Psychiatry Research 230 (2015) 919–923
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Lexical and sub-lexical reading skills and their correlation to clinical symptoms in young Chinese patients with schizophrenia Jiuju Wang a,b,c, Pengfei Wang a,b,c, Zhichao Xia d, Jin Liu a,b,c, Wenxiang Quan a,b,c, Ju Tian a,b,c, Taeko N. Wydell e, Wentian Dong a,b,c,n a
Peking University Sixth Hospital, Beijing 100191, China Peking University Institute of Mental Health, Beijing 100191, China c Key Laboratory of Mental Health, Ministry of Health (Peking University), Beijing 100191, China d State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China e Centre for Cognition and Neuroimaging, Brunel University London, Uxbridge, UK b
art ic l e i nf o
a b s t r a c t
Article history: Received 13 January 2015 Received in revised form 6 November 2015 Accepted 15 November 2015 Available online 21 November 2015
Patients with schizophrenia often experience severe reading deficits such as oral reading and reading comprehension deficits. However, it is not known whether different types of lexical or sub-lexical components in reading are also impaired. In order to address this issue, the present study had 22 young Chinese patients with schizophrenia and 22 young Chinese normal controls undergo a battery of reading tests, which specifically measures lexical and sub-lexical components of reading in Chinese. The schizophrenic group further underwent Brief Psychiatric Rating Scale (BPRS) in order to ascertain the severity of patients’ clinical symptoms. The results showed that compared to the controls, (1) the schizophrenic patients performed significantly poorly in orthographic processing, orthography–phonology mapping, and orthography–semantic mapping tests and further that (2) their performances in orthographic processing, and orthography–semantic mapping skill tests negatively correlated with the BPRS score. Note however that their ability to access their mental lexicon was intact. There is thus a clear need for studies with a larger sample-size and neurobiological measures which would lead to our better understanding of the behavioral as well as the neural relationships between schizophrenic patients, and their reading processing impairments, thus developing effective reading intervention programs for the schizophrenic patients. & 2015 Published by Elsevier Ireland Ltd.
Keywords: Schizophrenia Sub-lexical & lexical reading skills Mental lexicon Clinical symptoms
1. Introduction Schizophrenia is a common mental disorder, and the prevalence in the population is generally estimated between 0.5% and 1.0% (Erritty and Wydell, 2013). In China, however, an incidence rate of 0.65% across lifespan has been reported (Chen et al., 1998). It is characterized by cognitive impairments involving memory, executive function, language and reading. Especially, recent studies found linguistic-cognitive deficits were associated with clinical symptoms, such as auditory hallucinations and thought disorders (Oertel-Knoechel et al., 2013; Tsao et al., 2013). Therefore, exploring the relationship between cognitive impairments and clinical symptoms is helpful for fully understanding the nature of this disorder. The finding will also promote more accurate diagnosis and more effective therapy programs (De Loye et al., 2013). n Corresponding author at: Peking University Sixth Hospital, Beijing 100191, China. E-mail address:
[email protected] (W. Dong).
http://dx.doi.org/10.1016/j.psychres.2015.11.023 0165-1781/& 2015 Published by Elsevier Ireland Ltd.
For example, as reading is an essential skill for normal lives in modern society, many researchers investigated how reading skills might be affected by schizophrenia, and have repeatedly reported that reading skills were impaired in those individuals with schizophrenia (Clare et al., 1993; Dalby and Williams, 1986). Recently, Revheim et al. (2014) assessed reading ability and sensory function in individuals diagnosed with schizophrenia and found that all schizophrenic patients displayed both visual and phonological impairments, and further that more than 70% of the patients met the criteria for acquired dyslexia (Revheim et al., 2014). In alphabetic language speaking countries, phonological processing skills are the single most crucial factor for the successful development/attainment of literacy skills. Indeed it has been reported that the individuals with schizophrenia showed deficits in both rapid naming and phonological awareness skills (Arnott et al., 2011; Whitford et al., 2013). Contrary to reading in alphabetic languages, in reading Chinese, orthography and semantic skills are shown to be more important, thus the relative contribution from phonology, orthography and semantics to reading vary widely according to different languages (Chen et al., 2009). Using
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statistical learning models, Yang and colleagues (Yang et al., 2009, 2013) found that although adults in general used the same basic reading processes across very different writing systems, the impact of semantics on reading performance was much greater in Chinese than English (Shibahara et al., 2003). In line with these cross-cultural differences in the way reading is being processed, many studies reported that Chinese speakers with developmental dyslexia had mixed deficits in morphological, orthographical, and phonological processing skills (Ho et al., 2007, 2004; Shu et al., 2006; Siok et al., 2009) unlike alphabetic language users with developmental dyslexia whose predominant deficit is in the phonological processing skills (Ramus et al., 2003; Savill and Thierry, 2011). Against this background, it is necessary to examine how those multiple components of reading in Chinese might be affected in Chinese schizophrenic patients. Although some studies showed that general reading skills were impaired in schizophrenic individuals, hardly any systematic investigations have been conducted, especially in Chinese. For example, Tsao et al. (2013) revealed that Chinese adults with schizophrenia were less accurate than normal controls in discriminating lexical tones (a reading related cognitive skill), which in turn further correlated with the severity of schizophrenic symptoms (Tsao et al., 2013). However, this study only detected the deficit in a specific aspect of phonological processing, i.e., tone discrimination in reading, leaving other important reading-related skills in Chinese, such as orthographic and semantic skills in reading (Yang et al., 2009, 2013). The Brief Psychiatric Rating Scale (BPRS) used in much psychiatric/psychological research is an effective instrument for assessing severity of psychotic symptoms among patients with mental disorders. Previous research has also demonstrated a strong correlation between BPRS scores and language skills. For example, (Horton and Silverstein, 2011) found that a significant correlation between language-related skills such as the processing skills in grammar, fluency and comprehension in sentences and BPRS scores in both deaf and hearing schizophrenic patients. Thus, following the above, the next question we need to address is whether there is a correlation between reading-related sub-lexical/lexical skills and the BPRS. Based on previous studies, the current study aims to explore whether the most important sublexical and lexical reading skills in Chinese, i.e., orthographic, orthography–phonology mapping, and orthography–semantic mapping skills as well as abilities to access mental lexicon might be impaired in Chinese patients with schizophrenia. The study will further explore the relationships between possible sub-lexical and lexical skills deficits and clinical symptoms. 2. Methods 2.1. Participants There were in total 44 participants who took part in the study, 22 of whom were patients with schizophrenia and the other 22 were normal controls. The schizophrenic patients (age range: 18–30; 12 males) were recruited from Peking University Sixth Hospital in Beijing, China. Criteria for inclusion were: (1) individual’s symptoms met the diagnostic criteria for schizophrenia in the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV); (2) no nervous system diseases or any other psychotic disorders besides schizophrenia; (3) right-handed; and (4) they were assessed using the Brief Psychiatric Rating Scale (BPRS). Those individuals were excluded (i) if Chinese was not their first language; and (ii) if they had a current substance abuse or history of substance abuse in the last month. All but two patients used antipsychotics medication on conventional doses. See more details in Table 1. The normal controls were volunteers (age range: 18–30; 13 males) working in Peking University Sixth Hospital and Beijing Normal University. The criteria for inclusion were that (1) none of the participant’s second-degree and third-generation relatives had history of psychosis, (2) no history of psychotic disorders or nervous system diseases and (3) were right-handed.
Table 1 Sample characteristics for patients and controls [mean (S.D.)].
Age Gender (M/F)a Education O O–P O–S Mental lexicon Length of illness BPRS Daily chlorpromazine equivalent (mg)
Patients (n¼ 22)
Controls (n ¼22)
24.36(4.03) 12/10 14.77(1.06) 36.61(9.41) 19.43(5.46) 28.09 (10.22) 18.94(5.20) 5.51(3.50) 36.67(8.63) 733.73 (582.16)
23.14(1.94) 13/9 15.00(0.01) 63.61(9.23) 30.51(7.62) 46.09(7.46) 19.44(4.61) – – –
Partial Eta squared
p valueb
0.687 0.423 0.515
0.205 1.000 0.323 o0.001 o0.001 o0.001
0.003
0.737
Note: O for orthography, P for phonology, S for semantics. a b
M for male and F for female. χ2 test for gender, independent-sample t test for the other measures.
The patients and controls did not differ significantly in gender (p ¼1.000), age (p ¼ 0.205) and years of education (p ¼ 0.323) at group level. This study was approved by Peking University Sixth Hospital Ethics Committee and informed written consent was obtained from each normal participant and the guardian of each patient.
2.2. Reading measurements A battery of reading tests consisting of an ‘orthographic test’, an ‘orthography– phonology mapping test’, an ‘orthography–semantics mapping test’, and a ‘lexical access ability test’ was administered. Each of the tests had time limits (see below), so no participant could finish all the items on any task. Several practice items were provided before each of the formal tests. The scores were adjusted by subtracting the number of false-alarm items from the number of hit items. Therefore, a higher score indicates a higher test performance and thus better sub-lexical as well as lexical skills (Xu et al., 2015; Zou et al., 2012).
2.2.1. A Nonword Cross-out test was used to assess orthographic processing skills. The task consisted of 100 nonwords and 208 high frequency Chinese characters as stimuli. All the items were presented in a random order. Participants were asked to mark all the nonwords with a slash “\” as accurately and quickly as possible within 40 s (Zou et al., 2012). 2.2.2. An Onset Judgment test was used to measure orthography–phonology mapping skills. This task consisted of 308 single-character words as stimuli. They were all familiar words with an average word frequency of approximately 125 times per million. The pronunciation of 100 of the items began with /b/ (e.g., ‘北, /bei3/’), whereas the remaining items did not (e.g., ‘回, /hui2/’). The items were presented randomly. Participants were asked to mark all the words produced with an initial /b/ with a slash “\” as quickly and accurately as possible. The time limit for this task was 80 s (Zou et al., 2012).
2.2.3. An Animal Word Cross-out test was used to measure orthography–semantics mapping skills. This task consisted of 220 two- or three-character compound words as stimuli, 74 of which were animal words, such as “青蛙” (/qing1wa1/, frog). They were all familiar words with an average word frequency of approximately 16 times per million. Animal and nonanimal words were presented in a random order. Participants were asked to mark all the animal words with a slash “\” as quickly and accurately as possible. A 50-s time limit was given (Zou et al., 2012).
2.2.4. A Pseudo-Homophone Discrimination test was used to measure ability to access word lexicon. This task consisted of 220 two-character words as stimuli, all of which were familiar with an estimated word frequency of 27 times per million. 72 had one character replaced with another that was pronounced the same, producing a pseudo-homophone, which does not exist in Chinese (e.g., ‘何花’, /he2hua1/). The pseudo-homophones and real words were presented in a random order. Participants were asked to cross out all pseudohomophones with a slash “\” as accurately and quickly as possible within 70 s (Zou et al., 2012).
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2.3. Clinical symptoms The BPRS test scores indicate severity of psychotic symptoms. The test comprises of 18 items that can be scored from 1 (not present) to 7 (very severe). The total BPRS score is the sum of the scores for each of the 18 items. The factor solution includes four subscales: positive symptoms, negative symptoms, manic excitement/ disorganization items and depression/anxiety components. This was based on a clinical interview with the patients and observations of patient behaviors over the previous 1–3 days. Global scores were used to indicate the severity of clinical symptoms (Overall and Gorham, 1962). 2.4. Statistical analysis
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Table 2 Partial correlation between sub-lexical skills and clinical symptoms.
O O–P O–S Mental lexicon
r value p value r value p value r value p value r value p value
BPRS
O
O–P
O–S
0.535* 0.013 0.144 0.532 0.488* 0.025 0.048 0.837
0.408** 0.066 0.421** 0.057 0.115 0.619
0.275 0.227 0.091 0.696
0.243 0.288
Statistical analysis was undertaken using SPSS 16.0 (SPSS Inc., USA). Independent-Sample t-tests were applied to detect the difference between the two groups. Correlations between reading tasks and clinical symptoms were explored using Pearson correlation.
Note: age as the control factor. O for orthography, P for phonology, S for semantics.
3. Results
orthography–semantics mapping skills (in the Animal Word Crossout task), while they showed no impairment in word level lexicon accessing (in the Pseudo-Homophone Discrimination task). Furthermore, their orthography processing skills in the Nonword Cross-out task and orthography–semantics mapping skills in the Animal Word Cross-out task negatively correlated with the severity of their clinical symptoms. In Chinese, orthography processing skills (Ho et al., 2004), orthography–phonology mapping skills (Yang et al., 2009; Zhang et al., 2012) and orthography–semantics mapping skills (Shu et al., 2006; Yang et al., 2013) are the central components for successful reading. Our findings that the Chinese patients with schizophrenia had impairments in these reading-related skills were consistent with the previous studies of alphabetic languages, which demonstrated wide-ranging reading impairments associated with schizophrenia (Arnott et al., 2011; Whitford et al., 2013). Unexpectedly, we found these schizophrenic patients’ ability to access to the word-level mental lexicons (in Pseudo-Homophone Discrimination) was not different from that of the normal controls. This counter-intuitive pattern of the results can be explained by the characteristics of the patients in our study. Specificity, we recruited only young adults with a high level of education. Often the size of mental lexicon correlates with level of education. Further, cognitively this task was not demanding even for the schizophrenic patients, as all the participants were asked to look for pseudo-homophones among two-character compound stimuli. The pseudo-homophones (i.e., nonwords) stood out among twocharacter compound words. This saliency made the task easier to respond correctly for all the participants including the schizophrenic patients. In contrast, the tasks such as the Nonword Cross-out task, the Onset Judgment task, and the Animal Word Cross-out task in Chinese all require an initial in-depth analysis of orthography, i.e., stimulus words/nonwords characters. For example, the single character nonwords in the orthographic lexical decision task looked like Chinese characters, but their stroke configurations were illegal, and hence in order to correctly respond to this task required an indepth orthographic analysis. In order to identify the initial phonemes of single character words in the Onset Judgment task, the initial in-depth orthographic analysis is also vital in order to identify the initial phonemes of the stimulus words. Similarly, in order to correctly identify animal names in the two- to threecharacter words in the Animal Word Cross-out task, the initial indepth orthographic analysis of the stimulus words is essential. In these tasks, the participants were not able to rely on the saliency of the stimuli alone. Altogether the results thus suggest that the Chinese schizophrenic patients in this study showed impairments in orthographic processing skills during reading, as seen in the orthographic processing skills test, orthography–phonology
3.1. Sub-lexical and lexical skills Table 1 shows the means and SDs of the two groups performing in the four reading-related tests. 3.1.1. Orthography (Nonword Cross-out) Compared to normal controls, the patient group showed significantly lower scores on the Nonword Cross-out test: t (42) ¼ 9.605, p o0.05. 3.1.2. Orthography to phonology (Onset Judgments) The patient group showed significantly lower scores than the control group on tests for Onset Judgments: t(42) ¼ 5.544, p o0.05. 3.1.3. Orthography to semantics (Animal Word Cross-out) Compared to the control group, the patient group showed significantly lower scores in the Animal Word Cross-out test: t (42) ¼ 6.673, po 0.05. 3.1.4. Mental lexicon accessing (Pseudo-Homophone Discrimination) There was no significant difference between the two groups in the Pseudo-Homophone Discrimination test: t(42) ¼ 0.338, p ¼0.737. 3.2. Correlation between reading-related skills and BPRS Pearson correlation results indicated that both performance on both the Nonword Cross-out (Orthography) and Animal Word Crossout (Orthography-to-Semantics) tasks negatively correlated with BPRS for the schizophrenic patient group only, r (22) ¼ 0.535, p o0.05 and r (22) ¼ 0.488, po 0.05 respectively. The results were illustrated in Table 2.
4. Discussion The present study explored the possible impairments in the sub-lexical and lexical reading skills in patients with schizophrenia as a consequence of the disease. In order to reliably test different kinds of lexical and sub-lexical reading processing skills, we used young Chinese schizophrenic patients as well as normal controls with a higher level of education (high school or above) as our participants. Compared with normal controls, the patients with schizophrenia manifested significant deficits in the orthography processing skills (in the Nonword Cross-out), orthography–phonology mapping skills (in the Onset Judgment task), and
* **
p o0.05. p o 0.1.
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mapping skills test and orthography–semantics mapping skills test. Overall, this study indicates that the patients have deficits in the processing of orthography, orthography–phonology mapping and orthography–semantics mapping, while their mental lexicon accessing remained intact. It is supported by the mixed representation model (Marslenwilson et al., 1994). When Chinese two-character words were used to access the mental lexicon, the whole word was activated first for familiar words (Tian et al., 2009). In our study, the words used in Homophone Discrimination were all high frequency words. This may suggest that schizophrenic patients have intact activation of the whole words, but impaired ability of orthography processing, orthography–phonology mapping and orthography–semantics mapping. Moreover, the negative correlation between the orthography processing skills as measured in the Nonword Cross-out task and the orthography–semantics mapping skills as measured in the Animal Word Cross-out task with the BPRS suggest that readingrelated skills in particular in-depth orthographical processing skills are impaired in accordance with the severity of clinical symptoms. Of course in order to respond correctly for the Animal Word Cross-out, lexico-semantic processing skills are required. These results, as an extension of several previous studies (Horton and Silverstein, 2011; Hugdahl et al., 2008; Tsao et al., 2013; Wolf et al., 2007) confirm the statement that deficits of language-related skills correlate with clinical symptoms in schizophrenia, which could be used for an indicator for illness severity of schizophrenic patients. Interestingly, the BPRS scores only correlated with orthography processing skills (Nonword Cross-out) and orthography–semantics mapping skills (Animal Word Cross-out), but not with orthography–phonology mapping skills (Onset Judgments) and ability to access mental lexicon (Pseudo-Homophone Judgments). These results were similar to those found by Revheim et al. (2006). The authors used reading comprehension, phonological processing and test of contrast sensitivity functions to investigate the reading and visual processing skills in schizophrenia, and found that the clinical symptom (measured by Positive and Negative Syndrome Scale) correlated significantly only with reading comprehension skills, but not with phonological processing and other readingrelated tests without demands on comprehension (Revheim et al., 2006). As noted earlier all but two schizophrenic patients in the study were treated with antipsychotic drugs. We therefore accept that it may be difficult to tease apart the effects of the disorder from the effects of the medication on cognitive performance. In turn we can also see the argument that that the apparent impairments in the reading-related skills exhibited by the schizophrenic patients in the study might be induced by these drugs that have been taken, and may not be due to the consequence of the disease. If this was the case, however, we should see the impairments across all the language-related skills tasks. Furthermore the significant correlations between the severity of the disease measured by the BPRS and impairments in the orthographic processing skills measured in the orthographic lexical decisions and the orthographic-semantics mapping skills as measured in the Animal Word Cross-out task could not have happened if the impairments were all due to the effects of psychotic drugs. It is therefore reasonable to assume that these impairments were the consequence of the disease, i.e., schizophrenia. However we are also aware that in order to make this argument stronger, and the results generalizable we need to conduct further research with larger sample size. The size of sample size in the current study was constraint by the requirements for high level of education of the participants. In addition we also need to include drug-naïve patients with schizophrenia in the study if we
could find such individuals. We could also divide schizophrenic patients into different clinical symptom-types such as those with hallucinations and thought disorders in future.
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