Schizophrenia Research 85 (2006) 1 – 11 Evidence for impaired mnemonic strategy use among patients with schizophrenia using the part-list cuing paradigm Bruce K. Christensen a,b,*, Todd A. Girard a,b, Aaron S. Benjamin c, Pierre Vidailhet d a Neuropsychology Lab, Schizophrenia Program, Centre for Addiction and Mental Health, 250 College Street, Toronto, ON, Canada M5T 1R8 b Department of Psychiatry, University of Toronto, Canada c Department of Psychology and Beckman Institute for Advanced Science and Technology, University of Illinois, Urbana-Champaign, USA d INSERM Unite 405 Psychopathologie et Pharmacologie de la Cognition, Strasbourg, France Received 3 March 2006; accepted 3 March 2006 Purpose: Strategic and mnemonic abilities of person with schizophrenia (SCZ) were studied using a part-list cuing (PLC) task.
In this task, presentation of retrieval cues in the form of a subset of studied words typically impairs recall of the remainingitems. This impairment is thought to reflect a disruption of participants’ natural retrieval strategies.
Methods: Participants with SCZ and healthy controls (ns = 28) studied word lists with three different levels of semanticorganization: (a) unrelated, (b) categorized, but presented in a random order, and (c) presented by category. For each type of list,participants recalled words under both free-recall and PLC conditions.
Results: Consistent with SCZ-related impairment of strategic retrieval processes, the SCZ group was less disrupted by PLCinterference than controls in the unrelated-list condition. Comparison of free recall across lists also indicated a consistent deficitin SCZ despite varying levels of difficulty and retrieval contexts. Nonetheless, the SCZ group demonstrated parallelimprovement to the healthy group with increasing list organization.
Conclusions: These results provide evidence of deficient retrieval processes in SCZ in a context placing maximal requirementsfor utilization of self-initiated, effortful, mnemonic strategies. Unlike most extant results demonstrating mnemonic impairmentin persons with SCZ, the present results cannot be accounted for by task difficulty; SCZ participants’ recall was less disruptedby PLC than was that of healthy participants. Results also demonstrated that SCZ participants could benefit, in terms of recalland strategy use, from list organization when this structure was explicitly provided at test.
D 2006 Elsevier B.V. All rights reserved.
Keywords: Schizophrenia; Part-list cuing interference; Memory; Semantic organization; Mnemonic strategy * Corresponding author. Neuropsychology Lab, Schizophrenia Program, Centre for Addiction and Mental Health—College Street Site, 250 College Street, Toronto, Ontario, Canada M5T 1R8. Tel.: +1 416 535 8501x6843; fax: +1 416 979 6936.
0920-9964/$ - see front matter D 2006 Elsevier B.V. All rights reserved.
B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 strategies aimed at free recall of the whole list to a lessefficient plan that is guided by the external, experi- Deficits in declarative memory are particularly menter-supplied cues. That PLC results in a tempo- robust among persons with schizophrenia (SCZ; rary disruption at retrieval is further supported by observations that recall for bforgottenQ target items and Zakzanis, 1998; Saykin et al., 1991, 1994; Weiss returns if tested again under uncued conditions and Heckers, 2001). However, the specific underlying mechanisms of this impairment remain largely un- and Milner, 1993). Although several theoretical clear. One notable aspect of deficient memory in SCZ is a reduction in the spontaneous application of Aslan, 2004; Mueller and Watkins, 1977; Nickerson, organizational strategies to aid recall, including 1984; Raaijmakers and Phaf, 1999; Raaijmakers and Shiffrin, 1981; Rundus, 1973; Sloman et al., 1991), the strategy disruption hypothesis remains a particu- 2004) organization of to-be-remembered material.
larly prominent, accepted, and tenable account ( Furthermore, persons with SCZ typically require a den and Basden, 1995; MacLeod et al., 2003). This more objective, salient, and/or explicit representation hypothesis predicts that PLC will result in less in order to benefit from any inherent organizational disruption to individuals who are less able to utilize techniques that enhance memory organization. In this Interpretations of many SCZ memory findings are regard, diminished interference in SCZ would signify complicated, however, by a confounding of differen- organizational memory deficits unencumbered by tial deficit with task difficulty (e.g., less organized lists are more difficult to recall). The challenge of Importantly, several factors influence the magni- equating tasks for difficulty in order to demonstrate a tude and direction of PLC effects, which depend on btrueQ differential deficit is non-trivial and the compatibility of participants’ free (uncued) recall and Chapman (1973) suggest an alternative solution: strategies with the organization imposed by retrieval use experimental manipulations where deficits actu- cues and its relation to the remaining targets ( ally improve performance or disrupt it less compared and Basden, 1995; Sloman et al., 1991). Of particular relevance is the importance of list structure ( erson, 1984). Manipulations of list structure may be In this regard, one promising approach for inves- used to induce common output strategies between tigating differential strategic mnemonic processes in participants. For example, presenting category mem- SCZ involves interference via part-list cuing (PLC).
bers consecutively encourages participants to encode those items as exemplars of a common category.
evidenced when the provision of a subset of previ- Consequently, when using organized lists, cues ously studied words as retrieval cues interferes with facilitate recall to the extent that they remind recall of the remaining non-cued target items. In this participants of super-ordinate categories. However, vein, it is more appropriate to consider PLC as increasing the proportion of cues from a given providing a retrieval context than a recall aid category increasingly impairs recall of remaining 1995; Bellezza and Hartwell, 1981; Lewis, 1971; 1977) have conceptualized PLC interference as a Nickerson, 1984; Penney, 1988; Roediger, 1973, retrieval strategy disruption. From this view, the 1974; Roediger et al., 1977; Rundus, 1973). This structure of recall output is a reflection of an result presumably arises because the presence of cues organized retrieval plan that may be influenced by encourages participants to switch from their bnaturalQ retrieval order to a strategy by which they use cues to 1995; Slamecka, 1968; Sloman, 1991). In other elicit memories for unpresented items.
words, PLC alters the retrieval environment and In contrast to lists blocked by category, scrambled prompts participants to switch from self-generated presentation of exemplars from multiple categories B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 may lead participants to form categories that are more assessed performance across three levels of semantic narrow or broad than intended by the experimenter organization: (a) unrelated lists, whose recall relies most on participant-generated strategy; (b) scrambled zational strategies are even more expected with lists of category lists; and (c) blocked category lists that unrelated words, where the likelihood of congruency explicitly define organizational structure. We pre- between random/experimenter-selected cues with par- dicted a Group x Cue x List type interaction such that ticipant-generated strategies may reduce to chance the SCZ group would demonstrate attenuated PLC interference especially with unrelated lists, but show a tion across these three list types–unrelated, scrambled, similar effect of cuing when provided an organiza- and blocked–should facilitate more homogenous tional strategy in the blocked condition.
mnemonic strategy use across individuals. To theextent that persons with SCZ are similarly influencedby semantic organization, increased list structure should produce more similar PLC profiles.
Although extensively investigated in healthy sam- ples, application of PLC to clinical populations hasbeen rare ( Thirty persons with either SCZ or Schizoaffective and Milner, 1993). Attenuated PLC interference in Disorder were recruited via the Schizophrenia Regis- SCZ was indirectly suggested by the multinomial try for Research at the Centre for Addiction and Mental Health (CAMH, Toronto, Canada), poster separately demonstrated that (a) PLC in healthy advertisement at the CAMH, and referrals from health individuals affected only retrieval parameters and that professionals; 30 healthy control (HC) participants (b) performance of a SCZ group tested only on free were recruited from the community via local news- recall implicated reduced storage as well as greater paper advertisements or word of mouth. However, retrieval deficits. However, only one prior study has data for two participants per group were excluded due directly studied PLC in SCZ and concluded that to technical problems during the PLC computer similar PLC profiles to a healthy group bindicates program; all results reported are based on the remai- normal retrieval performance in SCZ patients under Inclusion criteria included ability to provide 2005, p. 278). Visual inspection of these data, informed consent, age between 18 and 60 years, however, suggests that the study may have been English as the primary language, and (corrected-to-) underpowered to detect a subtle differential PLC normal vision. Exclusion criteria consisted of a history effect in SCZ. In fact, their power to detect even a of neurological injury/disease (including brain injury large interaction effect ( f = .40) was only .57 (al- with loss of consciousness), lifetime history of any (HC) or any non-psychotic (SCZ) Axis I psychiatric weak grounds for concluding a null hypothesis, but disorder (including alcohol/substance dependence or significance hypothesis testing only allows for a abuse—SCZ accepted if abuse N6 months prior), first- dfailure to rejectT it. Alternatively, the scrambled degree relative with a psychotic disorder (HC), recent category lists used may not be sensitive to differential (b2 weeks) use of psychotropic drugs (HC) or change interference in SCZ. Clearly these results from this in use of antipsychotic medication (SCZ), and single study underscore the need for increased prescribed medications with known deleterious cog- research of the PLC phenomenon in SCZ.
nitive effects (i.e., tricyclic antidepressants, anticholi- In sum, this study’s purpose was to investigate nergics). Three patients prescribed benzodiazepines mnemonic strategy use in SCZ via PLC, for which (bas neededQ) and who abstained from these for at deficient organizational retrieval processes would lead least 3 days prior testing were accepted, as were six to less interference, a result not accounted for by a patients prescribed serotonin specific re-uptake inhib- difficulty confound. Given the importance of list itors and one prescribed bupropion for depressive structure for both general recall and PLC effects, we symptoms. Confirmation of SCZ diagnoses and B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 screening of HC participants were made via the relative impairment of declarative memory, however, Structured Clinical Interview for DSM-IV-TR Axis I measures of verbal and visual memory were inferior in SCZ. Nonetheless, both groups’ mean performance was in the average range across these measures.
participants were provided compensation of $10.00/h.
Descriptive information for the SCZ group is provided in As shown in the groupsdid not differ significantly with regards to sex, age, or Three list types were constructed: (a) unrelated; (b) education; but, expectedly, the SCZ group had lower scrambled (semantically related words in random levels of competitive employment. Symptom ratings order, without replacement); and (c) blocked (clus- confirmed that the SCZ group was clinically stable with tered by category). The organized lists (b, c) were respect to patient norms (but reported greater derived from 24 of the taxonomic lists in psychopathological symptomatology than HCs ( Montague (1969; median category potency, Md = 2). All HC participants were within normal limits on all 6.86). Eight words per category were selected, symptom measures (save one scoring in the mildly omitting the two highest frequency exemplars to elevated range on the depression and stress scales).
reduce guessing biases. For each SCZ–HC pair, fourlists (designated Blocked sets A and B and Scrambled sets A and B), comprised of eight words selectedrandomly from six categories (i.e., 48 words per list), Assessment of general intelligence failed to reveal were created. Unrelated sets A and B (48 words each) were obtained from the MRC PsycholinguisticsDatabase (to match the psycholinguis-tic characteristics of the categorized lists (3–10 letters; concreteness 426–645; imagability 461–640; written Frequencies and medians (ranges) of SCZ patient characteristics frequency b 203). The final 96 nouns randomly selected from this pool further met requirements that they could not be easily grouped into semantic categories and did not belong to any categories used in the organized lists. Each of the six sets was presented twice in a row during the learning phase to 3 (loxapine, zuclopenthixol,perphenazine + methotrimeprazine) aid encoding, but such that no two words followed each other in both presentations, in order to negate the use of serial order as a mnemonic strategy. Scrambled lists also required that words from the same category did not immediately follow each other. Additionally, blocked lists were formed such that adjacent pairs of categories differed between study presentations. All Abbreviations: AIMS = Abnormal Involuntary Movement Scale random-order procedures were conducted on an individual SCZ–HC pair-wise basis (i.e., 30 series of Rating Scale; CPZe = Clorpromazine equivalents ( Butler and Jeffries, 2004); DDD = defined daily dose ( Sets A and B for each list type were counter- 2005); PANSS = Positive and Negative Symptom Scale ( balanced within groups to either the free (FR) or cued a Two patients had been neuroleptic free for several weeks.
recall (QR) condition. Free recall sheets consisted of b Includes one or both olanzapine and resperidone.
six columns of blank lines for participants’ responses.
c CPZe-values were unavailable for zuclopenthixol, perphenazine, Sheets for the blocked and scrambled conditions and methotrimeprazine; DDD was unavailable for methotrimepra- provided category labels as column headings (in zine; data include nil values from the two neuroleptic-free patients.
lower-case) in a pseudo-randomized order to limit the One individual taking double the conventional dose of antipsychotics scored 10 on the AIMS; the next highest value was 3.
experimental manipulation to word (as opposed to B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 Table 2Demographic and clinical characteristics of the HC and SCZ groups a,b Use of (a) meansF standard deviations (M F S.D.) or (b) medians (range) reflect normal or non-normal distributions of data, respectively, ineither group; t-test results are reported for both as these paralleled non-parametric results.
c Employment status: unemployed/student/employed/retired; significant 2 reflects more (z N 2) unemployed SCZ and student HC participants.
d e data excludes four SCZ participants with incomplete ratings.
Abbreviations: DASS-21 = 21-item version of the Depression, Anxiety and Stress Scale (1995); PAI = Personality Assessment Inventory (WAIS-III FSIQe = estimated full-scale intelligence quotient derived from theMatrix Reasoning and Information subtests of the Wechsler Adult Intelligence Scale—Third Edition (1997a); WMS-III = Wechsler Memory Scale—Third Edition (WRAT-3 = Wide Range Achievement Test—Third Edition( stone, 1966); the order for blocked lists did not matchthat at study. Cued recall sheets included 30 studied Unrelated lists were presented first, followed by words (cues) in capital letters and 18 blanks to be the blocked and scrambled lists in a counterbalanced filled in with the respective target words. Cues and order. Within each list condition, FR preceded QR. At blanks were presented pseudo-randomly such that encoding, participants made pleasantness judgements adjacent words differed from their presentation at (bLikeQ, bDislikeQ) to single words presented on a study and no more than three cues or two blanks computer monitor for 2 s each (ISI = 1 s). Study words were presented consecutively; for organized lists, five were presented in uppercase type and lowercase labels exemplars per category were cues and three were preceded each category in the blocked condition.
deemed targets. Three random assortments defining Participants were also instructed to remember the targets and cues were created for each of the words. After each list was shown twice, a 90-s buffer unrelated sets and the category lists and these consisting of recall instructions plus a symbol configurations were assigned haphazardly among cancellation task was inserted to avoid any differential B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 Slamecka, 1969). Recall of each list was then limited ance, or sphericity. Deviation from normality was to 7 min. For blocked and scrambled conditions this was divided into 1-min per category (remaining parametric results reported did not differ from trans- categories covered), plus a seventh for any additional recall. On QR trials, participants were instructed to Results were evaluated at an alpha-level of .05 with read the cues and consider them as aids.
The primary measure of interest was the number of correctly recalled target words, equating FR and QR measures to a score out of 18. Two additionalmeasures provided validity checks: (a) percent correct of available words to recall (FR/48, QR/18), where revealed main effects of all factors on target recall, comparable results indicate appropriate randomization Group (SCZ b HC), F(1, 54) = 6.77, p = .012, f = 0.35, List (Unrelated b Scrambled b Blocked), F(2, 108) = difference as a percent of total correct (QR + FR), 254.60, p b .001, f = 2.17, and Cue (QR b FR), F(1, given the potential for general ability to influence 54) = 33.44, p b .001, f = 0.79. Importantly however, these effects were qualified by their three-way Chapman, 1988, 1989, 2001), including PLC con- interaction, F(2, 108) = 4.69, p = .011, f = 0.29 (see These analyses yielded parallel results to those with List type revealed a two-way interaction only with raw targets and thus, we present only the latter more Unrelated lists, F(1, 54) = 10.77, p = .002, f = 0.45.
conventional data. For clarity, the remaining word This finding reflected that the SCZ group was types are termed bcuesQ (QR) or bnon-targetsQ (FR) impaired in FR, t(54) = À 2.88, p = .006, d = À 0.77, depending solely on the cuing condition under which but that a greater interference effect among HCs resulted in equivalent Unrelated-QR performances, Target recall revealed no significant outliers or t(54) = À 0.07, p = .944, d = À 0.02. Similar analyses of violations regarding normality, homogeneity of vari- Scrambled and Blocked Lists revealed only main Fig. 1. Mean recall of target words (+ S.E.) in HC and SCZ groups during free recall (FR) and cued recall (QR) conditions at each of the threelevels of semantic organization. Note the attenuated interference of part-list cues in SCZ for the most difficult unrelated-list condition.
B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 effects of Cue and Group; that is, although overall represented the degree to which each participant’s recall was reduced in SCZ, similar PLC interference QR performance deviated from that predicted from was observed in the context of organized lists.
his/her FR score. The mean zQR for the HC group is In addition to within-list effects, it was of interest thus zero and the z-scores for SCZ participants to examine the effects of list organization. Main indicate their deviation from the HC expected values.
effects of Group and List were maintained in separate Regression of HC QR on FR scores confirmed significant, positive, and medium to large associa- organization aided FR of both groups similarly, F(2, tions, Unrelated R2 = .27, p = .005, f 2 = 0.37, Scram- 108) = 0.07, p = .934, f = 0.03. In contrast, a Group x bled R2 = .67, p b .001, f 2 = 2.03, Blocked R2 = .17, List interaction, F(2, 108) = 6.01, p = .003, f = 0.33, p = .028, f 2 = 0.20. A two-way ANOVA of zQR-scores reflected a SCZ deficit in QR only with organized revealed identical effects of List and Group x List interaction, both Fs(2, 108) = 3.91, ps = .023. Thisinteraction supported the previous raw target analyses and indicated better QR performance in SCZ thanexpected from the HC regression line in the Unrelated There was no overall difference in error production condition, t(27) = 2.52, p = .018, d = 0.48. Inter-corre- between the SCZ (Md = 6.00, range: 0–23) and HC lations further supported a division between Unrelated groups (Md = 6.50, range: 0–39), t(54) = 0.34, p = .733, and organized PLC interference: there was no relation d = 0.09. Moreover, the groups did not differ signif- between Unrelated and Scrambled, HC, r(28) b .01, icantly in their rates of any specific error types and p = .996, SCZ, r(28) = À .25, p = .209, or Blocked thus, these are primarily of task-related interest. Most zQR’s, HC, r(28) = .01, p = .957, SCZ, r(28) = .16, common were semantic intrusions in organized-list p = .408. In contrast, correlations between the orga- recall (170 by 86% of HC, 124 by 75% of SCZ), nized lists were significant, positive, and large, HC, which proved sensitive to PLC interference (FR N QR), r(28) = .51, p = .005, SCZ, r(28) = .50, p = .006.
F(1, 54) = 4.30, p = .043, f = 0.28. Intrusions of irrele- Correlations among the PLC zQR scores with vant/unrelated words were also common (48 and 62 by demographic, diagnostic, symptom, medication, and 61% of both HC and SCZ, respectively), the majority cognitive measures only revealed notable relations (88%) occurring with Unrelated lists. Thus, a majority between increased ratings of depression, anxiety, and of participants produced intrusions in recall that may 1995) with greater PLC interference (lower zQR’s) among HC participants on the organized lists also somewhat frequent (13 by 32% of HC, 23 by 43% (r’s b À.40). It is not immediately clear how to of SCZ), indicating that participants wrote down cue interpret these relations or why they were only found words that were printed in front of them. Other types of in the HC group; replication of these observations may prove interesting for future study.
3.3. Individual differences and correlational analyses Last, it was of interest to assess individual differ- ences in PLC effects and their correlations with other Strategic and mnemonic abilities in SCZ were sample characteristics. The FR–QR interference effect investigated using PLC at three levels of semantic was of most interest in this regard. Because of organization. Cuing at retrieval and increasing within- problems with raw difference scores, we instead used list semantic structure were successful in interfering standardized residualized scores as suggested by and facilitating recall output, respectively. An overall deficit in SCZ across PLC and neuropsychological mance of HC participants was first regressed on their measures of memory was also expected. Most FR scores, then these results were used to compute importantly, the three-way interaction reflected a standardized residuals (zQR) for both groups that differential PLC effect in the unrelated-list condition B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 only. In the context of maximal requirements for hypothesis that persons with SCZ are particularly less effortful, self-initiated, strategic organization, the SCZ apt to self-generate and employ effortful organized group demonstrated impaired FR but equivalent retrieval strategies. That is, the SCZ results indicate performance to the HC group in the more difficult use of an initially less efficient and less organized QR condition. That is, the SCZ group was less strategy during FR, which only reduces to an equally disrupted by PLC interference, consistent with hy- inefficient strategy as the HC group during QR (see pothesized deficits in the aforementioned abilities. In In sum, the current results are consistent with contrast, the SCZ group showed a similar ability to previous findings and strategy disruption accounts of that of HC participants to benefit from the semantic organization provided by scrambled and blocked lists, suggest that increased organization according to pre- and furthermore, showed a similar PLC effect under existing semantic representations allows for increased these conditions. In contrast to the parallel improve- flexibility and automaticity at the item (word) level, yet within a more consistent hierarchical (categorical) from unrelated to scrambled recall in SCZ. A key framework both work to dprotectT from interference.
difference was our provision of labels and forced As reviewed, study of PLC with special popula- category recall, both known to facilitate FR ( tions and the underlying neural mechanisms is et al., 1997; Incisa della Rocchetta and Milner, 1993; limited. In contrast to enhanced interference in Roediger, 1978; Tulving and Pearlstone, 1966).
Together these studies show that SCZ participants can benefit from organization, but only when this 1993), a left-temporal/hippocampal group showed structure is explicitly provided at test, and support a utilization deficit in SCZ, where the cognitive and Milner, 1993) with organized lists. Our SCZ resources required to organize/maintain mnemonic results are most consistent with the latter, but particularly those from our unrelated condition.
Despite prefrontal and temporal contributions to This study is unique in concurrently assessing PLC across unrelated and categorized lists within one 2003; Weiss and Heckers, 2001), we replicated experiment, let alone within participants. Interference was most pronounced among HCs in recall of differential interference with organized lists. The unrelated compared to organized lists, consistent with opposing effects of PLC suggested above may account for this lack of overt difference given man, 1991). The ability to form relational associations combined frontal–temporal dysfunction in SCZ. An alternative functional–anatomic distinction is that between archicortical (e.g., dorsal–lateral prefrontal, provide some descapeT from interference. The similar hippocampus) and paleocortical (e.g., orbital–frontal, effects across scrambled and blocked conditions suggest that both groups employed similar categorical where preferential archicortical dysfunction is sup- representations to each other and to those intended.
The observed semantic intrusions, and their suscepti- the archicortical trend is associated with controlled, bility to interference, further demonstrate participants’ effortful, volitional, goal-directed behaviour as re- quired for maximizing FR scores and susceptibility to Marsh et al., 2004) and can be attributed to false PLC interference in the unrelated condition. Con- memories elicited by semantic processes at retrieval versely, the paleocortical trend functions in a more automatic fashion towards which the highly struc- unrelated recall in HCs is consistent with their use of tured, organized list conditions likely catered. This more idiosyncratic strategies (e.g., imagery, forming duality is consistent with dependence of PLC inter- FR and PLC effect with unrelated lists support the 1991), lack of interference on more automatic tasks B.K. Christensen et al. / Schizophrenia Research 85 (2006) 1–11 for their assistance with stimuli preparation, partici- familiarity-based gist retrieval versus conscious rec- pant recruitment/testing, and data management. Por- tions of this research were presented at the biennial meeting of the International Congress on Schizophre- The impetus for the current investigation was to nia Research, Savannah, GA, 2005. This research was examine strategic retrieval deficits unencumbered by a supported, in part, with a grant received from the difficulty confound. As predicted, this result was Canadian Psychiatric Research Foundation.
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