (2005) 173 183 www.elsevier.

com/locate/schres

An investigation of semantic priming in schizophrenia using a new priming paradigm


Florence Quelen a,b, Jonathan Grainger a,*, Philippe Raymondet b
a

Laboratoire de Psychologie Cognitive, CNRS et Universite de Provence, Centre St Charles, Batiment 9, Case D, 3 place Victor Hugo, 13331 Marseille Cedex 3, France b Service de Psychiatrie secteur G01, Hopital Chalucet, rue Chalucet, 83000 Toulon, France Received 13 March 2005; received in revised form 11 July 2005; accepted 14 July 2005 Available online 2 September 2005

Abstract In the present study, twenty schizophrenic patients and twenty healthy controls were tested in a new priming paradigm that allows a clear distinction to be made between automatic, perceptual priming effects and effects related to decision bias. Participants had to identify briefly presented masked target words preceded by clearly visible primes that were semantically related to the target or not. Target presentation duration corresponded to a pre-determined perceptual threshold for each participant, and a two-alternative forced-choice methodology was used. Equivalent amounts of semantic priming were found in schizophrenic patients compared with healthy controls. However, for the schizophrenic patients, a positive correlation was found between the size of automatic perceptual priming effects and formal thought disorders, as measured by Andreasens Thought, Language and Communication (TLC) scale. The new paradigm tested in the present study overcomes some of the limitations of prior research on semantic priming in schizophrenia, and provides further evidence suggesting that an increased spreading of activation in the semantic network could partly underlie formal thought disorders in schizophrenia. D 2005 Elsevier B.V. All rights reserved.
Keywords: Semantic priming; Schizophrenia; Automatic processes; Formal thought disorders; Perceptual threshold

1. Introduction Formal thought disorders, as manifested in disorganized speech, is a core symptom of schizophrenia. Unfortunately, the processes underlying such disorders still remain unclear. In a recent review, Kerns and Berenbaum (2002) suggested four possible cognitive
* Corresponding author. Tel.: +33 488 576 892. E-mail address: grainger@up.univ-mrs.fr (J. Grainger). 0920-9964/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2005.07.020

impairments that could support such symptoms: impaired executive functioning, increased spreading of activation, impaired processing of semantic information, and impaired language production. Although impaired executive functioning has been consistently related to formal thought disorders, studies assessing semantic memory impairments, resulting from an increased spreading of activation in the semantic network, have produced less consistent results. This may be due in part to methodological problems associated

174

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

with the standard techniques used to measure such semantic memory impairments. One widely used technique is the semantic priming paradigm. In this paradigm, participants must respond to a target stimulus that is preceded by a prime stimulus that may or may not be semantically related to the target (e.g., the target bchairQ preceded by the prime btableQ or the prime briverQ). Semantic priming refers to the observation that participants performance in a given task (e.g., rapidly reading aloud the target wordthe word naming task, or rapidly deciding if it is a known word the lexical decision task) is improved by the presence of a semantically related prime (for a review, see Neely, 1991). Semantic priming has long since been the standard paradigm for evaluating the degree to which associations among concepts stored in semantic memory are intact. Unfortunately, the pattern of results one observes with standard semantic priming tasks is often tainted with specific methodological problems associated with these tasks. Since clarifying possible impairments of semantic memory in schizophrenia is crucial for developing our understanding of this illness and appropriately adapting the treatment process, the present study presents and tests an improved methodology for attaining these goals. Standard semantic priming is known to be influenced by so-called strategic factors that are extraneous to the normal operation of semantic memory. Researchers have used manipulations of SOA (Stimulus Onset Asynchrony, time elapsed between the appearance of the prime and the appearance of the target), and the proportion of related trials versus unrelated trials in an experiment, in order to tease apart automatic and more strategic components of priming. The use of short SOAs (i.e., b400500 ms), and a low proportion of related trials (i.e., b20%) are supposed to limit strategic influences thus emphasizing automatic effects (Neely, 1991). To date, research with schizophrenic patients using standard semantic priming has produced contradictory results (see Minzenberg et al., 2002, for a review). At shorter SOAs, several studies have found heightened semantic priming effects (hyperpriming) for schizophrenic patients compared to controls. Interestingly, this hyper priming was found in patients presenting disorganized forms of formal thought disorders such as associative loosening, loss of goal, and tangential speech. From a methodological point of view, heightened priming effects in thought disordered

(TD) patients were observed using both lexical decision and word naming tasks (e.g., Moritz et al., 2001a,b) and with direct (Chenery et al., 2004; Manschreck et al., 1988; Moritz et al., 2001a; Spitzer et al., 1994) as well as indirect1 semantic relationships (Moritz et al., 2001b, 2002; Spitzer et al., 1993; Weisbrod et al., 1998). In reference to classical semantic memory models (e.g., Collins and Loftus, 1975), this set of results lead authors like Spitzer and Moritz to hypothesize that thought disordered schizophrenic patients experience stronger and/or farther-reaching automatic spreading of activation within their associative network, which in turn could underlie disorganized or incoherent speech. In contrast, several other studies have found no evidence for enhanced semantic priming at short SOAs for schizophrenic patients as compared to controls using both the lexical decision (Chapin et al., 1992; Minzenberg et al., 2003; Ober et al., 1997; Vinogradov et al., 1992) and word naming tasks (Barch et al., 1996). It should be noted that most of these studies did not distinguish TD from non TD patients, thus making it difficult to compare their results with previous ones. However, at least two studies demonstrated normal priming (Barch et al., 1996) and even hypopriming (Blum and Freides, 1995) at short SOAs when thought disordered patients were selected. Aloia et al. (1998) also reported a negative relationship between semantic priming and positive thought disorder (less priming with more severe disorder) using a word naming task and a short SOA (b 400 ms). Regarding studies using longer SOAs (i.e., N 400 500 ms), a normal (Henik et al., 1992; Minzenberg et al., 2003) to hypopriming (i.e., less priming than controls, Barch et al., 1996; Chenery et al., 2004; Ober et al., 1997) was observed for schizophrenic patients, leading to the conclusion that controlled processes are disrupted in schizophrenia. TD patients also revealed less priming as compared to non TD patients (Besche et al., 1997; Besche-Richard and Passerieux, 2003; Passerieux et al., 1997), and conIn indirect or mediated priming, the prime is related to the target only via a third mediating word (that participants do not see) that is related to both the prime and the target (e.g., liontiger-stripes, and participants are presented with the prime word blionQ and the target word bstripesQ).
1

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

175

trols (Barch et al., 1996). However, hyperpriming effects were also reported in conditions that should have encouraged controlled processing (Baving et al., 2001; Kwapil et al., 1990). Recently, Gouzoulis-Mayfrank et al. (2003) reported a hyperpriming effect for TD patients in acute state using a lexical decision task with an SOA of 700 ms (i.e., conditions that are favorable to controlled influences). Given this large variability in results across different studies, it seems that the processes underlying semantic priming abnormalities in schizophrenia are still far from being resolved. As several authors stressed in recent publications (see Chenery et al., 2004; Minzenberg et al., 2002; Moritz et al., 2001b, 2002), the inconsistency in the literature may result from differences across studies in terms of patient selection criteria (indexed by medication status, length of illness, age, symptomatology), type and proportion of related prime-target pairs (direct priming versus indirect priming; high or low proportion), and type and configuration of the priming task (lexical decision versus word naming tasks, short or long SOAs). Of particular relevance to the present study is that the means of assessing thought disorders in schizophrenic patients was also suggested to be a possible source of variation. However, above and beyond the possible influence of these factors, there are a number of methodological problems that complicate the interpretation of the results obtained with standard semantic priming paradigms. One is the fact that the involvement of automatic or strategic processes is almost always inferred on the basis of SOA duration. Unfortunately, there is no universal SOA that distinctly separates such processes, and the SOA necessary to demonstrate automatic priming may vary from task to task (see Hutchison, 2003). A second main problem is that schizophrenic patients and controls are tested using the same prime durations, even if it is well established that schizophrenic patients typically need longer presentation durations to perceive a stimulus. Recent visual backward masking studies, for example, have demonstrated disruptions to patients perception of rapid, sequential bits of information (e.g., Butler et al., 2002; Cadenhead et al., 1997). Impairments in perceptual organization have also been demonstrated, and have been interestingly linked to disorganized thinking and speech in schizophrenic patients (e.g., Izawa and Yamamoto, 2002; Silverstein et al., 2000). Hence it is possible that some observed

differences in semantic priming could be due to perceptual processing deficits in schizophrenic patients. A third problem is that extensive research has demonstrated that schizophrenic patients are slower than normal control subjects on a range of reaction time tasks (Vinogradov et al., 1998). Difference scores (i.e., priming effect sizes) can be artifactually larger simply because the baseline reaction times are slower (the slower the baseline reaction time the more room there is for improvement). Thus, the quite large differences in overall reaction times between schizophrenic patients and controls that arise in standard semantic priming paradigms raise problems in interpreting differences in priming effect sizes. To rule out these methodological problems, and further explore the involvement of automatic and strategic processes in semantic priming in schizophrenia, the present study used a modified semantic priming paradigm (Huber et al., 2001). This new paradigm allows (1) a clear distinction to be made between automatic and more controlled processes, (2) the on-line modification of procedural parameters as a function of individual perceptual thresholds, (3) a focus on accuracy of response rather than reaction time. As presented in Fig. 1, participants have to identify a briefly presented, pattern-masked target (target flash duration corresponds to a pre-determined perceptual threshold for each participant) preceded by a clearly visible prime word, by selecting between two alternative choices, one of which is the target word and the other is called the foil (two-alternative forced-choice). Four conditions can be distinguished in this paradigm (examples are reported in Table 1): (C1) neither the target nor the foil are related to the prime (neither primed condition); (C2) both the target and the foil are related to the prime (both primed condition); (C3) only the target is related to the prime (target primed condition); (C4) only the foil is related to the prime (foil primed condition). In analyzing the priming effects obtained with this paradigm, Huber et al. (2001) made a critical distinction between prime-induced changes that affect extraction of information during processing of the target (what they referred to as a bperceptualQ priming effect), and other changes such as guessing biases that occur during decision making (what they referred to as a bpreferentialQ priming effect). Both perceptual and preferential priming effects are measured by comparing performance across specific priming condi-

176

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

500 ms

Blank

100 ms

PRIME

500 ms

Blank

100 ms

########

17 ms

TARGET (33, 50, ...., 168 ms, set individually) ######## Test display: until response TARGET XFOILX

Fig. 1. The sequence of events for the experimental session.

tions. Perceptual priming effects can be estimated by subtracting performance in the neither-primed condition from performance in the both-primed condition (C2C1). The idea is that, on average, preference
Table 1 Examples of priming materials, adapted from Huber et al. (2001) Priming condition C1: Neither C2: Both C3: Target C4: Foil Prime WOUND CABIN or HOTEL LODGE CABIN LODGE CABIN or BEACH SHELL C1: Neither the target nor the foil is related to the prime (wound is not related to cabin or hotel). C2: Both the target and the foil are related to the prime (lodge is related to cabin and hotel). C3: Only the target is related to the prime (lodge is only related to cabin, and not to beach). C4: Only the foil is related to the prime (shell is only related to beach, and not to cabin). Target Choice words (target and foil)

effects are equated if both choices are primed. Thus, improved performance in the both-primed condition as compared to the neither primed condition provides evidence of a perceptual enhancement of the target stimulus by the prime presentation. In a semantic priming situation, this perceptual enhancement could arise via automatic spreading activation from the prime words semantic representation to that of the target word. In the present study we refer to this as an automatic, perceptual priming effect. On the other hand, preferential effects can be estimated by comparing the target-primed condition to the both-primed condition (C3C2). Both conditions involve equal effects on target perception because in both cases the prime is related to the target, thus equating perceptual effects. In such conditions, enhanced performance in the target primed condition as compared to the both primed condition provides evidence for preferential effects. Similarly, a comparison of neither primed to foil-primed (C1C4) involves equal effects on target perception, because in both cases the prime is unrelated to the target. Therefore, a decreased per-

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

177

formance in the foil primed condition is also an indicator of preference effects. Finally, a comparison of the target primed condition to the neither primed condition (C3C1) provides a measure of a global priming effect, combining both perceptual and preference effects. Using this procedure, this new paradigm allows a distinction to be made between automatic perceptual effects and decision bias effects in a priming situation using relatively long SOAs and clearly identifiable primes. This is to our knowledge the first study that tests semantic priming in schizophrenic patients using this paradigm. The paradigm allows a principled analysis of automatic priming versus more strategically based priming while maintaining clearly visible prime stimuli. Furthermore, overall performance across patient and control groups is equated by adjusting target presentation times to each participant, hence allowing us to avoid potential artifacts associated with large differences in overall performance across groups. In the present study we use this new paradigm: (1) to test for semantic priming abnormalities in schizophrenic patients; (2) to determine whether priming effects are obtained on perceptual or preferential indices; (3) to establish a link between priming effects and patients symptoms with particular regard to formal thought disorders.

nia where included for the present study. Exclusion criteria were a history of drug or alcohol abuse, significant brain pathology (e.g., epilepsy or brain injury), electroconvulsive therapy within the last 6 months. All patients took medication at the time of the study. Psychopathology was assessed using two rating scales: the Positive And Negative Syndrome Scale (PANSS, Kay et al., 1987), a widely used measure for assessing psychiatric symptoms; and the scale for the assessment of Thought, Language and Communication (TLC scale, Andreasen, 1979a,b; French version: Bazin et al., 2002). These scales were chosen because of their widespread use in clinical work and research. The TLC scale was selected because of its emphasis on the linguistic components of thought disorder. Psychopathology ratings were performed without knowledge of task performance. Patients showed a range of illness severity on both scales. Twenty other participants (18 males, 2 women) served as healthy controls. Exclusion criteria were a history of psychiatric illness, significant brain pathology (e.g., epilepsy or brain injury), drug or alcohol abuse and the use of psychoactive medication. Participants characteristics are summarized in Table 2. There were no significant differences between participants with schizophrenia and the controls on age, F b 1, or education level, F(1,38) = 1.76, P = .19. All participants gave informed consent to participate. 2.2. Design and stimuli

2. Methods 2.1. Participants Twenty psychiatric in- and outpatients (18 males, 2 women) fulfilling the DSM-IV criteria for schizophreSixteen critical prime-target triplets (one prime and two targets) were generated using French free association norms for concrete words (Ferrand and Alario,

Table 2 Participants characteristics: demographic profile for both groups (patients and controls) and clinical data for schizophrenic patients Schizophrenic patients Mean Age (years) School education (years) PANSS total score PANSS positive subscale score PANSS negative subscale score PANSS psychopathology subscale score TLC scale total score Length of illness (years) Dosage equiv. chlorpromazine (mg/day) 31.10 11.40 79.30 18.75 22.50 38.05 7.60 8.30 639.75 S.D. 7.46 2.01 21.13 6.20 6.23 11.52 6.72 5.94 330.92 Healthy controls Mean 30.05 12.40 S.D. 9.45 2.70

178

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

1998). In each triplet, one word (the prime) was associated with the two others (targets). The first target was selected as being the most frequently related to the prime (i.e., the highest associative response given to the prime word). The second associated target was selected as being also related to the prime, and having the same length in letters as the first associate (e.g., prime=manteau bcoatQ, target 1=froid bcoldQ, target 2=hiver bwinterQ). All targets were between 3 to 6 letters long. Mean association strength (mean percentage of associative responses) for all prime-target pairings was 24.8. These triplets were then used to form the four priming conditions described in Table 1. Priming condition was manipulated within-participants and within-items. Thus, for every participant, each of the critical target words was presented as both target and foil in each of the four conditions (neutral, both primed, target primed, and foil primed). Thus a given target word appeared 8 times as one of the choice alternatives, 4 times as a target and 4 times as a foil. The prime word of each triplet was used to prime both its associates (once in the both primed condition and once in the target primed condition), but served also to prime the two associates of another triplet in the neither primed and foil primed conditions (e.g., bcoatQ served to prime its associates bcold/winterQ in the both primed and target primed conditions and the two associates byellow/ acidQ of the prime bcitrusQ in the neither primed and foil primed conditions). Thus, each prime word appeared 8 times during the experimental session. For the training session and measurement of perceptual thresholds (see the procedure section), unrelated prime-target-foil triplets were used (e.g., prime= house, target=foot, choices=foot/time). None of these appeared in the experimental session. 2.3. Procedure The experiment was divided into three sessions in the following order: (1) training session, (2) measurement of perceptual thresholds, (3) main experiment. The training session consisted of 5 trials. Participants were informed that they had to recognize very briefly presented, pattern-masked words. A complete trial (prime + target + two alternative choices, see Fig. 1) was then presented slowly, step-by-step, on the screen. Participants were then invited to position

their right and left index fingers on two keys of a computer keyboard (respectively bSQ and bLQ in an AZERTY keyboard) and to press the key corresponding to their choice (the right key corresponding to the word on the right, the left key to the word on the left). Participants were instructed that the word to be recognized would always be the second briefly displayed stimulus (i.e., the target flash) and that this word would always appear as one of the choices given for response. They then performed 4 further practice trials with the normal experimental procedure and a fixed target duration of 200 ms. The perceptual threshold procedure involved 5 blocs of 10 trials. Participants were told that the word to be recognized would be presented more and more rapidly, making their task more and more difficult. Participants were invited to try to do their best and were informed that they had to select a response on every trial even if they had not identified the target (forced-choice procedure). Individual perceptual thresholds were measured using a staircase procedure. Target duration was initially 100 ms and then adjusted until performance was at 6070% correct measured at the end of each block of 10 trials. If performance was above 70%, the following 10 trials were presented with 17 ms shorter target duration. On the other hand, if performance was less than 60%, then target duration was increased by 17 ms. Note that if 6070% performance was obtained in the first block (at 100 ms), the same target duration was used in a second block to confirm this performance. Participants were then tested in the main experiment with target duration fixed at the value obtained using the threshold setting procedure. The experimental session contained 128 critical trials (16 stimulus triplets 4 experimental conditions 2 targets, see the design and stimuli section). Fig. 1 shows the sequence of events on each experimental trial, divided as follows: (1) presentation of a fixation point (always 500 ms), (2) presentation of the prime (always 500 ms), (3) presentation of the target (200 ms for the training session, from 33 to 168 ms for the threshold session, and the previously individually determined perceptual threshold for the experimental session), (4) presentation of the choice alternatives (target and foil) until participants responded. On presentation of the two choices, the target appeared randomly at the right or the left position on half of the trials. Participants were instructed to decide which of

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

179

Table 3 Mean probability correct responses as a function of priming condition (neither, both, target, foil) and group (schizophrenic patients, healthy controls), and priming effects (global, perceptual, preferential) Schizophrenic patients Mean (%) Neither primed condition (C1) Both primed condition (C2) Target primed condition (C3) Foil primed condition (C4) Perceptual priming (C2C1) Preferential priming (C3C2) Preferential priming (C1C4) Global priming (C3C1) 75.05 81.05 83.25 73.5 6 2.2 1.55 8.2 S.D. 13.08 9.2 12.53 12.04 9.33 11 8.69 10.78 Healthy controls Mean (%) 81.85 85.85 88.6 78.1 4 2.75 3.75 6.75 S.D. 12.31 10.65 10.42 14.34 6.13 6.34 10.05 8.25

the two words had been briefly presented immediately before. Stimuli were displayed on a DELL PC laptop computer in bcourier newQ 18 font. Screen resolution was 1024 768. Screen refresh rate was 60 Hz. Order of presentation was randomized and participants were given the opportunity to rest three times during the main testing session.

3. Results 3.1. Perceptual thresholds The ANOVA on perceptual threshold durations (in ms) revealed that on average, schizophrenic patients exhibited a higher perceptual threshold (M = 57.40 F 19.90) compared to control participants (M = 42.30 F 18.51), F(1,38) = 6.169, P = .01. 3.2. Probability correct responses Table 3 provides the means for each priming condition and each group of participants. The ANOVA on probability

correct responses revealed a significant main effect of condition, F(3,114) = 18.951, P b.0001, no effect of group, F(1,38) = 2.674, P = .11, and no interaction, F b 1. Planned comparisons revealed a difference between the target primed condition (M = 85.92 F 11.69) and the neither primed (M = 78.45 F 13.00) (C3C1), indicating a global priming effect including both perceptual and preferential processes, F(1,39) = 24.721, P b.0001. A significant difference was also found between the both primed condition (M = 83.45 F 10.12) and the neither primed (C2C1), indicating a perceptual priming effect, F(1,39) = 16.16, P b.001. There was a trend to a significant difference between the neither primed condition and the foil primed (M = 75.80 F 13.28) (C1C4), F(1,39) = 3.217, P = .08, and between the target primed condition and the both primed (C3C2), F(1,39) = 3.115, P = .08, both suggestive of preferential priming effects. None of these pairwise comparisons interacted significantly with group. 3.3. Correlation analyses The relationship between priming effect sizes and clinical symptoms of schizophrenia was examined using Pearsons correlation coefficients (see Table 4). Results showed a

Table 4 Correlations between priming effects (global: C3C1; perceptual: C2C1; preferential: C3C2 and C1C4), perceptual threshold, and symptom severity as measured by the TLC scale (Thought, Language and Communication scale) and the PANSS (Positive And Negative Syndrome Scale) and subscales (positive, negative, and psychopathology) among the schizophrenic patients group Priming effects C3C1 TLC total score PANSS positive subscale PANSS negative subscale PANSS psychopathology PANSS total score *p b .10; **p b .05. .159 .314 .144 .267 .280 C2C1 .454** .059 .161 .002 .031 C3C2 .229 .358 .005 .260 .248 C1C4 .155 .087 .134 .102 .121 Perceptual threshold .392* .308 .479** .401* .450**

180

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

significant positive relationship between perceptual priming effect sizes and the presence of thought, language and communication disorders. Clinical symptoms as measured by the PANSS scale (total score and negative symptoms) were also found to be positively linked to perceptual threshold. No other correlations reached significance. A trend to a significant positive relationship was found between the TLC score and perceptual thresholds. Closer investigations concerning the link between perceptual priming effects and each item of the TLC scale revealed that btangentialityQ and bloss of goalQ were significantly correlated with these priming effects (r = .55 and .51 respectively, Ps b .05). No other correlations reached significance. Neither educational level, nor the length of schizophrenic illness, nor age and medication dosage (chlorpromazine equivalents) significantly modulated semantic priming in schizophrenia on the global, perceptual or preferential indices ( Ps N .10).

4. Discussion The main purpose of the present study was to further explore the mechanisms underlying semantic memory impairments and its relations to formal thought disorders in schizophrenia. To do so, we used a modified semantic priming paradigm (Huber et al., 2001) allowing a clear distinction to be made between automatic perceptual processes and decisionrelated processes that typically combine to generate observable priming effects. The new paradigm also helped rule out possible methodological artifacts related to perceptual deficits in schizophrenia and the observed large differences in overall performance between schizophrenic patients and controls by using long prime presentation durations (allowing clear perception of primes), and an individually adjusted target duration that equates performance across subject groups. First of all, statistically equivalent amounts of priming were found in schizophrenic patients compared to healthy controls on the global, perceptual, and preferential priming indices. Both groups (schizophrenic and controls) showed a significant global priming effect (i.e., priming including perceptual and preferential processes), and a significant perceptual priming effect. On the other hand, preferential priming effects were only marginal. This general pattern of results is somewhat similar to the pattern obtained

in Huber et al.s (2001) Experiment 4, and provides a further validation of this priming procedure, with significant variation in performance across the four priming conditions. Following Huber et al. (2001) we found significant perceptual priming effects with the forced-choice paradigm, confirming its sensitivity to automatic semantic priming. The critical comparison for measuring such effects is between the both primed condition (blodgeQ as a prime for the target bcabinQ with bhotelQ as the alternative choice) and the neither primed condition (bwoundQ as a prime for the target bcabinQ with bhotelQ as the alternative choice). Any advantage for the both primed condition cannot be attributed to any kind of strategic, decision-related mechanism, since these would favor both choice alternatives. We therefore interpret our observed perceptual priming effects, following Huber et al. (2001), as reflecting improved target word processing by activation of the targets semantic representation following spread of activation from the prime word. The fact that perceptual priming effects did not differ as a function of subject group adds support to prior research reporting equivalent amounts of semantic priming in schizophrenic patients and controls at short SOAs (Barch et al., 1996; Chapin et al., 1992; Minzenberg et al., 2003; Ober et al., 1997; Vinogradov et al., 1992). Taken together, these results would at first sight suggest that automatic semantic priming processes operate normally in schizophrenia. However, a second main result emerged from our study when taking into account schizophrenic patients displayed symptomatology. The perceptual semantic priming effect was found to be enhanced for schizophrenic patients with higher levels of formal thought, language and communication disorders (TLC scale), and especially for tangentiality (replying to a question in an oblique, tangential, or irrelevant manner) and loss of goal (failure to follow a chain of thought to its natural conclusion). No other significant correlations were found between patients symptomatology as measured by the PANSS and the TLC scale and any of our priming indices. The significant correlation between perceptual priming effects and scores on the TLC scale adds support to prior research reporting enhanced semantic priming for TD schizophrenic patients, especially at short SOAs (Chenery et al., 2004; Manschreck et al.,

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183

181

1988; Moritz et al., 2001a; Spitzer et al., 1994). As preferential effects are equated in the both primed condition compared to the neither primed condition, our estimation of perceptual priming effects is assumed to be free from any influence of expectancy or strategic processes. Thus, taking into consideration the patterns of priming effects observed in prior studies and the pattern obtained in the present study, it would appear that while general semantic priming (including both automatic and strategic influences) is not affected by schizophrenia symptomatology, automatic semantic priming is enhanced as a function of formal thought, language and communication disorders. These results, obtained with a paradigm that rules out some of the limitations associated with standard semantic priming methodology, lend support to Spitzer and Moritzs hypothesis concerning excessive automatic spreading of activation in TD patients semantic network. Known potential confounding variables such as length of illness or medication dosage did not significantly modulate our priming effects. Prior research has found that length of illness is associated with a reduction of priming at short SOAs (Maher et al., 1996). One difference with this study is that our schizophrenic sample did not include very chronic patients, thus limiting the potential impact of this variable on our data. Medication dosage has also been found to be positively related to priming effects (Barch et al., 1996). However, this variable was also strongly associated with slower response times, thus allowing for possible artifacts (with longer baseline RTs allowing for more priming). In the present testing conditions, limiting the role of such artifacts, we did not observe an influence of medication dosage. Concerning strategic influences, we found equal amounts of preferential priming for schizophrenic patients and healthy controls. These results add support to prior observations of normal priming in schizophrenia at long SOAs (Henik et al., 1992; Minzenberg et al., 2003), while contrasting with other studies reporting hypopriming (Barch et al., 1996; Ober et al., 1997) or hyperpriming (Baving et al., 2001; Gouzoulis-Mayfrank et al., 2003). In addition, no significant relationship was found between preferential priming effects and the severity of patients thought disorders, as might have been expected on the basis of some prior work (Aloia et

al., 1998; Besche et al., 1997; Besche-Richard and Passerieux, 2003; Passerieux et al., 1997). This may be due to the fact that these studies either tested very chronic patients (Aloia et al., 1998) or patients with very high levels of thought disorders (e.g., BescheRichard and Passerieux, 2003), whereas our sample of patients covered a wider spectrum of severity. This discrepancy might also be due to a relative insensitivity of our paradigm to controlled mechanisms in priming. There was only a marginally significant main effect of preferential priming, indicating that the configuration of the task (instructions, proportion of prime-target related pairs) may have limited strategic influences. A third main point is that preferential priming effects sizes could rely on higher cognitive dysfunctions, such as executive functions (Kerns and Berenbaum, 2002; Minzenberg et al., 2003), that were not assessed in our study. To clarify these different points, further modifications of the task (such as more explicit instructions concerning prime-target relatedness, a higher or lower proportion of related primetarget pairs), selection of particular patients subtypes (including acute versus stabilized state, GouzoulisMayfrank et al., 2003), and co-measurement of higher level cognitive functions are needed. Finally, schizophrenia patients had significantly higher perceptual thresholds than controls, and these thresholds were found to correlate significantly with symptom severity as measured by the PANSS. This is not surprising given that schizophrenia patients have already been shown to be impaired in perception of rapid, sequential bits of information (e.g., Butler et al., 2002). Perceptual organization has also shown to be impaired and positively related to disorganized symptomatology (e.g., Silverstein et al., 2000). Some of the inconsistent results in the semantic priming literature, especially at short SOAs and therefore short prime durations, may have resulted from such limitations in perceptual processing, especially when symptomatic patients were tested. We argue that stimulus presentation conditions need to be appropriately equated between schizophrenic patients and control participants when higher-level cognitive deficits are to be investigated free from lower-level perceptual deficits. To conclude, this study shed light on two important aspects of semantic priming in schizophrenia. First, it highlights the necessity to use adapted paradigms that take into account individual differences in symptoma-

182

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183 Besche, C., Passerieux, C., Segui, J., Sarfati, Y., Laurent, J.-P., Hardy-Bayle, M.-C., 1997. Syntactic and semantic processing in schizophrenic patients evaluated by lexical-decision tasks. Neuropsychology 11, 498 505. Besche-Richard, C., Passerieux, C., 2003. Semantic context-processing deficit in thought-disordered schizophrenic patients: evidence from new semantic priming paradigms. Cogn. Neuropsychiatry 8, 173 189. Besche-Richard, C., Passerieux, C., Segui, J., Sarfati, Y., Laurent, J.-P., Hardy-Bayle, M.-C., 1997. Syntactic and semantic proces sing in schizophrenic patients evaluated by lexical-decision tasks. Neuropsychology 11, 498 505. Blum, N.A., Freides, D., 1995. Investigating thought disorder in schizophrenia with the lexical decision task. Schizophr. Res. 16, 217 224. Butler, P.D., DeSanti, L.A., Maddox, J., Harkavy-Friedman, J.M., Amador, X.F., Goetz, R.R., Javitt, D.C., Gorman, J.M., 2002. Visual backward-masking deficits in schizophrenia: relationship to visual pathway function and symptomatology. Schizophr. Res. 59, 199 209. Cadenhead, K.S., Geyer, M.A., Butler, R.W., Perry, W., Spock, J., Braff, D.L., 1997. Information processing deficits of schizophrenia patients: relationship to clinical ratings, gender and medication status. Schizophr. Res. 28, 51 62. Chapin, K., McGown, J., Vann, L., Kenney, D., Youssef, I., 1992. Activation and facilitation in the lexicon of schizophrenics. Schizophr. Res. 6, 251 255. Chenery, H.L., Copland, D.A., McGrath, J., Savage, G., 2004. Maintaining and updating semantic context in schizophrenia: an investigation of the effects of multiple remote primes. Psychiatry Res. 126, 241 252. Collins, A.M., Loftus, E.F., 1975. A spreading activation theory of semantic processing. Psychol. Rev. 82, 407 428. Ferrand, L., Alario, F.-X., 1998. Normes dassociations verbales pour 366 noms dobjets concrets. Annee Psychol. 98, 659 709. Gouzoulis-Mayfrank, E., Voss, T., Morth, D., Thelen, B., Spitzer, M., Meincke, U., 2003. Semantic hyperpriming in thought disordered patients with schizophrenia: state or trait? A longitudinal investigation. Schizophr. Res. 15, 65 73. Henik, A., Priel, B., Umansky, R., 1992. Attention and automaticity in semantic processing of schizophrenic patients. Neuropsychiatry Neuropsychol. Behav. Neurol. 5, 161 169. Huber, D.E., Shiffrin, R.M., Lyle, K.B., Ruys, K.I., 2001. Perception and preference in short-term word priming. Psychol. Rev. 108, 149 182. Hutchison, K.A., 2003. Is semantic priming due to association strength or feature overlap? A microanalytic review. Psychon. Bull. Rev. 10, 785 803. Izawa, R., Yamamoto, S., 2002. Spatio-temporal disintegration of visual perception in schizophrenia as revealed by a novel cognitive task, the searchlight test. Schizophr. Res. 53, 67 74. Kay, S.R., Fiszbein, A., Opler, L.A., 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13, 261 276. Kerns, J.G., Berenbaum, H., 2002. Cognitive impairments associated with formal thought disorder in people with schizophrenia. J. Abnorm. Psychology 111, 211 224.

tology and perceptual processing in order to clarify semantic memory abnormalities in schizophrenia. Second, it provides data that further suggest that increased activation in the semantic network could partly contribute to disorganized forms of thought and communication disorders by making words more susceptible to extraneous cognitive associations. In that framework, the two-choice paradigm of Huber et al. (2001) appears to offer an interesting methodological tool for further exploring the mechanisms underlying formal thought disorders in schizophrenia.

Acknowledgements The authors would like to thank Dr. Christine Lerouge and Anne Deleris-Raucoules for their help in data collection, Stephane Dufau for programming the experiment, and the staff of the Chalucet Hospital Psychiatry Department G01. Thanks also to Gina Kuperberg and Donna Kreher for comments on an earlier version of this work. Correspondence concerning this article can be sent to Florence Quelen (florence.quelen@up.univ-mrs.fr).

References
Aloia, M.S., Gourovitch, M.L., Missar, D., Pickar, D., Weinberger, D.R., Goldberg, T.E., 1998. Cognitive substrates of thought disorder: II. Specifying a candidate cognitive mechanism. Am. J. Psychiatry 155, 1677 1684. Andreasen, N.C., 1979a. Thought, language and communication disorders: I. Clinical assessment, definition of terms and evaluation of their reliability. Arch. Gen. Psychiatry 36, 1315 1321. Andreasen, N.C., 1979b. Thought, language and communication disorders: II. Diagnostic significance. Arch. Gen. Psychiatry 36, 1325 1330. Barch, D.M., Cohen, J.D., Servan-Schreiber, D., Steingard, S., Steinhauer, S.S., van Kammen, D.P., 1996. Semantic priming in schizophrenia: an examination of spreading activation using word pronunciation and multiple SOAs. J. Abnorm. Psychology 105, 592 601. Baving, L., Wagner, M., Cohen, R., Rockstroh, B., 2001. Increased semantic and repetition priming in schizophrenic patients. J. Abnorm. Psychology 110, 67 75. Bazin, N., Lefrere, C., Passerieux, Y., Sarfati, Y., Hardy-Bayle, M.-C., 2002. Troubles formels de la pensee : traduction fran caise de lechelle devaluation de la pensee, du langage et de la communication (Scale for the assesment of Thought, Language and Communication: TLC). Encephale 28, 109 119.

F. Quelen et al. / Schizophrenia Research 80 (2005) 173183 Kwapil, T.R., Hegley, D.C., Chapman, L.J., Chapman, J.P., 1990. Facilitation of word recognition by semantic priming in schizophrenia. J. Abnorm. Psychology 99, 215 221. Maher, B.A., Manschreck, T.C., Redmond, D., Beaudette, S., 1996. Lengh of illness and the gradient from positive to negative semantic priming in schizophrenic patients. Schizophr. Res. 22, 127 132. Manschreck, T.C., Maher, B.A., Milavetz, J.J., Ames, D., Weisstein, C.C., Schneyer, M.L., 1988. Semantic priming in thought disordered schizophrenic patients. Schizophr. Res. 1, 61 66. Minzenberg, M.J., Ober, B.A., Vinogradov, S., 2002. Semantic priming in schizophrenia: a review and a synthesis. J. Int. Neuropsychol. Soc. 8, 699 720. Minzenberg, M.J., Poole, J.H., Vinogradov, S., Shenaut, G.K., Ober, B.A., 2003. Slowed lexical access is uniquely associated with positive and disorganised symptoms of schizophrenia. Cogn. Neuropsychiatry 8, 107 127. Moritz, S., Mersmann, K., Kloss, M., Jacobsen, D., Andresen, B., Krausz, M., Pawlik, K., Naber, D., 2001a. Enhanced semantic priming in thought-disordered schizophrenic patients using a word pronunciation task. Schizophr. Res. 48, 301 305. Moritz, S., Mersmann, K., Kloss, M., Jacobsen, D., Wilke, U., Andresen, B., Naber, D., Pawlik, K., 2001b. dHyper-primingT in thought-disordered schizophrenic patients. Psychol. Med. 31, 221 229. Moritz, S., Woodward, T.S., Kuppers, D., Lausen, A., Schickel, M., 2002. Increased automatic spreading of activation in thought disordered schizophrenic patients. Schizophr. Res. 59, 181 186. Neely, J.H., 1991. Semantic priming effects in visual word recognition: a selective review of current findings and

183

theories. In: Besner, D., Humphreys, G.W. (Eds.), Basic Progress in Reading: Visual Word Recognition. Erlbaum, Hillsdale, NJ, pp. 264 333. Ober, B.A., Vinogradov, S., Shenaut, G.K., 1997. Automatic versus controlled semantic priming in schizophrenia. Neuropsychology 11, 506 513. Passerieux, C., Segui, J., Besche, C., Chevalier, J.-F., Widlocher, D., Hardy-Bayle, M.-C., 1997. Heterogeneity in cognitive functioning of schizophrenic patients evaluated by a lexical decision task. Psychol. Med. 27, 1295 1302. Silverstein, S.M., Kovacs, I., Corry, R., Valone, C., 2000. Perceptual organization, the disorganized syndrome, and context processing in chronic schizophrenia. Schizophr. Res. 43, 11 20. Spitzer, M., Braun, U., Hermle, L., Maier, S., 1993. Associative semantic network dysfunction in thought disordered schizophrenic patients: direct evidence from indirect semantic priming. Biol. Psychiatry 34, 864 877. Spitzer, M., Weiker, I., Winter, M., Maier, S., Hermle, L., Maher, B.A., 1994. Semantic and phonological priming in schizophrenia. J. Abnorm. Psychology 103, 485 494. Vinogradov, S., Ober, B.A., Shenaut, G.K., 1992. Semantic priming of word pronunciation and lexical decision in schizophrenia. Schizophr. Res. 8, 171 181. Vinogradov, S., Poole, J.H., Willis-Shore, J., Ober, B.A., Shenaut, G.K., 1998. Slower and more variable reaction times in schizophrenia: what do they signify? Schizophr. Res. 32, 183 190. Weisbrod, M., Maier, S., Harig, S., Himmelsbach, U., Spitzer, M., 1998. Lateralised semantic and indirect semantic priming effects in people with schizophrenia. Br. J. Psychiatry 172, 142 146.