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Cognitive Neuropsychiatry Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/pcnp20
Verbatim recall in formal thought disorder in schizophrenia: a study of contextual influences a
ab
cd
Karen Dwyer , Emmanuelle Peters , Peter McKenna , Anthony David
be
fg
& Rosaleen McCarthy
a
Department of Psychology, King's College London, Institute of Psychiatry, London, UK b
National Institute for Health Research (NIHR) Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust, London, UK c
FIDMAG Research Foundation, Germanes Hospitalàries, Barcelona, Spain d
CIBERSAM, Madrid, Spain
e
Department of Psychosis Studies, King's College London, Institute of Psychiatry, London, UK f
Department of Psychology, University of Southampton, Southampton, UK g
Wessex Neurological Centre, Southampton General Hospital, Southampton University Hospital Trust, Tremona Road, Southampton, UK Published online: 13 Jan 2014.
To cite this article: Karen Dwyer, Emmanuelle Peters, Peter McKenna, Anthony David & Rosaleen McCarthy (2014) Verbatim recall in formal thought disorder in schizophrenia: a study of contextual influences, Cognitive Neuropsychiatry, 19:4, 337-358, DOI: 10.1080/13546805.2013.870069 To link to this article: http://dx.doi.org/10.1080/13546805.2013.870069
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Cognitive Neuropsychiatry, 2014 Vol. 19, No. 4, 337–358, http://dx.doi.org/10.1080/13546805.2013.870069
Verbatim recall in formal thought disorder in schizophrenia: a study of contextual influences Karen Dwyera, Emmanuelle Petersa,b*, Peter McKennac,d, Anthony Davidb,e and Rosaleen McCarthyf,g
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a
Department of Psychology, King’s College London, Institute of Psychiatry, London, UK; bNational Institute for Health Research (NIHR) Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust, London, UK; cFIDMAG Research Foundation, Germanes Hospitalàries, Barcelona, Spain; dCIBERSAM, Madrid, Spain; eDepartment of Psychosis Studies, King’s College London, Institute of Psychiatry, London, UK; fDepartment of Psychology, University of Southampton, Southampton, UK; gWessex Neurological Centre, Southampton General Hospital, Southampton University Hospital Trust, Tremona Road, Southampton, UK (Received 4 January 2013; accepted 25 November 2013) Introduction. We have previously reported that people with schizophrenia and formal thought disorder (FTD) were disproportionately impaired in recalling sentences verbatim and in judging their plausibility. We proposed that these deficits were due to impairment in integrating higher-order semantic information to construct a global whole. However, it is also possible that a lower-level linguistic problem affecting lexical activation could account for this pattern. Methods. The present study analysed and compared the sentence repetition errors produced by people with FTD, people with schizophrenia who were non-FTD and healthy controls. Errors due to failure of activation of the target lexical items were differentiated from those due to erroneous integration of information. Results. People with FTD produced significantly more unrelated lexical substitutions and omissions in their corpora than the other two groups, indicating an impairment of activation. In addition, they made significantly more erroneous contextual inferences and unrelated references, suggesting they were impaired in reconstructing the global whole from successfully activated items. Conclusion. These findings are consistent with a dual process account of impairments in FTD. Difficulties in repeating and judging sentence acceptability arises due to a combination of difficulty with activation and deficits in using linguistic context to process and produce speech. It is suggested that processing difficulties in FTD result from an impairment in using semantic context to drive lexical access and construction of a global whole. Keywords: formal thought disorder; schizophrenia; contextual processing; lexical activation
Language abnormalities affecting both production and comprehension have been consistently observed in schizophrenia. Formal thought disorder (FTD) is characterised by disrupted, illogical and incomprehensible speech, and is observed in approximately 16% of schizophrenia patients, with a further 40% exhibiting less severe symptoms in their spontaneous speech (Andreasen, 1979). The two main accounts of a language deficit
*Corresponding author. Email: [email protected] © 2014 Taylor & Francis
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in schizophrenia are of an abnormality in the structure and functioning of semantic memory, and of impairment in the use of linguistic context. The semantic activation hypothesis has been investigated using lexical decision in which a target stimulus is preceded by a “priming” word. Semantic activation is indexed by the relative facilitation of response speed when the prime is related to the target. Although the findings of these studies have been somewhat mixed, there appears to be evidence for stronger effects of semantic relatedness (hyper-priming) in FTD. Pomarol-Clotet, Oh, Laws, and McKenna (2008) carried out a meta-analysis of 36 studies concluding that patients with the symptom of FTD showed hyper-priming whereas unselected groups of people with schizophrenia did not show a reliable pattern of abnormality (e.g. Maher, Manschreck, Hoover, & Weisstein, 1987; Manschreck et al., 1988; Moritz et al., 2001; Spitzer, Braun, Hermle, & Maier, 1993). More fine-grain evaluation showed that FTD patients seemed to demonstrate a specific abnormality in the earlier or automatic stages of semantic activation: a disorder of access to semantics. Other studies have investigated the possibility of disorders of access to semantic memory via word retrieval techniques (e.g. confrontation naming, generating words belonging to designated semantic categories or beginning with specific letters). Patients with schizophrenia may demonstrate variable difficulties in which words are retrieved successfully on one occasion and are inaccessible on others (Allen, Liddle, & Frith, 1993; Vogel et al., 2009). This variability is consistent with an impairment in access to semantic knowledge rather than the loss of semantic representations themselves (Warrington & Shallice, 1979). Case studies of individual patients with FTD have also established variability in so far as words that can be retrieved or understood on one occasion are inaccessible on others (e.g., Laws, Kondel, & McKenna, 1999; Leeson, Laws, & McKenna, 2006). However, impaired lexical access cannot easily account for the disturbances in expression at the sentence and discourse levels that are also displayed in FTD. Speech at the sentence level may be disorganised despite intact word retrieval on confrontation naming tasks (Oh, McCarthy, & McKenna, 2002). At the sentence level, information governing word usage (the potential syntactic role of a lexeme and its combinatorial properties) may be impaired (Barrera, McKenna, & Berrios, 2005; Oh et al., 2002; Rodriguez-Ferrera, McCarthy, & McKenna, 2001). At a higher level, FTD patients are reported to use fewer cohesive ties between sentences (Rochester & Martin, 1979), display reduced cohesion (Allen & Allen, 1985; Harvey, 1983; Harvey & Brault, 1986; McPherson & Harvey, 1996) and show an increase in the use of ambiguous verbal references (Doherty, Schnur, & Harvey, 1988). Such studies demonstrate patients’ difficulty in mapping lexical features across multiple sentence elements within discourse, that is, a problem of the integration of semantic meaning. Receptive impairments in integrating contextual information at the level of the sentence and above have also been documented in schizophrenia (Salisbury, Shenton, Nestor, & McCarley, 2002). Patients’ interpretation of homophones and homographs may not be appropriately influenced by context (Sitnikova, Salisbury, Kuperberg, & Holcomb 2002; Titone, Levy, & Holzman, 2000). Electrophysiological studies have shown that while patients with schizophrenia may show a normal amplitude of the N400 (a wave form that reflects processing of semantic incongruity), when accessing meaning within a sentence, they may demonstrate a reduced amplitude of this component when required to build context over several sentences (Kuperberg, Sitnikova, Goff, & Holcomb, 2006) or to draw inferences that depend on contextual processing (Ditman & Kuperberg, 2008). The later P600 component, which is thought to arise when incongruous semantic and syntactic information is re-evaluated, may be reduced in its amplitude in schizophrenia (Kuperberg et al., 2006).
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Impaired processing of context has also been shown to be specific to FTD. Kuperberg, McGuire, and David (1998) found that compared to non-FTD patients and controls, FTD patients were less disrupted by semantic and pragmatic incongruity in detecting target words embedded in anomalous sentences. This finding was considered to reflect a lack of sensitivity to linguistic context. This work points to difficulties FTD patients have in the interpretation of the global whole to interpret the sentence under construction. Kuperberg, Kreher, and Ditman (2010) have proposed that in schizophrenia there is an imbalance between two strategies, namely an associative semantic memory–based analysis and an integrative process whereby information is combined and integrated in order to yield a complete combinatorial parse. While those with FTD had the greatest impairment, receptive deficits could also be documented in other patients with schizophrenia when demands were sufficiently great. In a previous study (Dwyer, David, McCarthy, McKenna, & Peters, 2013), we concurrently investigated comprehension and production in people with schizophrenia with and without FTD. We found that FTD patients, compared to both non-FTD patients and healthy controls, produced fewer correct plausibility judgments and less accurate verbatim recall, demonstrating concurrent impairments of comprehension and production. We also found that while the FTD group showed poorer comprehension, weaknesses emerged in the non-FTD patients as well, supporting the view of a continuum of context processing deficits in schizophrenia, compatible with Kuperberg et al.’s (2010) account. Aims This study extends our previous study by analysing the errors made by people with schizophrenia and healthy control participants in a test of verbatim sentence repetition. When participants attempt to reproduce sentences that are longer than their working memory spans, their reconstructions reflect the operation of their internal grammar and productive syntactic abilities (Potter & Lombardi, 1990). This technique potentially provides a window on the process of language production while specifying the target semantic content of the utterance and constraining the pragmatic element of communication. If an impairment of activation contributes to poor performance on this task, then we might expect to see errors in which targets were omitted or replaced by unrelated content. Impairments in reorganisation and reconstruction are likely to result in target items being inappropriately organised into a global whole. We predicted that FTD patients would make more errors consistent with problems in lexical activation and would also produce more responses that indicated impairment in contextual processing (i.e. failures to reorganise lexical items into a global structure). There should be no significant difference between patients with and without FTD and healthy controls on those errors in which the original meaning was maintained (i.e. when the target was replaced by a synonym, or a substituted item that was related to the target, or where the response demonstrated the operation of contextual inferences and the participant made use of appropriate referencing devices). Method Participants Thirty-two patients with a diagnosis of schizophrenia, based on Diagnostic and Statistical Manual of Mental Disorders, 4th Edition (DSM-IV) (American Psychiatric Association, 1994) criteria, were recruited from the inpatient wards in the South London and Maudsley
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NHS Foundation Trust (SLaM), and from Fulbourn Hospital, Cambridge. All participants were chronic patients despite being stable on neuroleptic medication for between 4 months and 5 years (average 3.9 years). Positive FTD and poverty of speech were assessed with the version of Andreasen’s Thought, Language and Communication (TLC) scale in the Comprehensive Assessment of Symptoms and History (CASH) (Andreasen, Flaum, & Arndt, 1992). All recorded interviews were rated by a separate author (P.J.M), a senior clinician with extensive experience of schizophrenia. Those with a summative CASH score of 3, 4 or 5 (moderate, marked or severe FTD) were assigned to the FTD group (N = 14). Participants receiving a global score of less than or equal to 2 were allocated to the non-FTD group (N = 18). Each patient’s symptomatology was rated using the Scale for the Assessment of Positive Symptoms (SAPS; Andreasen, 1984). The scores for the hallucinations, delusions and bizarre behaviour were scored collectively under positive symptoms and the maximum score was 5, representing higher levels of symptoms. Scores for FTD were entered separately and the maximum score was also 5. Interviews were recorded at the time of testing. Fifteen healthy control participants were also recruited from the Camberwell job centre in London and others from administrative posts at University College London. Inclusion criteria were native British speakers, aged between 18 and 65 years, and exclusion criteria were a history of head injury or recent substance abuse or dependence. Estimated pre-morbid IQ was measured using the National Adult Reading Test (NART; Nelson, 1982) and current IQ for patient groups using the Wechsler Adult Intelligence Scales Revised (WAIS-R; Wechsler, 1981). Working memory function was assessed using the WAIS-III (Wechsler, 1997) forward digit span task and letter-tonumber span tasks. The three groups were matched for age and there was no difference between the patients groups on the NART-estimated pre-morbid IQ, or on the forward digit span measure of working memory function although there was a significant difference between the FTD patients and healthy controls on letter-to-number span scores. The two patient groups did not differ on current IQ or on global scores for delusions of hallucinations in the SAPS; they did however differ significantly on global scores for FTD. Demographic details of the patients and healthy controls are shown in Table 1. Procedures A sense judgement task and a verbatim recall task were used to assess comprehension and production of the same materials. Participants were asked to listen to pairs of sentences, and after each pair, to (1) make a judgement about the semantic plausibility of the sentence pair, and then (2) to repeat the sentence pair verbatim. All responses were recorded on an Olympus DM-20 dictaphone and later transcribed for error analyses. Participants were tested in two or three sessions, each lasting approximately 40 to 60 minutes. The order of administration of tasks was counterbalanced across participants and across conditions. Stimuli The task stimuli were adapted from Almor, Kempler, MacDonald, Andersen, and Tyler, (1999) and consisted of pairs of spoken sentences. The first sentence introduced two entities, one singular and one plural, for example, “the children loved the silly clown at the party”. The second sentence incorporated one of the entities in the first sentence as a synonymous noun phrase, and the other as a pronoun, for example, “during the
Gender (M/F) Age (years) NART estimated IQ mean (SD) Working memory (summed from both conditions) mean (SD) Letter-to-number mean (SD) Forward digit span Mean (SD) SAPS positive symptoms (without FTD) mean (SD) Thought disorder mean (SD) WAIS-R mean (SD)
Healthy controls (n = 15)
non-FTD patients (n = 18)
FTD patients (n = 14)
Tests of significance
9/6 35.9 (14.77) 103.51 (9.41) 20.47 (6.96) 11.47 (3.87) 9.17 (3.42) – – –
14/4 37.5 (10.16) 113.72 (9.09) 18.94 (5.70) 9.67 (2.93) 8.5 (2.03) 1.71 0.00 98 (12.93)
10/4 41 (12.6) 112.93 (11.24) 16.29 (5.05) 8.5 (2.6) 7.00 (1.66) 2.43 3.57 (0.85) 94.36 (8.85)
χ2 = 2.63, df = (2), p = .304 F(2,45)= .63, p = .54 F(2,44) = 5.2, p = .01b*c* F(2,44) = 1.82, p = .17 F(2,44) = 3.22, p = .05b* F(2,44) = 2.9, p = .07 (t = 1.49, p = .46) (t = 18.8, p < .001) (t =−.90, p = .22)
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Table 1. Demographics characteristics of the three groups.
Note: LSD Least significant difference test: a – FTD patients versus non-FTD patients; b – FTD patients versus healthy controls; c – non-FTD patients versus healthy controls (*p < 0.05).
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performance the jester threw them candy”. The position of synonyms, pronouns and antecedents was not predictable. There were 64 sentence pairs appearing in four forms varying in their plausibility. In half of the plausible forms, the synonym in the second sentence referred back to the object of the first and the pronoun referred back to the subject (e.g. The tourists listened to the safari guide on the long trip. During the dull parts, the rep really tried to entertain them.). In the remainder, the synonym referred to the subject and the pronoun to the object (e.g. The careers adviser questioned the job seekers about work. Mostly, the employment officer found them something.). There were two types of incongruous sentence. The first type was incongruous syntactic agreement in which either the synonym or the pronoun was incongruous with the preceding sentence (e.g. The children loved the silly clown at the party. During the performance, the jester threw sweets to him.). The second type of incongruity was semantic. The second sentence was semantically implausible when taking into account the relationships between the subject and the object in the first (e.g. The trainer told the footballers not to tackle so hard. But unfortunately, he couldn’t hear the players.). Sentence pairs were randomised and appeared in their appropriate forms in the first block of 16 items and as an inappropriate form in a second set of 16 (with an equal number of agreement and semantically incongruous forms). There were 32 sentence pairs in each condition, making a total of 64 items. Two versions of each sentence pair were presented in conditions intended to manipulate emotional salience, making a total of 128 sentence pairs per participant. Scoring A preliminary qualitative linguistic analysis established that errors could be divided into two main categories: Omissions and Deviations. Deviation errors were further subdivided into Context Appropriate and Context Inappropriate subtypes. The development of these categories with example errors is presented in Appendix 1. The overall classification of errors is presented in Table 2. Responses were transcribed, and scored by three linguists (including the first author). Two of the raters were blind to the group from which the responses were taken. Raters scored across groups and did not score all responses for any given participant. Each response was mapped onto its target structure. Each deviation from the target at the phrase or word level was scored as an error. When participants generated additional content, their response was scored as an intrusion; when phrases and lexical items were not maintained in the response they were scored as omissions. In order to capture the complexity of the data, individual multi-word responses could be scored as containing more than one error; however, only one error type was allocated to each error and there were no cases in which the same error was counted twice. For example Target sentence: The fortune-teller told the newlyweds about their future. During the reading, the psychic worried them. Response: The fortune-teller told the readers about secret. During the reading, the psychic enlightened them.
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Table 2. Classification of the errors types. Error classification Omissions Lexical omissions
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Makeshift fillers
Error description Failure to recall the lexical target.
Filler expressions such as “something”, “someone”, “somewhere”.
Context appropriate References Accurate use of a pronominal form replacing an NP, or vice versa. Synonyms Use of a synonymous phrase to represent the target accurately. Target-related A non-synonymous item that shares substitutions sufficient features to maintain the overall message of the target item. Contextual A synonymous substitution of the inferences target information based on contextual interpretation. Context inappropriate Unrelated The replacement of a target item with substitutions a semantically unrelated item. Intrusions Additional information that is not contained in the target.
Erroneous inferences Unrelated references
Target information is used elsewhere in the response structure to reconstruct a novel interpretation. Use of a pronoun whose antecedent cannot be established from context.
Example T: After the show, he praised the performers. R: After, he praised the performers. T: The customer generously tipped the staff. R: The customer something something. T: The panel intimidated them. R: They intimidated them. T: the interviewee. R: the candidate. T: …the school principal. R: …the teacher. T: The children asked the childminder for a bedtime story. Afterwards, they kissed the babysitter. R: … they kissed the reader. T: The theatre critic watched… R: The tourists worked… T: The theatre critic watched the performance on the opening night. After the show the performers praised him. R: There’s a Christmas performance. T: The demanding guests nagged the maid… R: The nagger woman was… T: Lady Thomas was extremely cruel to her maids… In fact, she actually bullied the servants. R: She led him.
Note: T indicates the target sentence that the participants were presented, while R indicates the response that was provided.
There were three errors allocated to the response (shown by underlining). Each error was then sub-classified according to a scheme that had been established on the basis of preliminary qualitative review. Inter-rater agreement was established by using a random subset of 80 responses that were scored by each of the three markers; each marker scored the full 80 sentence pairs (a total of 160 sentences) so that each of the 80 sentence pairs in the subset was scored three times, and their ratings were then moderated to ensure agreement was reached on categories of analysis. This achieved inter-rater agreement of 89%.
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Results There were no main effects of the emotional salience manipulation and hence the data were combined across these conditions (see Dwyer et al., 2013). The error analysis was carried out hierarchically with the broadest level of classification followed by successively finer-grain comparisons. There was a significant difference between groups in total errors [F(2,43) = 11.26, p < .001; effect size (g2p ¼ .33)]; the FTD group made a mean of 264.5 (SD = 83.1) errors, while the non-FTD patients made 175.2 (SD = 67.7) errors and the healthy controls produced an average of 120.9 (SD = 55.2) errors. LSD post hoc analysis showed that while the FTD group produced significantly more errors than both non-FTD patients (p < .001) and the healthy controls (p < .001), both with large effect sizes (d = 1.18 and d = 2.08 respectively), the non-FTD patients did not differ from healthy controls (p = .28) with a large effect size (d = 0.9). There was also a significant effect of working memory [F(1,43) = 6.830, p < .05; effect size (g2p ¼ .14)]. There was no effect of stimulus plausibility [F(1,43) = 1.11, p = .3; (g2p ¼ .03)] or any interaction between group and plausibility [F(2,43) = 0.11, p = .9; (g2p ¼ .01)], demonstrating that the plausibility of the sentence pairs did not impact any of the three groups error rates in the regeneration of structure. Error subtypes The distribution of errors made by the three groups is shown in Figure 1. Considering the contrast between errors with additional information (Deviation Errors) and those where information was lost (Omissions), there were significantly more Deviations than Omissions [F(1,43) = 18.97, p < .001; (g2p ¼ .31)] but there was no interaction between the Omission/Deviation variable and group [F(2,43) = .05, p = .95; (g2p ¼ .002)]. There was no interaction between working memory and Omission/Deviation errors [F(1,43) = .927, p = .34; (g2p ¼ .02)] (see Figure 2a). Context appropriate vs. Context inappropriate errors Deviation errors showed a graded main effect of group [F(2,43) = 3.65, p < .03] with most Deviation Errors being made by the FTD patients, fewer by the non-FTD group and 160 140 120 100 FTD non-FTD Healthy controls
80 60 40 20 0 Omissions
Figure 1.
Deviations
Total errors scores produced by the three groups.
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(a)
140 120 100 FTD non-FTD Healthy controls
80 60 40 20
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0 Omissions 100 90
Deviations
(b)
80 70 60 FTD patients non-FTD patients Healthy controls
50 40 30 20 10 0 Context Appropriate
Context Inappropriate
Figure 2. (a) Error rate on Omissions and Deviations across the three groups. (b) Error rate on Context Appropriate and Context Inappropriate errors across the three groups.
least by the healthy controls [FTD vs. non-FTD: F(1,29) = 11.94, p < .001; (g2p ¼ .29); FTD vs. healthy controls: F(1,26) = 52.53, p < .001; (g2p ¼ .67)]. The non-FTD patients were worse that the healthy controls [F(1,26) = 12.05, p < .001; (g2p ¼ .29)]. Working memory was just short of significance [F(1,43) = 3.36, p = .07; (g2p ¼ .07)]. Deviation errors were further subdivided into Context Inappropriate and Context Appropriate subtypes. Context Inappropriate errors were those where no relationship could be established between the target and the response (considering both the level of the word and in relation to the larger structure). There was a highly significant interaction between Context Appropriate and Context Inappropriate errors and group [F(1,41) = 21.93, p < .001], with a large effect size (g2p ¼ .51) (see Figure 2b). While the three groups were indistinguishable on Context Appropriate errors, they differed strikingly on the Context Inappropriate subset. The FTD group produced nearly 35% more Context Inappropriate errors than Context Appropriate errors whereas the healthy controls made 34% fewer (both ps .95). However, Context Inappropriate errors were associated with comprehension (r = .514, p < .01) with Unrelated Substitutions and Erroneous Contextual Inferences being the most strongly related to comprehension (r = .525 and r = .523 respectively, p < .001). Unrelated References and Intrusions were also associated but to a slightly weaker extent (r = .33 and r = .396; p < .01). A further analysis of the errors in repetition was undertaken on those sentences that had been correctly comprehended in order to determine whether poor performance on verbatim repetition was attributable to poor comprehension. This analysis did not yield any different results from the data-set as a whole. Deviation errors were still more common than Omissions [F(1,43) = 15.41, p < .001; (g2p ¼ .26)] and there was no interaction of Omission/Deviation and group [F(2,43) = .044, p .96; (g2p ¼ .002)] or any
Omissions Lexical omissions Makeshift fillers Context appropriate Synonyms Target-related substitutions Contextual inferences References Context inappropriate Unrelated substitutions Erroneous inferences Unrelated reference Intrusions
Healthy controls (n = 15) Mean (SD)
non-FTD patients (n = 18) Mean (SD)
FTD patients (n = 14) Mean (SD)
ANCOVAs F(df = 2,43)
pa
26.47 (16.1) 1.93 (2.6)
42.48 (23.2) 0.92 (1.16)
80.07 (35.7) 2.50 (3.4)
12.67 2.42
Cognitive Neuropsychiatry Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/pcnp20
Verbatim recall in formal thought disorder in schizophrenia: a study of contextual influences a
ab
cd
Karen Dwyer , Emmanuelle Peters , Peter McKenna , Anthony David
be
fg
& Rosaleen McCarthy
a
Department of Psychology, King's College London, Institute of Psychiatry, London, UK b
National Institute for Health Research (NIHR) Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust, London, UK c
FIDMAG Research Foundation, Germanes Hospitalàries, Barcelona, Spain d
CIBERSAM, Madrid, Spain
e
Department of Psychosis Studies, King's College London, Institute of Psychiatry, London, UK f
Department of Psychology, University of Southampton, Southampton, UK g
Wessex Neurological Centre, Southampton General Hospital, Southampton University Hospital Trust, Tremona Road, Southampton, UK Published online: 13 Jan 2014.
To cite this article: Karen Dwyer, Emmanuelle Peters, Peter McKenna, Anthony David & Rosaleen McCarthy (2014) Verbatim recall in formal thought disorder in schizophrenia: a study of contextual influences, Cognitive Neuropsychiatry, 19:4, 337-358, DOI: 10.1080/13546805.2013.870069 To link to this article: http://dx.doi.org/10.1080/13546805.2013.870069
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content
should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/termsand-conditions
Cognitive Neuropsychiatry, 2014 Vol. 19, No. 4, 337–358, http://dx.doi.org/10.1080/13546805.2013.870069
Verbatim recall in formal thought disorder in schizophrenia: a study of contextual influences Karen Dwyera, Emmanuelle Petersa,b*, Peter McKennac,d, Anthony Davidb,e and Rosaleen McCarthyf,g
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a
Department of Psychology, King’s College London, Institute of Psychiatry, London, UK; bNational Institute for Health Research (NIHR) Biomedical Research Centre for Mental Health at South London and Maudsley NHS Foundation Trust, London, UK; cFIDMAG Research Foundation, Germanes Hospitalàries, Barcelona, Spain; dCIBERSAM, Madrid, Spain; eDepartment of Psychosis Studies, King’s College London, Institute of Psychiatry, London, UK; fDepartment of Psychology, University of Southampton, Southampton, UK; gWessex Neurological Centre, Southampton General Hospital, Southampton University Hospital Trust, Tremona Road, Southampton, UK (Received 4 January 2013; accepted 25 November 2013) Introduction. We have previously reported that people with schizophrenia and formal thought disorder (FTD) were disproportionately impaired in recalling sentences verbatim and in judging their plausibility. We proposed that these deficits were due to impairment in integrating higher-order semantic information to construct a global whole. However, it is also possible that a lower-level linguistic problem affecting lexical activation could account for this pattern. Methods. The present study analysed and compared the sentence repetition errors produced by people with FTD, people with schizophrenia who were non-FTD and healthy controls. Errors due to failure of activation of the target lexical items were differentiated from those due to erroneous integration of information. Results. People with FTD produced significantly more unrelated lexical substitutions and omissions in their corpora than the other two groups, indicating an impairment of activation. In addition, they made significantly more erroneous contextual inferences and unrelated references, suggesting they were impaired in reconstructing the global whole from successfully activated items. Conclusion. These findings are consistent with a dual process account of impairments in FTD. Difficulties in repeating and judging sentence acceptability arises due to a combination of difficulty with activation and deficits in using linguistic context to process and produce speech. It is suggested that processing difficulties in FTD result from an impairment in using semantic context to drive lexical access and construction of a global whole. Keywords: formal thought disorder; schizophrenia; contextual processing; lexical activation
Language abnormalities affecting both production and comprehension have been consistently observed in schizophrenia. Formal thought disorder (FTD) is characterised by disrupted, illogical and incomprehensible speech, and is observed in approximately 16% of schizophrenia patients, with a further 40% exhibiting less severe symptoms in their spontaneous speech (Andreasen, 1979). The two main accounts of a language deficit
*Corresponding author. Email: [email protected] © 2014 Taylor & Francis
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in schizophrenia are of an abnormality in the structure and functioning of semantic memory, and of impairment in the use of linguistic context. The semantic activation hypothesis has been investigated using lexical decision in which a target stimulus is preceded by a “priming” word. Semantic activation is indexed by the relative facilitation of response speed when the prime is related to the target. Although the findings of these studies have been somewhat mixed, there appears to be evidence for stronger effects of semantic relatedness (hyper-priming) in FTD. Pomarol-Clotet, Oh, Laws, and McKenna (2008) carried out a meta-analysis of 36 studies concluding that patients with the symptom of FTD showed hyper-priming whereas unselected groups of people with schizophrenia did not show a reliable pattern of abnormality (e.g. Maher, Manschreck, Hoover, & Weisstein, 1987; Manschreck et al., 1988; Moritz et al., 2001; Spitzer, Braun, Hermle, & Maier, 1993). More fine-grain evaluation showed that FTD patients seemed to demonstrate a specific abnormality in the earlier or automatic stages of semantic activation: a disorder of access to semantics. Other studies have investigated the possibility of disorders of access to semantic memory via word retrieval techniques (e.g. confrontation naming, generating words belonging to designated semantic categories or beginning with specific letters). Patients with schizophrenia may demonstrate variable difficulties in which words are retrieved successfully on one occasion and are inaccessible on others (Allen, Liddle, & Frith, 1993; Vogel et al., 2009). This variability is consistent with an impairment in access to semantic knowledge rather than the loss of semantic representations themselves (Warrington & Shallice, 1979). Case studies of individual patients with FTD have also established variability in so far as words that can be retrieved or understood on one occasion are inaccessible on others (e.g., Laws, Kondel, & McKenna, 1999; Leeson, Laws, & McKenna, 2006). However, impaired lexical access cannot easily account for the disturbances in expression at the sentence and discourse levels that are also displayed in FTD. Speech at the sentence level may be disorganised despite intact word retrieval on confrontation naming tasks (Oh, McCarthy, & McKenna, 2002). At the sentence level, information governing word usage (the potential syntactic role of a lexeme and its combinatorial properties) may be impaired (Barrera, McKenna, & Berrios, 2005; Oh et al., 2002; Rodriguez-Ferrera, McCarthy, & McKenna, 2001). At a higher level, FTD patients are reported to use fewer cohesive ties between sentences (Rochester & Martin, 1979), display reduced cohesion (Allen & Allen, 1985; Harvey, 1983; Harvey & Brault, 1986; McPherson & Harvey, 1996) and show an increase in the use of ambiguous verbal references (Doherty, Schnur, & Harvey, 1988). Such studies demonstrate patients’ difficulty in mapping lexical features across multiple sentence elements within discourse, that is, a problem of the integration of semantic meaning. Receptive impairments in integrating contextual information at the level of the sentence and above have also been documented in schizophrenia (Salisbury, Shenton, Nestor, & McCarley, 2002). Patients’ interpretation of homophones and homographs may not be appropriately influenced by context (Sitnikova, Salisbury, Kuperberg, & Holcomb 2002; Titone, Levy, & Holzman, 2000). Electrophysiological studies have shown that while patients with schizophrenia may show a normal amplitude of the N400 (a wave form that reflects processing of semantic incongruity), when accessing meaning within a sentence, they may demonstrate a reduced amplitude of this component when required to build context over several sentences (Kuperberg, Sitnikova, Goff, & Holcomb, 2006) or to draw inferences that depend on contextual processing (Ditman & Kuperberg, 2008). The later P600 component, which is thought to arise when incongruous semantic and syntactic information is re-evaluated, may be reduced in its amplitude in schizophrenia (Kuperberg et al., 2006).
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Impaired processing of context has also been shown to be specific to FTD. Kuperberg, McGuire, and David (1998) found that compared to non-FTD patients and controls, FTD patients were less disrupted by semantic and pragmatic incongruity in detecting target words embedded in anomalous sentences. This finding was considered to reflect a lack of sensitivity to linguistic context. This work points to difficulties FTD patients have in the interpretation of the global whole to interpret the sentence under construction. Kuperberg, Kreher, and Ditman (2010) have proposed that in schizophrenia there is an imbalance between two strategies, namely an associative semantic memory–based analysis and an integrative process whereby information is combined and integrated in order to yield a complete combinatorial parse. While those with FTD had the greatest impairment, receptive deficits could also be documented in other patients with schizophrenia when demands were sufficiently great. In a previous study (Dwyer, David, McCarthy, McKenna, & Peters, 2013), we concurrently investigated comprehension and production in people with schizophrenia with and without FTD. We found that FTD patients, compared to both non-FTD patients and healthy controls, produced fewer correct plausibility judgments and less accurate verbatim recall, demonstrating concurrent impairments of comprehension and production. We also found that while the FTD group showed poorer comprehension, weaknesses emerged in the non-FTD patients as well, supporting the view of a continuum of context processing deficits in schizophrenia, compatible with Kuperberg et al.’s (2010) account. Aims This study extends our previous study by analysing the errors made by people with schizophrenia and healthy control participants in a test of verbatim sentence repetition. When participants attempt to reproduce sentences that are longer than their working memory spans, their reconstructions reflect the operation of their internal grammar and productive syntactic abilities (Potter & Lombardi, 1990). This technique potentially provides a window on the process of language production while specifying the target semantic content of the utterance and constraining the pragmatic element of communication. If an impairment of activation contributes to poor performance on this task, then we might expect to see errors in which targets were omitted or replaced by unrelated content. Impairments in reorganisation and reconstruction are likely to result in target items being inappropriately organised into a global whole. We predicted that FTD patients would make more errors consistent with problems in lexical activation and would also produce more responses that indicated impairment in contextual processing (i.e. failures to reorganise lexical items into a global structure). There should be no significant difference between patients with and without FTD and healthy controls on those errors in which the original meaning was maintained (i.e. when the target was replaced by a synonym, or a substituted item that was related to the target, or where the response demonstrated the operation of contextual inferences and the participant made use of appropriate referencing devices). Method Participants Thirty-two patients with a diagnosis of schizophrenia, based on Diagnostic and Statistical Manual of Mental Disorders, 4th Edition (DSM-IV) (American Psychiatric Association, 1994) criteria, were recruited from the inpatient wards in the South London and Maudsley
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NHS Foundation Trust (SLaM), and from Fulbourn Hospital, Cambridge. All participants were chronic patients despite being stable on neuroleptic medication for between 4 months and 5 years (average 3.9 years). Positive FTD and poverty of speech were assessed with the version of Andreasen’s Thought, Language and Communication (TLC) scale in the Comprehensive Assessment of Symptoms and History (CASH) (Andreasen, Flaum, & Arndt, 1992). All recorded interviews were rated by a separate author (P.J.M), a senior clinician with extensive experience of schizophrenia. Those with a summative CASH score of 3, 4 or 5 (moderate, marked or severe FTD) were assigned to the FTD group (N = 14). Participants receiving a global score of less than or equal to 2 were allocated to the non-FTD group (N = 18). Each patient’s symptomatology was rated using the Scale for the Assessment of Positive Symptoms (SAPS; Andreasen, 1984). The scores for the hallucinations, delusions and bizarre behaviour were scored collectively under positive symptoms and the maximum score was 5, representing higher levels of symptoms. Scores for FTD were entered separately and the maximum score was also 5. Interviews were recorded at the time of testing. Fifteen healthy control participants were also recruited from the Camberwell job centre in London and others from administrative posts at University College London. Inclusion criteria were native British speakers, aged between 18 and 65 years, and exclusion criteria were a history of head injury or recent substance abuse or dependence. Estimated pre-morbid IQ was measured using the National Adult Reading Test (NART; Nelson, 1982) and current IQ for patient groups using the Wechsler Adult Intelligence Scales Revised (WAIS-R; Wechsler, 1981). Working memory function was assessed using the WAIS-III (Wechsler, 1997) forward digit span task and letter-tonumber span tasks. The three groups were matched for age and there was no difference between the patients groups on the NART-estimated pre-morbid IQ, or on the forward digit span measure of working memory function although there was a significant difference between the FTD patients and healthy controls on letter-to-number span scores. The two patient groups did not differ on current IQ or on global scores for delusions of hallucinations in the SAPS; they did however differ significantly on global scores for FTD. Demographic details of the patients and healthy controls are shown in Table 1. Procedures A sense judgement task and a verbatim recall task were used to assess comprehension and production of the same materials. Participants were asked to listen to pairs of sentences, and after each pair, to (1) make a judgement about the semantic plausibility of the sentence pair, and then (2) to repeat the sentence pair verbatim. All responses were recorded on an Olympus DM-20 dictaphone and later transcribed for error analyses. Participants were tested in two or three sessions, each lasting approximately 40 to 60 minutes. The order of administration of tasks was counterbalanced across participants and across conditions. Stimuli The task stimuli were adapted from Almor, Kempler, MacDonald, Andersen, and Tyler, (1999) and consisted of pairs of spoken sentences. The first sentence introduced two entities, one singular and one plural, for example, “the children loved the silly clown at the party”. The second sentence incorporated one of the entities in the first sentence as a synonymous noun phrase, and the other as a pronoun, for example, “during the
Gender (M/F) Age (years) NART estimated IQ mean (SD) Working memory (summed from both conditions) mean (SD) Letter-to-number mean (SD) Forward digit span Mean (SD) SAPS positive symptoms (without FTD) mean (SD) Thought disorder mean (SD) WAIS-R mean (SD)
Healthy controls (n = 15)
non-FTD patients (n = 18)
FTD patients (n = 14)
Tests of significance
9/6 35.9 (14.77) 103.51 (9.41) 20.47 (6.96) 11.47 (3.87) 9.17 (3.42) – – –
14/4 37.5 (10.16) 113.72 (9.09) 18.94 (5.70) 9.67 (2.93) 8.5 (2.03) 1.71 0.00 98 (12.93)
10/4 41 (12.6) 112.93 (11.24) 16.29 (5.05) 8.5 (2.6) 7.00 (1.66) 2.43 3.57 (0.85) 94.36 (8.85)
χ2 = 2.63, df = (2), p = .304 F(2,45)= .63, p = .54 F(2,44) = 5.2, p = .01b*c* F(2,44) = 1.82, p = .17 F(2,44) = 3.22, p = .05b* F(2,44) = 2.9, p = .07 (t = 1.49, p = .46) (t = 18.8, p < .001) (t =−.90, p = .22)
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Table 1. Demographics characteristics of the three groups.
Note: LSD Least significant difference test: a – FTD patients versus non-FTD patients; b – FTD patients versus healthy controls; c – non-FTD patients versus healthy controls (*p < 0.05).
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performance the jester threw them candy”. The position of synonyms, pronouns and antecedents was not predictable. There were 64 sentence pairs appearing in four forms varying in their plausibility. In half of the plausible forms, the synonym in the second sentence referred back to the object of the first and the pronoun referred back to the subject (e.g. The tourists listened to the safari guide on the long trip. During the dull parts, the rep really tried to entertain them.). In the remainder, the synonym referred to the subject and the pronoun to the object (e.g. The careers adviser questioned the job seekers about work. Mostly, the employment officer found them something.). There were two types of incongruous sentence. The first type was incongruous syntactic agreement in which either the synonym or the pronoun was incongruous with the preceding sentence (e.g. The children loved the silly clown at the party. During the performance, the jester threw sweets to him.). The second type of incongruity was semantic. The second sentence was semantically implausible when taking into account the relationships between the subject and the object in the first (e.g. The trainer told the footballers not to tackle so hard. But unfortunately, he couldn’t hear the players.). Sentence pairs were randomised and appeared in their appropriate forms in the first block of 16 items and as an inappropriate form in a second set of 16 (with an equal number of agreement and semantically incongruous forms). There were 32 sentence pairs in each condition, making a total of 64 items. Two versions of each sentence pair were presented in conditions intended to manipulate emotional salience, making a total of 128 sentence pairs per participant. Scoring A preliminary qualitative linguistic analysis established that errors could be divided into two main categories: Omissions and Deviations. Deviation errors were further subdivided into Context Appropriate and Context Inappropriate subtypes. The development of these categories with example errors is presented in Appendix 1. The overall classification of errors is presented in Table 2. Responses were transcribed, and scored by three linguists (including the first author). Two of the raters were blind to the group from which the responses were taken. Raters scored across groups and did not score all responses for any given participant. Each response was mapped onto its target structure. Each deviation from the target at the phrase or word level was scored as an error. When participants generated additional content, their response was scored as an intrusion; when phrases and lexical items were not maintained in the response they were scored as omissions. In order to capture the complexity of the data, individual multi-word responses could be scored as containing more than one error; however, only one error type was allocated to each error and there were no cases in which the same error was counted twice. For example Target sentence: The fortune-teller told the newlyweds about their future. During the reading, the psychic worried them. Response: The fortune-teller told the readers about secret. During the reading, the psychic enlightened them.
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Table 2. Classification of the errors types. Error classification Omissions Lexical omissions
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Makeshift fillers
Error description Failure to recall the lexical target.
Filler expressions such as “something”, “someone”, “somewhere”.
Context appropriate References Accurate use of a pronominal form replacing an NP, or vice versa. Synonyms Use of a synonymous phrase to represent the target accurately. Target-related A non-synonymous item that shares substitutions sufficient features to maintain the overall message of the target item. Contextual A synonymous substitution of the inferences target information based on contextual interpretation. Context inappropriate Unrelated The replacement of a target item with substitutions a semantically unrelated item. Intrusions Additional information that is not contained in the target.
Erroneous inferences Unrelated references
Target information is used elsewhere in the response structure to reconstruct a novel interpretation. Use of a pronoun whose antecedent cannot be established from context.
Example T: After the show, he praised the performers. R: After, he praised the performers. T: The customer generously tipped the staff. R: The customer something something. T: The panel intimidated them. R: They intimidated them. T: the interviewee. R: the candidate. T: …the school principal. R: …the teacher. T: The children asked the childminder for a bedtime story. Afterwards, they kissed the babysitter. R: … they kissed the reader. T: The theatre critic watched… R: The tourists worked… T: The theatre critic watched the performance on the opening night. After the show the performers praised him. R: There’s a Christmas performance. T: The demanding guests nagged the maid… R: The nagger woman was… T: Lady Thomas was extremely cruel to her maids… In fact, she actually bullied the servants. R: She led him.
Note: T indicates the target sentence that the participants were presented, while R indicates the response that was provided.
There were three errors allocated to the response (shown by underlining). Each error was then sub-classified according to a scheme that had been established on the basis of preliminary qualitative review. Inter-rater agreement was established by using a random subset of 80 responses that were scored by each of the three markers; each marker scored the full 80 sentence pairs (a total of 160 sentences) so that each of the 80 sentence pairs in the subset was scored three times, and their ratings were then moderated to ensure agreement was reached on categories of analysis. This achieved inter-rater agreement of 89%.
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Results There were no main effects of the emotional salience manipulation and hence the data were combined across these conditions (see Dwyer et al., 2013). The error analysis was carried out hierarchically with the broadest level of classification followed by successively finer-grain comparisons. There was a significant difference between groups in total errors [F(2,43) = 11.26, p < .001; effect size (g2p ¼ .33)]; the FTD group made a mean of 264.5 (SD = 83.1) errors, while the non-FTD patients made 175.2 (SD = 67.7) errors and the healthy controls produced an average of 120.9 (SD = 55.2) errors. LSD post hoc analysis showed that while the FTD group produced significantly more errors than both non-FTD patients (p < .001) and the healthy controls (p < .001), both with large effect sizes (d = 1.18 and d = 2.08 respectively), the non-FTD patients did not differ from healthy controls (p = .28) with a large effect size (d = 0.9). There was also a significant effect of working memory [F(1,43) = 6.830, p < .05; effect size (g2p ¼ .14)]. There was no effect of stimulus plausibility [F(1,43) = 1.11, p = .3; (g2p ¼ .03)] or any interaction between group and plausibility [F(2,43) = 0.11, p = .9; (g2p ¼ .01)], demonstrating that the plausibility of the sentence pairs did not impact any of the three groups error rates in the regeneration of structure. Error subtypes The distribution of errors made by the three groups is shown in Figure 1. Considering the contrast between errors with additional information (Deviation Errors) and those where information was lost (Omissions), there were significantly more Deviations than Omissions [F(1,43) = 18.97, p < .001; (g2p ¼ .31)] but there was no interaction between the Omission/Deviation variable and group [F(2,43) = .05, p = .95; (g2p ¼ .002)]. There was no interaction between working memory and Omission/Deviation errors [F(1,43) = .927, p = .34; (g2p ¼ .02)] (see Figure 2a). Context appropriate vs. Context inappropriate errors Deviation errors showed a graded main effect of group [F(2,43) = 3.65, p < .03] with most Deviation Errors being made by the FTD patients, fewer by the non-FTD group and 160 140 120 100 FTD non-FTD Healthy controls
80 60 40 20 0 Omissions
Figure 1.
Deviations
Total errors scores produced by the three groups.
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(a)
140 120 100 FTD non-FTD Healthy controls
80 60 40 20
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0 Omissions 100 90
Deviations
(b)
80 70 60 FTD patients non-FTD patients Healthy controls
50 40 30 20 10 0 Context Appropriate
Context Inappropriate
Figure 2. (a) Error rate on Omissions and Deviations across the three groups. (b) Error rate on Context Appropriate and Context Inappropriate errors across the three groups.
least by the healthy controls [FTD vs. non-FTD: F(1,29) = 11.94, p < .001; (g2p ¼ .29); FTD vs. healthy controls: F(1,26) = 52.53, p < .001; (g2p ¼ .67)]. The non-FTD patients were worse that the healthy controls [F(1,26) = 12.05, p < .001; (g2p ¼ .29)]. Working memory was just short of significance [F(1,43) = 3.36, p = .07; (g2p ¼ .07)]. Deviation errors were further subdivided into Context Inappropriate and Context Appropriate subtypes. Context Inappropriate errors were those where no relationship could be established between the target and the response (considering both the level of the word and in relation to the larger structure). There was a highly significant interaction between Context Appropriate and Context Inappropriate errors and group [F(1,41) = 21.93, p < .001], with a large effect size (g2p ¼ .51) (see Figure 2b). While the three groups were indistinguishable on Context Appropriate errors, they differed strikingly on the Context Inappropriate subset. The FTD group produced nearly 35% more Context Inappropriate errors than Context Appropriate errors whereas the healthy controls made 34% fewer (both ps .95). However, Context Inappropriate errors were associated with comprehension (r = .514, p < .01) with Unrelated Substitutions and Erroneous Contextual Inferences being the most strongly related to comprehension (r = .525 and r = .523 respectively, p < .001). Unrelated References and Intrusions were also associated but to a slightly weaker extent (r = .33 and r = .396; p < .01). A further analysis of the errors in repetition was undertaken on those sentences that had been correctly comprehended in order to determine whether poor performance on verbatim repetition was attributable to poor comprehension. This analysis did not yield any different results from the data-set as a whole. Deviation errors were still more common than Omissions [F(1,43) = 15.41, p < .001; (g2p ¼ .26)] and there was no interaction of Omission/Deviation and group [F(2,43) = .044, p .96; (g2p ¼ .002)] or any
Omissions Lexical omissions Makeshift fillers Context appropriate Synonyms Target-related substitutions Contextual inferences References Context inappropriate Unrelated substitutions Erroneous inferences Unrelated reference Intrusions
Healthy controls (n = 15) Mean (SD)
non-FTD patients (n = 18) Mean (SD)
FTD patients (n = 14) Mean (SD)
ANCOVAs F(df = 2,43)
pa
26.47 (16.1) 1.93 (2.6)
42.48 (23.2) 0.92 (1.16)
80.07 (35.7) 2.50 (3.4)
12.67 2.42
