Abstract
Individuals with schizophrenia exhibit problems in language comprehension that are most evident during discourse processing. We hypothesized that deficits in cognitive control contribute to these comprehension deficits during discourse processing, and investigated the underlying cognitive-neural mechanisms using EEG (alpha power) and ERPs (N400). N400 amplitudes to globally supported or unsupported target words near the end of stories were used to index sensitivity to previous context. ERPs showed reduced sensitivity to context in patients versus controls. EEG alpha-band activity was used to index attentional engagement while participants listened to the stories. We found that context effects varied with attentional engagement in both groups, as well as with negative symptom severity in patients. Both groups demonstrated trial-to-trial fluctuations in alpha. Relatively high alpha power was associated with compromised discourse processing in participants with schizophrenia when it occurred during any early portion of the story. In contrast, discourse processing was only compromised in controls only when alpha was relatively high for longer segments of the stories. Our results indicate that shifts in attention from the story context may be more detrimental to discourse processing for participants with schizophrenia than for controls, most likely due to an impaired ability to benefit from global context.
Keywords: language, EEG, attention, schizophrenia, alpha
Introduction
Individuals with schizophrenia have a variety of cognitive impairments that are resistant to standard treatments, and are related to functional outcomes (Carter, 2006; Green, Kern, Braff, & Mintz, 2000; Green, Kern, & Heaton, 2004; Green & Nuechterlein, 1999). Language processing is one area in which abnormalities have consistently been observed in the disorder, in both speech production and comprehension (Bleuler, 1950; Kraepelin, 1971; Kuperberg, 2010; Kuperberg & Caplan, 2003). Recent studies of language comprehension have found that individuals with schizophrenia tend to exhibit the most pronounced impairment at the discourse (multi-sentence) level, when demands on controlled processing are high (Ditman & Kuperberg, 2007; Swaab et al., 2013). This pattern of impairment has been related to more general context processing and cognitive control deficits that are often observed in schizophrenia (see Boudewyn, Carter, & Swaab, 2012 for a review).
Our goal in this study was to investigate the extent to which individuals with schizophrenia use context in language to guide processing of incoming words. Participants listened to cartoon-style stories, in which inanimate objects (e.g., a peanut) were described as animate protagonists. This allowed us to examine how listeners process incoming words as a function of the local context (e.g., The peanut was elated/salted) and as a function of knowledge from the global context that the object had animate characteristics. Previous work has demonstrated that healthy adults quickly develop discourse representations and that these global representations can facilitate processing of incoming words that violate local animacy constraints (e.g. a singing, dancing inanimate peanut in a cartoon) (Nieuwland & Van Berkum, 2006). Our overarching hypothesis is that individuals with schizophrenia are impaired in their use of global context as they process incoming words due to general context processing deficits. Numerous studies suggest that these deficits form a core impairment in schizophrenia (Barch, Carter, MacDonald, Braver, & Cohen, 2003; Carter, Minzenberg, West, & Macdonald, 2012; Lesh, Niendam, Minzenberg, & Carter, 2011). We were further interested in the role of attentional engagement during listening as a contributing factor in whether or not context is used in processing incoming words. Below, we introduce previous research on language and context processing deficits in schizophrenia and then provide a brief introduction to previous work that has linked changes in alpha-band EEG activity to attention. Finally, we describe our experimental manipulation and predicted results.
Language and Context Processing Deficits in Schizophrenia
Previous studies have documented significant deficits in language in schizophrenia. In speech production, a number of commonly observed abnormalities have been reported at the discourse level. For example, speech that is characterized by disjointed slips from one topic to another is captured by the clinical term derailment, and is one feature of the disorganized speech that is often seen in the disorder (Andreasen, 1979a, 1979b). Several studies have provided evidence for discourse-level impairments in language comprehension, as well (Ditman & Kuperberg, 2007; Swaab et al., 2013). The results of these studies indicate that individuals with schizophrenia are limited in their ability to benefit from context when processing incoming words and phrases (Boudewyn, Carter, et al., 2012; Gernsbacher, Tallent, & Bolliger, 1999; Kuperberg, 2010).
Previous studies suggest that individuals with schizophrenia tend to show the most marked language comprehension impairments when these cognitive control functions are taxed. For example, individuals with schizophrenia do not benefit from discourse organization to the same extent as control participants, showing limited improvements in text recall with increased text coherence (Levy & Maxwell, 1968; Maher, Manschreck, & Rucklos, 1980). Individuals with schizophrenia also demonstrate deficits in the ability to draw inferences using available context compared to control participants (Ditman & Kuperberg, 2007). Further, we recently found that participants with schizophrenia showed a context effect during the processing of incoming words only when primed by an immediately preceding cue word (Swaab et al., 2013).
Lexical ambiguity provides another example of a language processing situation in which cognitive control functions are engaged. When ambiguous words such as bridge are encountered in discourse, both meanings (e.g. card-game and architectural structure) are initially activated and then context is used to select the appropriate meaning and suppress the inappropriate one (e.g. The guests were playing….bridge; suppress architectural structure). In contrast to healthy controls, individuals with schizophrenia are impaired at suppressing the context-irrelevant meaning of an ambiguous word in favor of the context-relevant meaning one (Sitnikova, Salisbury, Kuperberg, & Holcomb, 2002). Results such as these have led to the hypothesis that many language impairments in schizophrenia may be related to an underlying deficit in cognitive control (Boudewyn, Carter, et al., 2012).
Attention, Alpha-Band Activity and Language Processing
Readers and listeners must sustain attention to incoming words and phrases in order to construct an accurate and coherent discourse representation. This is especially true during listening comprehension, due to the fleeting nature of the speech signal. However, attention during discourse processing typically waxes and wanes: some studies estimate that individuals spend between 30–50% of the time off-task during language processing (Franklin, Smallwood, & Schooler, 2011; Giambra, 1995; Smallwood, McSpadden, & Schooler, 2008; Uzzaman & Joordens, 2011). Lapses of attention during comprehension lead to impaired comprehension performance. Smallwood et al. (2008) found that increases in the number of attentional lapses that were reported while reading a detective story were associated with poorer comprehension on a subsequent multiple-choice comprehension test.
Attention engages numerous neural substrates, and there is no straightforward neural signature to indicate when an individual is off-task. However, neuroimaging studies have linked attentional lapses to activity in the default mode network, a large-scale neural network in which activity appears to be suppressed during active task engagement in numerous fMRI studies (Allen et al., 2013; Andrews-Hanna, Smallwood, & Spreng, 2014; Christoff, Gordon, Smallwood, Smith, & Schooler, 2009; Dumontheil, Gilbert, Frith, & Burgess, 2010; Kucyi, Salomons, & Davis, 2013; Mason et al., 2007; Mittner et al., 2014; Stawarczyk, Majerus, Maquet, & D’Argembeau, 2011). In EEG, changes in attentional focus have been linked to changes in alpha-band (~8–12 Hz) activity. For example, alpha activity increases when the eyes are closed compared to when they are open (e.g. Adrian & Matthews, 1934), and tends to decrease as task difficulty increases (e.g. Gevins, Smith, McEvoy, & Yu, 1997; Van Winsum, Sergeant, & Geuze, 1984). There are several theories as to the functional significance of alpha activity, including that it reflects a “cortical idling” signal (Pfurtscheller, Stancak Jr, & Neuper, 1996), the active inhibition of sensory stimuli (Klimesch, 2012; Klimesch, Sauseng, & Hanslmayr, 2007; Roux & Uhlhaas, 2014), and that it is modulated in concert with activity in other bands to facilitate the processing of sensory input (Arnal & Giraud, 2012; Samaha, Bauer, Cimaroli, & Postle, 2015).
One reliable finding is that increases in alpha are associated with the direction of attention inward, away from external stimuli, in scalp-recorded EEG (Jensen, Gelfand, Kounios, & Lisman, 2002; Jensen & Mazaheri, 2010; Mazaheri & Jensen, 2010; Roux & Uhlhaas, 2014). This does not necessarily equate increases in alpha with attentional lapses, as that depends on the nature of the task. For example, a shift of attention inward toward internal representations and away from external stimuli may optimize task performance during the delay period of a working memory task, when a memory set must be maintained prior to recall. Indeed, increases in alpha accompany increases in memory load during such tasks (Jensen et al., 2002). In other tasks, however, such as language comprehension, shifts of attention away from the auditory or visual input are not likely to promote optimal task performance, since information relevant to comprehension may be missed. In this case, increases in alpha may indicate shifts in attention away from the task that may be detrimental to task performance. In line with this reasoning, we recently found that relative increases in alpha power when critical information was presented during story listening predicted individuals’ later ability to access that information (Boudewyn et al., 2015).
The engagement of attention has typically been studied separately from language processing in schizophrenia. However, deficits in sustained attention and vigilance have consistently been demonstrated in individuals with the disorder (e.g. Liu et al., 2002; Nestor, Faux, McCarley, Shenton, & Sands, 1990; Nuechterlein et al., 2015). In addition, there is some indication that individuals with the disorder may be more prone to attentional lapses during cognitive tasks than are control participants, which may partially drive differences in performance (Barch et al., 2012). In the current study, we examined how fluctuations in attention during language processing influence discourse comprehension. Specifically, we used changes in alpha power as an index of attentional engagement as participants listened to cartoon-style stories for comprehension.
Current Study
The goal of this study was to examine whether individuals with schizophrenia use global discourse representations of cartoon-like stories to override local animacy violations (e.g., a singing peanut). Specifically, EEG was recorded while participants listened to cartoon-style stories featuring an inanimate character (see Table 1 for a sample story set; see Appendix 1 for additional sample stories). The stories introduced an inanimate object in the first sentence as an animate character. Its animacy was established by using language that is normally reserved for animate agents (e.g. references to the character having a big smile on his face). In the animate condition, a critical target word in the fourth sentence (e.g. elated) was used that requires an animate object as one of its thematic roles. In the inanimate condition, this word was replaced by a target word (e.g. salted) that was inappropriate in the global context but typically takes an inanimate object as one of its thematic roles in the real world (e.g., peanuts are often salted). Thus, context-appropriate processing of the critical target word requires having developed a representation of the inanimate object as an animate protagonist in the global context, sufficient to render a local animacy violation acceptable by the fourth sentence. We hypothesized that participants with schizophrenia would be impaired at this task compared to control participants, such that they would continue to show a local animacy violation effect on the critical target word even though the global context licensed treatment of the character as animate.
Table 1.
Sentence 1: A lucky peanut had a big smile on his face. |
Sentence 2: The peanut was amazed about his good fortune. |
Sentence 3: Just now he had won the jackpot of two million dollars. |
Sentence 4: The peanut was elatedANIMATE / saltedINANIMATE, and who could blame him. |
True/False: The peanut won the jackpot. |
In order to test this hypothesis, we examined the N400 elicited by critical target words. The N400 is a negative-going ERP waveform that is reduced in amplitude as a function of semantic fit and lexical properties (see Swaab, Ledoux, Camblin, & Boudewyn, 2012, p. for a review). Previous studies have demonstrated that healthy adult readers and listeners are rapidly sensitive to the currently developing discourse context, showing reduced N400 amplitudes to target words that are context-appropriate compared to context-inappropriate (Boudewyn, Gordon, Long, Polse, & Swaab, 2012; Camblin, Gordon, & Swaab, 2007; Van Berkum, Hagoort, & Brown, 1999). Previous work in healthy adults has also shown that, in cartoon contexts similar to those used in the current study, N400 effects at the target words are influenced by the current discourse context, such that “the peanut was elated” yields a reduced N400 amplitude compared to “the peanut was salted” (Nieuwland & Van Berkum, 2006). We predicted that a similar pattern would be observed in the healthy control group. In contrast, we predicted that context processing deficits in individuals with schizophrenia would lead to reduced N400 effects of discourse context.
We also hypothesized that the extent to which processing of the critical target words was guided by context would vary across individuals in both groups. To examine individual differences in the ERP effects, all participants completed three behavioral tasks in addition to the EEG task: the Listening Span task, the AX version of the Continuous Performance Task (AX-CPT), and the Nelson-Denny vocabulary test. The Listening Span task was included as a measure of working memory span, which has been related to the ability to use language context in previous ERP studies (e.g. Boudewyn, Long, & Swaab, 2013; Nakano, Saron, & Swaab, 2010; Van Petten, Weckerly, McIsaac, & Kutas, 1997). Thus, performance on the Listening Span task may be predictive of the N400 context effect. The AX-CPT has been used in previous studies to examine individual differences in the ability to maintain and use context during the performance of cognitive tasks (Cohen et al., 1999), and therefore may also be predictive of the N400 context effect in the current study. A measure of vocabulary size was included because this measure accounts for more variation in language comprehension ability than individual differences in other linguistic and cognitive abilities (Blozis & Traxler, 2007; Hamilton, Freed, & Long, 2013; Long, Johns, & Morris, 2006). We used a multiple regression approach to determine whether performance on the Listening Span task, the AX-CPT, and the vocabulary test were unique in predicting variation in the N400 context effect.
Finally, we used EEG activity in the alpha frequency band in order to examine the relation between shifts in attention to the external stimulus (the story) and language context effects at the critical target words in the fourth sentence of each story. In previous work, we have investigated the role of attention during language comprehension by examining individual differences in alpha power changes during language processing and relating those changes to ERP effects (Boudewyn et al., 2015). Here, we adopted a similar approach, but focused on within-participant (trial-to-trial) fluctuations in alpha-band activity, measured while participants listened to the story context preceding the critical words to which ERPs were time-locked. We predicted that N400 amplitude to the critical target words in sentence 4 would be modulated by condition (Animate, Inanimate) and by alpha power. Specifically, we predicted that higher alpha power would be associated with a reduced N400 effect.
Methods
Participants
Thirty individuals with schizophrenia or a schizophrenia-spectrum disorder and 27 healthy controls completed the study. All participants provided informed consent prior to enrollment, with the approval of the Institutional Review Board at the University of California, Davis. All participants were compensated at a rate of $15 per hour for EEG and behavioral testing; patient participants were compensated $25 for completion of a clinical interview and symptom ratings session. Participants with schizophrenia were within 5 years of the onset of their psychotic symptoms, and were recruited through the Early Diagnosis and Preventive Treatment of Psychosis (EDAPT) clinic at the University of California, Davis Medical Center.
Four participants in the schizophrenia (SZ) group and three HC were ultimately excluded from all analyses due to the presence of excessive artifacts in their EEG data (see EEG Recording & Processing section below for details). Thus, the SZ group included 26 individuals and the HC group included 23 individuals. Participants with schizophrenia ranged in age from 18–30 years (mean: 22.6); 81% were male. HC ranged in age from 18–29 years (mean: 22); 74% were male. All participants were recruited with the following exclusion criteria: (1) IQ below 70, as measured by the Wechsler Abbreviated Scale of Intelligence or Wechsler Test of Adult Reading; (2) history of neurological illness, including head injury; (3) substance-related disorder in the previous six months; (4) uncontrolled medical illness; (5) history of electro-convulsive therapy. Twenty-four of the 26 participants with schizophrenia were right-handed (92.3%), and 21 of the 23 HC were right-handed (91.3%). HC were evaluated using the Structured Clinical Interview for DSM-IV-TR (SCID) (First, 2005) to exclude those with a history of an Axis 1 disorder or first-degree relatives with a psychotic disorder. All participants tested negative on a urine drug screen test immediately prior to completion of the study. See Table 2 for additional demographic information.
Table 2.
Control Participants (N = 23) | Participants with Schizophrenia (N = 26) |
|||
---|---|---|---|---|
Demographics | Mean | SD | Mean | SD |
Age | 22 | 2.9 | 22.6 | 3.1 |
Participant Education (Years) | 15 | 2 | 13.5** | 1.2 |
Parental Education (Years) | 15.7 | 2.9 | 15.1 | 2.1 |
Symptom Ratings | Mean | SD | Min | Max |
SAPS Total | 3.2 | 2.8 | 0 | 10 |
SANS Total | 8.9 | 3.9 | 1 | 15 |
p<0.01
Clinical and Functional Characteristics
Clinicians conducted all diagnostic evaluations, and diagnoses were confirmed by consensus conference. All clinicians had demonstrated reliability, defined by >.8 intra-class correlation-coefficients for continuous measures, and kappa >.7 for categorical measures; all participated in monthly reliability checks to prevent drift from these standards. Clinical symptom scores were measured using the Scales for the Assessment of Positive and Negative Symptoms (SAPS and SANS) (Andreasen, 1981, 1984).
EEG Task Stimuli
The stimuli consisted of 80 story sets. A set was comprised of two conditions of the same story: Animate and Inanimate. Stories were translated from Dutch to English and adapted for the purposes of the current study from those used in Nieuwland and Van Berkum (2006). Each story contained 4 sentences. For all stories, an inanimate, cartoon-like character was introduced in the first sentence (e.g. a peanut that is described as happy and smiling). The passages were written so that each sentence reinforced that the normally inanimate object (e.g., the peanut) served as an animate character in this context. This was accomplished by references in the first three sentences to the character using pronouns reserved for animate characters (he/she), and by the use of verbs and descriptions likewise reserved for animate characters (e.g. the peanut had a big smile…; the peanut was amazed…). Then, in sentence 4, the character was described using a critical word that requires an animate or inanimate object to fill one of its thematic roles. This critical word was therefore consistent with either the immediately preceding context (cartoon-style context-Animate critical word), or inconsistent (cartoon-style context-Inanimate critical word). Inanimate critical words were chosen to be consistent with the most typical, non-cartoon-style meaning of the inanimate objects that served as the animate character. See Table 1 for an example.
The critical words (e.g. elated, salted) were matched in lexical frequency, length and number of syllables across conditions1. To measure lexical frequency, we used LG10CD values from the SUBTLEXus database (http://expsy.ugent.be/subtlexus). The average LG10CD lexical frequency value for critical words in the Animate condition was 1.94 (SD: .62), and 1.8 (SD: .66) in the Inanimate condition. Critical words were also matched in length and number of syllables. The average length of Animate critical words was 7.9 characters (SD: 1.7), and 7.5 (SD: 1.9) for Inanimate critical words. The average number of syllables of Animate critical words was 2.6 (SD: 0.8), and 2.4 (SD: 0.84) for Inanimate critical words.
Stimuli were recorded for auditory presentation by a female speaker, using a natural inflection and speaking rate. The first three sentences of each passage, which comprised the discourse context for the fourth sentence (which contained the critical words), were recorded separately from the critical fourth sentences. The onset and offset of all critical words were determined by visual inspection of the speech waveform and by listening to the waveforms using speech-editing software (Audacity, by Soundforge). The average duration of the critical words was 637.6 ms (range: 366- 974 ms); the critical words did not differ in duration between conditions (p=.4).
One hundred and sixty filler stories of comparable length and structure were also included. These served as experimental stories for a separate study, and also consisted of spoken 4-sentence stories, but did not feature cartoon-style protagonists. Instead, the filler stories featured canonically animate protagonists in non-anomalous scenarios (e.g. a seamstress mending clothes). These stories included a syntactic manipulation in which a prepositional phrase in the fourth sentence attached to the main verb or attached to the direct object (e.g. repaired the sock with the thread/hole). Comprehension questions followed all stories (experimental items and fillers). The correct answer to half of the questions was true, whereas the correct answer to the other half was false. Stimuli were divided into four lists for presentation, such that each list contained 40 stories in each condition (Animate, Inanimate), and no list contained both conditions of the same item.
Stimuli for Behavioral Tasks
In addition to the EEG task, participants completed three behavioral tasks designed to assess vocabulary, working memory, and cognitive control (the Nelson-Denny vocabulary test, Listening Span, and the AX-CPT, respectively).
All participants completed the vocabulary section of the Nelson-Denny Reading Test, a standardized paper and pencil multiple-choice assessment. Participants were allotted 15 minutes to complete the section. Vocabulary is strongly predictive of language comprehension abilities (Long, Prat, Johns, Morris, & Jonathan, 2008) and was employed in this study to examine individual variation in the ERP/EEG data that may be due to variability in verbal ability. Nelson-Denny vocabulary scores were calculated as the total percent correct for the vocabulary section, Form G (out of 80 possible).
The Listening Span task was adapted from Daneman and Carpenter (1980) and consisted of 25 sets of sentences ranging from two to six sentences per set; there were five sets of each set size. Participants were instructed to listen to all sentences within each set for comprehension and then to indicate whether each sentence was true or false immediately after hearing it. In addition, participants were instructed to remember the final word of each sentence in the set and were asked to recall them in any order after the whole set was presented. There was a 1500 ms pause between each sentence during which participants made their true/false response. Presentation of sets was random. Each correct response (accurate final word recall) was scored as one point, for a maximum of 100 points.
The AX-CPT was designed to assess cognitive control mechanisms, specifically the ability to maintain task goals and task-relevant context (Cohen et al., 1999). The version used here was developed as part of the CNTRACS (Cognitive Neuroscience Test Reliability and Clinical applications for Schizophrenia) initiative, and is freely available via the CNTRACS website (http://cntracs.ucdavis.edu/task/dpx). In this task, participants respond to a series of letters via key press. They are told to respond with their index finger only to the letter X (target) and only when the X is preceded by the letter A (cue); they are asked to respond with a middle finger button press to all other letters. A-X cue-probe target sequences are frequent (70%) and set up a tendency to make a target response when the letter X occurs. Therefore, participants often make errors when the letter X appears, but was not preceded by an A (e.g., X preceded by the letter B). Good performance involves the ability to attend to the context in which the letter X occurs and to maintain the task goal throughout processing. D-prime values were computed as a measure of context processing (Cohen et al., 1999), using accuracy on AX trials, controlling for errors on BX trials. This provides a measure of the ability to maintain context (having just seen an A) in order to correctly respond to the target (X), taking into account false alarms to BX trials (d’ context = z(AX accuracy) - z(BX error)).
Procedure
Stimuli were presented through Beyer dynamic headphones using Presentation software (Neurobehavioral Systems). Trials began with a white fixation marker at the center of the screen. The fixation marker was present from 1000 ms before stimulus onset and remained on the screen throughout presentation of the story. Following story offset, the fixation marker remained on the screen for 1000 ms, and was then replaced by a true/false comprehension question. Questions never queried information from the fourth sentence, which contained the critical target words. Participants were asked to make a true/false response via button press. Comprehension questions remained on the screen until participants responded.
Each stimulus list was divided into 20 blocks for presentation. Participants completed the 20 blocks from one list over two EEG sessions. Each session began with a practice block consisting of 8 stories. Lists and blocks were presented in counterbalanced order across participants. Participants completed the behavioral tasks after the second EEG session.
EEG Recording & Processing
EEG was recorded from 29 tin electrodes fitted in an elastic cap (ElectroCap International). The right mastoid electrode was used as the recording reference for all electrodes except those used to measure eye-movements. For these, electrodes above and below the left eye were referenced to each other and used to measure blinks; in addition, two electrodes at the outer canthi of each eye were referenced to each other and used to measure other eye-movements. Recordings from a left mastoid electrode were also obtained, and used for later re-referencing offline to the algebraic average of both mastoids. EEG was recorded using a Neuroscan Synamps 2 system, and digitized at a rate of 500 Hz, with half-amplitude cutoffs of .05 to 100 Hz. Electrode impedances were kept below 5 kΩ.
MATLAB (Mathworks) was used to process and analyze data, with the EEGlab toolbox (Delorme & Makeig, 2004) and ERPlab plugin (Lopez-Calderon & Luck, 2014), along with custom MATLAB code. Independent component analysis (ICA) was used to correct for artifacts caused by blinks, and single-trial waveforms were additionally screened for horizontal eye-movements, and any remaining blinks or movement-related artifacts. These artifact correction and rejection procedures were performed using epochs of 1200 ms for ERP analysis time-locked to the critical words (−200 to 1000 ms with respect to critical word onset). Baseline correction was performed using a −200 to 0 ms window relative to critical word onset. Average ERPs were computed using artifact-free trials in each of the two conditions. Four participants in the schizophrenia group and three in the healthy control group were excluded from all analyses because too few artifact-free trials (<20 per condition) remained following artifact correction and rejection procedures. The remaining participants in the HC group (N=23) had an average of 33 artifact-free Animate trials (SD: 5.1) and 32 artifact-free Inanimate trials (SD: 5.5). The remaining participants in the SZ group (N=26) had an average of 31 artifact-free Animate trials (SD: 5.8) and 30 artifact-free Inanimate trials (SD: 5.8). There were no statistically significant differences between groups in the number of trials included. All ERPs were filtered off-line using a Gaussian low-pass filter (25 Hz half-amplitude cutoff). Statistical analyses were conducted using the filtered data.
For EEG analysis, epochs of 7300 ms were used (−1800 to 5550 ms with respect to 1st and 2nd sentence onset). EEG spectral power was calculated using the EEGlab toolbox, by convolving single-trial epochs with seven-cycle complex Morlet wavelets. Power for 52 log-spaced frequencies from 4–30Hz was calculated for all trials and log-transformed. The alpha frequency band was defined as 8–12 Hz.
Results
Behavior
On average, individuals in the HC group were more accurate than individuals in the SZ group on the comprehension questions that followed the stories (p<0.05). Average accuracy was 93% (range: 82.5- 98.8%) in the HC group, compared to 89% (range: 73.8- 98.8%) in the SZ group. Neither the HC nor the SZ group showed differences in accuracy across conditions.
ERP Data: Animate vs. Inanimate Critical Words
To examine processing of the critical words in the fourth sentence, we focused on the N400 response. As in our previous work on discourse processing in schizophrenia, we conducted a repeated measures ANOVA on the mean amplitude of the N400 using the 350–650 ms time window relative to critical word onset, for the midline, medial, and lateral electrode columns. This time window was chosen following from our previous work examining the N400 effect in the same patient population as the current study (Swaab et al., 2013). Animacy (Animate, Inanimate) was included as a within-participants factor, and Group (SZ, HC) was included as a between-participants factor. To capture potential differences in distribution across the scalp, within-participants topographic factors were included for each column. For the midline column (electrodes Fz, Cz, Pz, PoZ), Electrode Site was included as a factor. For the medial (electrodes FC1, FC2, C3, C4, CP1, CP2) and lateral columns (electrodes F3, F4, FC5, FC6, CP5, CP6, P3, P4), two within-subjects topographic factors were included instead of Electrode Site: Hemisphere (Left, Right), and Anteriority (Medial: Fronto-Central, Centro-Parietal, Parietal; Lateral: Frontal, Fronto-Central, Centro-Parietal, Parietal). The Greenhouse-Geisser correction was applied to F tests with more than one degree of freedom in the numerator. Significant interactions with group were followed up with rANOVAs for each group separately. Results are summarized in Tables 3 and 4. ERP waveforms for each group are plotted in Figure 1.
Table 3.
df | Midline | Medial | Lateral | ||||
---|---|---|---|---|---|---|---|
F | p | F | p | F | p | ||
Animacy | (1,47) | 9.9 | ** | 4.5 | * | 2.5 | ns |
Animacy X Group | (1,47) | 4 | * | 1.3 | ns | 1.2 | ns |
Animacy X Electrode | (3,141) | 4.5 | * | ||||
Animacy X Electrode X Group | (3,54) | <1 | ns | ||||
Animacy X Hemisphere | (1,47) | <1 | ns | 2.9 | ns | ||
Animacy X Hemisphere X Group | (1,47) | 1.3 | ns | 3.6 | ^ | ||
Animacy X Anteriority | Medial: (2,94); Lateral: (3,141) |
5.2 | * | 4.2 | ^ | ||
Animacy X Anteriority X Group | <1 | ns | <1 | ns | |||
Animacy X Hemi X Anteriority X Group | 1.1 | ns | 2 | ns |
p<.1
p<.05
p<.01
Table 4.
df | Midline | Medial | Lateral | ||||
---|---|---|---|---|---|---|---|
Control Participants (N=23) | F | p | F | p | F | p | |
Animacy | (1,22) | 16.3 | ** | 5.7 | * | 3.5 | ^ |
Animacy X Electrode | (3,66) | 1.8 | ns | ||||
Animacy X Hemisphere | (1,22) | <1 | ns | <1 | ns | ||
Animacy X Anteriority | Medial: (2,44); Lateral: (3,66) |
1.3 | ns | 2.2 | ns | ||
Animacy X Hemi X Anteriority | <1 | ns | 2.3 | ns | |||
Participants with Schizophrenia (N=26) | F | p | F | p | F | p | |
Animacy | (1,25) | <1 | ns | <1 | ns | <1 | ns |
Animacy X Electrode | (3,75) | 3.3 | ^ | ||||
Animacy X Hemisphere | (1,25) | 2.2 | ns | 6 | * | ||
Animacy X Anteriority | Medial: (2,50); Lateral: (3,75) |
5.6 | * | 2.1 | ns | ||
Animacy X Hemi X Anteriority | <1 | ns | <1 | ns |
p<.1
p<.05
p<.01
The analyses yielded an effect of Animacy that significantly interacted with Group at the midline electrode column (p<.05; η2=.04). Follow-up analyses showed that the effect of Animacy was significant in HC at midline (p<.05; η2=.09) and medial columns (p<.05; η2=.08). This is consistent with the typical central-posterior maximum of the N400 effect. In contrast, the effect of Animacy in the SZ group was less robust, and only significant at a subset of electrodes in the medial (p<.05; η2=.01) and lateral columns (p<.05; η2=.01), as evidenced by interactions of Animacy with the topographic factors Anteriority and Hemisphere.
Predictors of the ERP Context Effect: Behavior and Symptoms
To investigate how individual differences in our behavioral and symptom severity measures related to the ERP effects (Animate vs. Inanimate critical words), we first calculated simple correlations for these measures for each group separately. We then used a multiple regression approach, which allowed us to determine the unique contribution of each predictor in accounting for variance in the dependent measure (the ERP context effect). This approach also allowed us to include interactions with group in the same regression model. The ERP context effect was defined in these analyses as the difference in mean amplitude between the Animate and Inanimate conditions (Inanimate minus Animate) in the N400 time window (350–650 ms) at electrode Pz. Results are summarized in Tables 5 and 6.
Table 5.
Control Participants (N=23) |
N400 Context Effect |
Vocabulary | Listening Span |
D-prime |
---|---|---|---|---|
N400 Context Effect | ||||
Vocabulary | −.48* | |||
Listening Span | −.226 | .53** | ||
D-prime | −.435* | .314 | .361^ |
Participants with Schizophrenia (N=26) |
N400 Context Effect |
Vocabulary | Listening Span |
D-prime |
---|---|---|---|---|
N400 Context Effect | ||||
Vocabulary | −.339^ | |||
Listening Span | −.95 | .451* | ||
D-prime | −.12 | .21 | .293 |
p<.1
p<.05
p<.01
Table 6.
N400 Context Effect | |||
---|---|---|---|
Predictor | b | β | p |
Constant | 6.373 | ||
Vocabulary | −0.074 | −0.407 | .018* |
D-prime | −2.612 | −0.251 | ns |
Group X Vocabulary | 0.017 | 0.308 | ns |
Group X D-prime | −1.631 | −0.308 | ns |
Vocabulary X D-prime | 0.008 | 0.893 | ns |
p<.05
The Pearson’s correlation results for the behavioral measures showed that Vocabulary and AX-CPT D-prime were significantly correlated with the N400 effect in HC (ps<.05). In the SZ group, there was a trend toward a significant correlation between Vocabulary and the N400 context effect (p=.09). Thus, Vocabulary and AX-CPT D-prime, along with their interaction term and interactions with group were entered into a stepwise multiple regression model. Results showed that only Vocabulary significantly predicted the N400 context effect, such that higher Vocabulary scores predicted larger N400 context effects (p<.05), with the overall model significant at trend level (R2 = .2, F(5,42)=2.1, p=.086). Figure 2 plots the N400 context effect as a function of Vocabulary score.
The Pearson’s correlation results for the symptom severity measures showed that only negative symptom severity (SANS total score) was correlated with the N400 context effect (p<.05), such that higher negative symptom severity scores were associated with smaller N400 context effects. Positive symptom severity was not significantly correlated with the N400 context effect (p=.1). Figure 3 plots the N400 context effect for individuals with schizophrenia as a function of negative symptom severity.
ERP Context Effect and Attention
Alpha Activity during Sentence 1
In order to investigate within-participant (trial-to-trial) fluctuations in alpha-band activity, we first obtained single-trial alpha power estimates, measured when participants were listening to sentence 1 of each story. For each participant, these estimates were divided into high and low alpha trials, using a median split (based on each individual’s median alpha value during sentence 1). Single-trial mean amplitude measures in the N400 time window for the critical words on the corresponding trials (which end in the same stories, 3 sentences later) were calculated, for electrode Pz (where the N400 effects were maximal). These were analyzed using a repeated measures ANOVA as a function of condition (within-participants factor of Animacy) and Alpha (within-participants factor of High/Low Alpha power), and using the between-participants factor of Group (HC, SZ). Significant interactions with group were followed up with rANOVAs for each group separately. As this analysis entailed using longer epochs than in the ERP analyses described above, one additional participant in each group was excluded for excessive artifacts in the long-epoch ERP data. Thus, N=22 in the HC group and N=25 in the SZ group for this analysis. Results are summarized in Table 7.
Table 7.
Group Level Results | |||
---|---|---|---|
df | F | p | |
Alpha | (1,45) | <1 | ns |
Alpha X Group | (1,45) | <1 | ns |
Animacy | (1,45) | 10.6 | ** |
Animacy X Group | (1,45) | 2.3 | ns |
Alpha X Animacy | (1,45) | 3.9 | ^ |
Alpha X Animacy X Group | (1,45) | 5.4 | * |
Results by Group | |||
---|---|---|---|
Control Participants (N=22) | df | F | p |
Alpha | (1,21) | <1 | ns |
Animacy | (1,21) | 9.6 | ** |
Alpha X Animacy | (1,21) | <1 | ns |
Participants with Schizophrenia (N=25) | df | F | p |
---|---|---|---|
Alpha | (1,24) | <1 | ns |
Animacy | (1,24) | 1.7 | ns |
Alpha X Animacy | (1,24) | 10 | ** |
Simple Effects Results for SZ Group | |||
---|---|---|---|
Participants with Schizophrenia (N=25) | df | F | p |
Low Alpha: Animate vs. Inanimate | (1,24) | 10.2 | ** |
High Alpha: Animate vs. Inanimate | (1,24) | 2.1 | ns |
p<.1
p<.05
p<.01
Results showed a significant main effect of Animacy (p<.01; η2=.06), characterized by a significant three-way interaction of Alpha X Animacy X Group (p<.05; η2=.03). Follow-up analyses showed a main effect of Animacy in the HC group (p<.01; η2=.13), but no main effect of alpha on N400 amplitude nor any significant interactions with Alpha. For the SZ group, Alpha and Animacy significantly interacted (p<.01; η2=.11). Simple effects comparisons for the SZ group showed that the N400 effect of Animacy was only significant for Low Alpha trials (p<.01; η2=.3). These results are plotted in Figure 4.
Alpha Activity during Sentence 2
In order to determine whether the relation between alpha activity and the N400 effect at Sentence 4 was specific to alpha activity at the beginning of the stories (Sentence 1), we conducted an analogous analysis using alpha activity measured during Sentence 2. Results are summarized in Table 8.
Table 8.
Group Level Results | |||
---|---|---|---|
df | F | p | |
Alpha | (1,45) | 1.1 | ns |
Alpha X Group | (1,45) | <1 | ns |
Animacy | (1,45) | 15 | *** |
Animacy X Group | (1,45) | 3.8 | ^ |
Alpha X Animacy | (1,45) | 4.2 | * |
Alpha X Animacy X Group | (1,45) | <1 | ns |
Results by Group | |||
---|---|---|---|
Control Participants (N=22) | df | F | p |
Alpha | (1,21) | <1 | ns |
Animacy | (1,21) | 14.8 | *** |
Alpha X Animacy | (1,21) | <1 | ns |
Participants with Schizophrenia (N=25) | df | F | p |
---|---|---|---|
Alpha | (1,24) | <1 | ns |
Animacy | (1,24) | 2.1 | ns |
Alpha X Animacy | (1,24) | 5.2 | * |
Simple Effects Results for SZ Group | |||
---|---|---|---|
Participants with Schizophrenia (N=25) | df | F | p |
Low Alpha: Animate vs. Inanimate | (1,24) | 9.6 | ** |
High Alpha: Animate vs. Inanimate | (1,24) | <1 | ns |
p<.1
p<.05
p<.01
p<.001
We found a significant main effect of Animacy (p<.001; η2=.09), characterized by a marginal Animacy X Group interaction p=.059; η2=.02) and a significant interaction of Animacy X Alpha (p<.05; η2=.02). Follow-up analyses showed a main effect of Animacy in the HC group (p<.001; η2=.18), and no main effect of alpha on N400 amplitude nor any significant interactions with Alpha. For the SZ group, Alpha and Animacy significantly interacted (p<.05; η2=.05). Simple effects comparisons for the SZ group showed that the N400 effect of Animacy was only significant for Low Alpha trials (p<.01; η2=.29). These results replicate the pattern found in the Sentence 1 analyses above, and are plotted in Figure 5.
Alpha Activity across both Sentence 1 and 2
Finally, in order to examine whether relatively high alpha activity across multiple sentences influenced the N400 effect, we conducted an analysis in which High Alpha and Low Alpha trials were defined using both Sentence 1 and 2 alpha estimates. In this analysis, High Alpha trials were defined as those trials on which alpha measured during both Sentence 1 and Sentence 2 was above the respective median alpha estimates for S1 and S2. Likewise, Low Alpha trials were trials on which alpha measured during Sentence 1 was below the median Sentence 1 alpha value, and on which alpha measured during Sentence 2 was below the median Sentence 2 alpha value. Results are summarized in Table 9.
Table 9.
Group Level Results | |||
---|---|---|---|
df | F | p | |
Alpha | (1,45) | <1 | ns |
Alpha X Group | (1,45) | <1 | ns |
Animacy | (1,45) | <1 | ns |
Animacy X Group | (1,45) | 1.5 | ns |
Alpha X Animacy | (1,45) | 5.8 | * |
Alpha X Animacy X Group | (1,45) | <1 | ns |
Results by Alpha Level | |||
---|---|---|---|
Low Alpha | df | F | p |
Animacy | (1,45) | 5.9 | * |
Animacy X Group | (1,45) | <1 | ns |
High Alpha | df | F | p |
---|---|---|---|
Animacy | (1,45) | 1.1 | ns |
Animacy X Group | (1,45) | 1.3 | ns |
p<.1
p<.05
p<.01
p<.001
Results showed a significant interaction of Animacy X Alpha (p<.05; η2=.04); no other effects were significant in the omnibus rANOVA. Follow-up analyses showed a main effect of Animacy for Low S1/S2 Alpha trials (p<.05; η2=.12), but not for High S1/S2 Alpha trials; this effect did not interact with group. These results are plotted in Figure 6.
Discussion
Our primary goal in this study was to investigate the role of attentional engagement in accounting for language processing deficits in comprehension. Participants listened to stories in which cartoon-like inanimate objects were established as main characters through the use of language normally reserved for animate protagonists (e.g. The lucky peanut had a big smile on his face….). In the final sentence of these stories, listeners encountered critical words that either constituted local animacy violations given the typical meaning of the inanimate object (Animate condition; the peanut was elated…), or constituted canonical descriptors of the inanimate object (Inanimate condition; the peanut was salted…). Importantly, target words in the Animate condition were supported by global context given the cartoon-like nature of the stories, whereas target words in the Inanimate condition were unsupported given the global context.
We found that both participants with schizophrenia and control participants showed an N400 effect of context, such that the N400 response to globally supported (Animate) target words was reduced compared to globally unsupported (Inanimate) words in both groups. However, this effect was significantly weaker in participants with schizophrenia compared to control participants. In addition, higher scores on a vocabulary test predicted larger ERP context effects in both the patient and control groups. In the patient group, higher negative symptom severity scores predicted smaller ERP effects. Most importantly, we found that whether or not processing of the critical target words was affected by global context depended on EEG alpha power measured on a trial-by-trial basis at earlier points in the stories. The relation between alpha power and the N400 effect at Sentence 4 varied as a function of group. Control participants did not show N400 effects when alpha activity was high across both Sentence 1 and Sentence 2 of the stories, but did show significant effects when alpha was only high during one of those sentences. In contrast, participants with schizophrenia showed N400 effects when alpha activity was low across Sentence 1 and also when it was low across Sentence 2. We discuss each of these findings in turn.
N400 Context Effect: Basic ERP Findings & Relation to Behavior and Symptoms
Our results showed a significantly weaker context effect in participants with schizophrenia than in control participants. This is consistent with previous studies that have demonstrated impaired discourse-level processing in schizophrenia (Ditman & Kuperberg, 2010; Swaab et al., 2013). However, participants with schizophrenia still showed some sensitivity to context, albeit not to the same extent as participants in the control group. Thus, it was not the case that processing of the critical target words in patients was completely uninfluenced by the preceding discourse, or that processing was completely influenced by lower-level effects2. If that had been the case, participants in the schizophrenia group would have demonstrated a reversal of the N400 effect relative to control participants, such that target words in the globally unsupported condition would have shown reduced N400 amplitude compared to the globally supported condition (which would normally be a local anomaly). Instead, the ability of participants in the schizophrenia group to override previous expectations (namely, that animate descriptors do not apply to inanimate objects) varied across individuals as a function of vocabulary and negative symptom severity, and varied within individuals as a function of attention to the story context.
Indeed, the influence of context on the processing incoming words varied in both groups as a function of vocabulary. Individuals with larger vocabularies tended to show stronger effects of context. This is consistent with our previous work in which individuals with larger vocabularies tended to show stronger referential ambiguity effects, which rely on accurate representations of preceding context (Boudewyn et al., 2015). This pattern is likely driven by the strong relation between the depth and breadth of vocabulary and general verbal ability (Long et al., 2006). Vocabulary is associated with a number of factors related to language comprehension ability, but is particularly related to print exposure, how much time individuals spend reading (Hamilton et al., 2013; Long et al., 2006). Our results extend previous research to show that vocabulary performance is associated with increased sensitivity to context not just in control participants but in participants with schizophrenia as well.
For participants with schizophrenia, negative symptom severity also contributed to variability in sensitivity to global context. Negative symptoms include several that are related to language and motivated behavior, such as poverty of speech (brief, unelaborated responses to questions), poverty of content of speech (responses conveying very little information), and inattentiveness (either social disengagement or lack of attention to clinician’s testing) (Andreasen, 1981, 1982). Individuals with high scores on these and similar symptoms tended to show reduced context effects in this study. Relatively high negative symptom severity has also been shown to correlate with reduced use of language context in a previous behavioral study (Kuperberg, McGuire, & David, 1998). Furthermore, negative symptoms have been associated with deficits in selective attention (Nuechterlein, Edell, Norris, & Dawson, 1986) and performance on a variety of other cognitive tasks (Addington, Addington, & Maticka-Tyndale, 1991; Andreasen, Flaum, Swayze, Tyrrell, & Arndt, 1990).
Sentence 4 N400 Context Effect and Attention
The nature of context processing deficits in the schizophrenia group is informed by our oscillatory results. Although participants with schizophrenia showed weaker context effects overall, patients were sensitive to prior discourse in some conditions. Specifically, we found the strongest context effects when participants with schizophrenia were attentionally engaged in the stories, as indexed by relatively low alpha activity measured on a trial-by-trial basis, but that the context effect was not present when alpha activity during either Sentence 1 or Sentence 2 of the stories was relatively high. This pattern stands in contrast to that observed in control participants, who demonstrated significant context effects at Sentence 4 even when alpha activity was relatively high in Sentence 1 or Sentence 2. Context effects were diminished in this group only when alpha activity was high during both Sentence 1 and Sentence 2.
We argue that high alpha activity reflects a partial shift in attention away from the external stimulus (the story). The alpha results indicate that control participants did not require full attention to the entirety of the short stories in order to establish a contextual representation that was sufficient to render the Sentence 4 target words appropriate given the context. Instead, control participants who “missed” a small portion of the stories as indicated by high alpha activity (Sentence 1 or 2, but not both) established representations of the context that were sufficient to influence the N400 effect at the end of the story. This is consistent with previous studies that have shown that healthy adults develop and use prior context rapidly to guide the processing of incoming words, after even a single sentence of establishing context (e.g. Nieuwland & Van Berkum, 2006; Van Berkum et al., 1999).
The difference between the patient and control groups with respect to how attentional disengagement from the story affects language processing has important implications for understanding comprehension deficits in schizophrenia. Overall, patients showed reduced sensitivity to context (reflected in a reduced N400 context effect) compared to control participants. This is consistent with previous work which has found limitations in the ability to benefit from context when processing incoming words and phrases in schizophrenia (Boudewyn, Carter, et al., 2012; Ditman & Kuperberg, 2007, 2010; Levy & Maxwell, 1968; Maher et al., 1980; Sitnikova et al., 2002; Swaab et al., 2013).
The extent to which patients showed the ERP effect depended on their allocation of attention earlier in the story. When alpha activity during either of the first two sentences of the stories was relatively high, the ERP effect was diminished. Our interpretation of this pattern of results depends on our assumption that alpha activity correlates with the focus of attention, specifically the degree to which attention is directed toward an external stimulus. As discussed in the introduction, this is a reasonable assumption given prior research linking shifts in attention away from external stimuli to increases in alpha activity (Jensen et al., 2002; Jensen & Mazaheri, 2010; Mazaheri & Jensen, 2010; Roux & Uhlhaas, 2014). Based on this assumption, we suggest that the context processing deficits observed in the schizophrenia group may be secondary to deficits in attention to the stories. Participants in both groups had changes in alpha activity across trials that we suggest correspond to changes in attention to the external stimulus (i.e. both groups have trials with relatively low alpha activity and trials with relatively high alpha activity). However, these trial-by-trial fluctuations in alpha activity had the most pronounced influence on context effects in the schizophrenia group. In other words, full attention to the first two sentences of the stories was necessary for participants with schizophrenia to show context effects at the critical target words in Sentence 4. In contrast, control participants showed context effects even when they did not fully attend to a portion of the stories. When control participants “missed” one of the available opportunities to establish the inanimate object as a cartoon-style protagonist, their representation was still sufficient to produce the N400 effect later in the story.
This pattern of results suggests that inattention or shifts in attention away from the story context had a greater influence on discourse processing in participants with schizophrenia than in control participants. We suggest that the negative influence of lapses in attention on comprehension in schizophrenia is influenced by an already weakened ability to use context representations and/or a delayed time-course in the construction of such representations. These results highlight how attentional control failures in schizophrenia may contribute to impairments in language comprehension tasks in which attention over time is required to construct accurate, high-quality discourse representations. Language comprehension may be disrupted more by momentary lapses in attention among individuals with schizophrenia than among healthy adults, in that it may represent a case of “adding insult to injury”. Namely, the cost of even brief lapses in attention to the developing discourse representation may be particularly pronounced in schizophrenia given existing impairments in establishing and making use of contextual representations.
Highlights.
We investigated discourse processing in schizophrenia using EEG and ERPs.
EEG alpha activity indexed attentional engagement during story listening.
Patients showed a smaller N400 context effect than controls.
Relatively high alpha power was associated with compromised discourse processing.
Acknowledgments
Funding
This work was supported by the National Institute of Mental Health (5R21MH099327 to T.Y.S and C.S.C).
Footnotes
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It was not possible to match critical words across conditions on all lexical properties (e.g. concreteness norming data was not available for the majority of critical words). Thus, there is the potential for some variance across lexical items. However, as noted above, critical words were carefully matched across conditions on lexical frequency, length, and number of syllables.
We attribute the N400 effect in the current study to the influence of discourse-level context on the processing of incoming words. It should be noted, however, that critical words differed across conditions; thus, it is possible that subtle changes in pronunciation based on particular upcoming critical words (coarticulation) could have contributed to these effects. As coarticulation would represent one type of contextual information embedded in spoken discourse, this would not change the interpretation of our findings: that the patient group was less sensitive to context during comprehension than the control group.
References
- Addington J, Addington D, Maticka-Tyndale E. Cognitive functioning and positive and negative symptoms in schizophrenia. Schizophrenia research. 1991;5(2):123–134. doi: 10.1016/0920-9964(91)90039-t. [DOI] [PubMed] [Google Scholar]
- Adrian ED, Matthews BH. The Berger rhythm: potential changes from the occipital lobes in man. Brain. 1934;57(4):355–385. doi: 10.1093/brain/awp324. [DOI] [PubMed] [Google Scholar]
- Allen M, Smallwood J, Christensen J, Gramm D, Rasmussen B, Gaden Jensen C, Lutz A. The balanced mind: the variability of task-unrelated thoughts predicts error-monitoring. Frontiers in human neuroscience. 2013;7:743. doi: 10.3389/fnhum.2013.00743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Andreasen NC. Thought, language, and communication disorders: I. Clinical assessment, definition of terms, and evaluation of their reliability. Archives of General Psychiatry. 1979a;36(12):1315–1321. doi: 10.1001/archpsyc.1979.01780120045006. [DOI] [PubMed] [Google Scholar]
- Andreasen NC. Thought, language, and communication disorders: II. Diagnostic significance. Archives of General Psychiatry. 1979b;36(12):1325–1330. doi: 10.1001/archpsyc.1979.01780120055007. [DOI] [PubMed] [Google Scholar]
- Andreasen NC. Scale for the Assessment of Negative Symptoms (SANS) 1981 [PubMed] [Google Scholar]
- Andreasen NC. Negative symptoms in schizophrenia: definition and reliability. Archives of General Psychiatry. 1982;39(7):784–788. doi: 10.1001/archpsyc.1982.04290070020005. [DOI] [PubMed] [Google Scholar]
- Andreasen NC. Scale for the assessment of positive symptoms (SAPS): University of Iowa Iowa City. 1984 [Google Scholar]
- Andreasen NC, Flaum M, Swayze VW, Tyrrell G, Arndt S. Positive and negative symptoms in schizophrenia: A critical reappraisal. Archives of General Psychiatry. 1990;47(7):615–621. doi: 10.1001/archpsyc.1990.01810190015002. [DOI] [PubMed] [Google Scholar]
- Andrews-Hanna JR, Smallwood J, Spreng RN. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Annals of the New York Academy of Sciences. 2014;1316(1):29–52. doi: 10.1111/nyas.12360. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arnal LH, Giraud A-L. Cortical oscillations and sensory predictions. Trends in cognitive sciences. 2012;16(7):390–398. doi: 10.1016/j.tics.2012.05.003. [DOI] [PubMed] [Google Scholar]
- Barch DM, Carter CS, Dakin SC, Gold J, Luck SJ, MacDonald A, Strauss ME. The clinical translation of a measure of gain control: the contrast-contrast effect task. Schizophrenia bulletin. 2012;38(1):135–143. doi: 10.1093/schbul/sbr154. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barch DM, Carter CS, MacDonald AW, Braver TS, Cohen JD. Context-processing deficits in schizophrenia: diagnostic specificity, 4-week course, and relationships to clinical symptoms. Journal of abnormal psychology. 2003;112(1):132. [PubMed] [Google Scholar]
- Bleuler E. Dementia praecox or the group of schizophrenias. 1950 [PubMed] [Google Scholar]
- Blozis SA, Traxler MJ. Analyzing individual differences in sentence processing performance using multilevel models. Behavior Research Methods. 2007;39(1):31–38. doi: 10.3758/bf03192841. [DOI] [PubMed] [Google Scholar]
- Boudewyn MA, Carter CS, Swaab TY. Cognitive control and discourse comprehension in schizophrenia. Schizophr Res Treatment. 2012;2012:484502. doi: 10.1155/2012/484502. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boudewyn MA, Gordon PC, Long D, Polse L, Swaab TY. Does Discourse Congruence Influence Spoken Language Comprehension before Lexical Association? Evidence from Event-Related Potentials. Lang Cogn Process. 2012;27(5):698–733. doi: 10.1080/01690965.2011.577980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boudewyn MA, Long D, Traxler MJ, Lesh TA, Dave S, Mangun GR, Swaab TY. EEG Correlates of Fluctuations in Attention to Discourse Context predict Sensitivity to Referential Ambiguity during Language Comprehension. Journal of Cognitive Neuroscience. 2015;27(12):2309–2323. doi: 10.1162/jocn_a_00837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boudewyn MA, Long DL, Swaab TY. Effects of working memory span on processing of lexical associations and congruence in spoken discourse. Frontiers in psychology. 2013:4. doi: 10.3389/fpsyg.2013.00060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Camblin CC, Gordon PC, Swaab TY. The interplay of discourse congruence and lexical association during sentence processing: Evidence from ERPs and eye tracking. J Mem Lang. 2007;56(1):103–128. doi: 10.1016/j.jml.2006.07.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carter CS. Understanding the glass ceiling for functional outcome in schizophrenia. American Journal of Psychiatry. 2006;163(3):356–358. doi: 10.1176/appi.ajp.163.3.356. [DOI] [PubMed] [Google Scholar]
- Carter CS, Minzenberg M, West R, Macdonald A., 3rd CNTRICS imaging biomarker selections: Executive control paradigms. Schizophr Bull. 2012;38(1):34–42. doi: 10.1093/schbul/sbr114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Christoff K, Gordon AM, Smallwood J, Smith R, Schooler JW. Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proceedings of the National Academy of Sciences. 2009;106(21):8719–8724. doi: 10.1073/pnas.0900234106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen JD, Barch DM, Carter C, Servan-Schreiber D. Context-processing deficits in schizophrenia: converging evidence from three theoretically motivated cognitive tasks. Journal of abnormal psychology. 1999;108(1):120. doi: 10.1037//0021-843x.108.1.120. [DOI] [PubMed] [Google Scholar]
- Daneman M, Carpenter PA. Individual differences in working memory and reading. Journal of verbal learning and verbal behavior. 1980;19(4):450–466. [Google Scholar]
- Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of neuroscience methods. 2004;134(1):9–21. doi: 10.1016/j.jneumeth.2003.10.009. [DOI] [PubMed] [Google Scholar]
- Ditman T, Kuperberg GR. The time course of building discourse coherence in schizophrenia: an ERP investigation. Psychophysiology. 2007;44(6):991–1001. doi: 10.1111/j.1469-8986.2007.00565.x. [DOI] [PubMed] [Google Scholar]
- Ditman T, Kuperberg GR. Building coherence: A framework for exploring the breakdown of links across clause boundaries in schizophrenia. J Neurolinguistics. 2010;23(3):254–269. doi: 10.1016/j.jneuroling.2009.03.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dumontheil I, Gilbert SJ, Frith CD, Burgess PW. Recruitment of lateral rostral prefrontal cortex in spontaneous and task-related thoughts. The Quarterly Journal of Experimental Psychology. 2010;63(9):1740–1756. doi: 10.1080/17470210903538114. [DOI] [PubMed] [Google Scholar]
- First MB. Structured clinical interview for DSM-IV-TR Axis I disorders: patient edition: Biometrics Research Department, Columbia University. 2005 [Google Scholar]
- Franklin MS, Smallwood J, Schooler JW. Catching the mind in flight: Using behavioral indices to detect mindless reading in real time. Psychonomic Bulletin & Review. 2011;18(5):992–997. doi: 10.3758/s13423-011-0109-6. [DOI] [PubMed] [Google Scholar]
- Gernsbacher MA. The structure-building framework: What it is, what it might also be, and why. Models of understanding text. 1996:289–311. [Google Scholar]
- Gernsbacher MA. Two decades of structure building. Discourse processes. 1997;23(3):265–304. doi: 10.1080/01638539709544994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gernsbacher MA, Tallent KA, Bolliger CM. Disordered discourse in schizophrenia described by the structure building framework. Discourse Studies. 1999;1(3):355–372. doi: 10.1177/1461445699001003004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gevins A, Smith ME, McEvoy L, Yu D. High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cerebral Cortex. 1997;7(4):374–385. doi: 10.1093/cercor/7.4.374. [DOI] [PubMed] [Google Scholar]
- Giambra LM. A laboratory method for investigating influences on switching attention to task-unrelated imagery and thought. Consciousness and cognition. 1995;4(1):1–21. doi: 10.1006/ccog.1995.1001. [DOI] [PubMed] [Google Scholar]
- Green MF, Kern RS, Braff DL, Mintz J. Neurocognitive deficits and functional outcome in schizophrenia. Schizophrenia bulletin. 2000;26(1):119–136. doi: 10.1093/oxfordjournals.schbul.a033430. [DOI] [PubMed] [Google Scholar]
- Green MF, Kern RS, Heaton RK. Longitudinal studies of cognition and functional outcome in schizophrenia: implications for MATRICS. Schizophrenia research. 2004;72(1):41–51. doi: 10.1016/j.schres.2004.09.009. [DOI] [PubMed] [Google Scholar]
- Green MF, Nuechterlein KH. Should schizophrenia be treated as a neurocognitive disorder? Schizophrenia bulletin. 1999;25(2):309. doi: 10.1093/oxfordjournals.schbul.a033380. [DOI] [PubMed] [Google Scholar]
- Hamilton ST, Freed EM, Long DL. Modeling reader and text interactions during narrative comprehension: A test of the lexical quality hypothesis. Discourse processes. 2013;50(2):139–163. doi: 10.1080/0163853X.2012.742001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jensen O, Gelfand J, Kounios J, Lisman JE. Oscillations in the alpha band (9–12 Hz) increase with memory load during retention in a short-term memory task. Cerebral Cortex. 2002;12(8):877–882. doi: 10.1093/cercor/12.8.877. [DOI] [PubMed] [Google Scholar]
- Jensen O, Mazaheri A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Frontiers in human neuroscience. 2010:4. doi: 10.3389/fnhum.2010.00186. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klimesch W. alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci. 2012;16(12):606–617. doi: 10.1016/j.tics.2012.10.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klimesch W, Sauseng P, Hanslmayr S. EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev. 2007;53(1):63–88. doi: 10.1016/j.brainresrev.2006.06.003. [DOI] [PubMed] [Google Scholar]
- Kraepelin E. Dementia praecox and paraphrenia. Krieger Publishing Company; 1971. [Google Scholar]
- Kucyi A, Salomons TV, Davis KD. Mind wandering away from pain dynamically engages antinociceptive and default mode brain networks. Proceedings of the National Academy of Sciences. 2013;110(46):18692–18697. doi: 10.1073/pnas.1312902110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuperberg GR. Language in schizophrenia part 1: An introduction. Language and linguistics compass. 2010;4(8):576–589. doi: 10.1111/j.1749-818X.2010.00216.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuperberg GR, Caplan D. Language dysfunction in schizophrenia. Neuropsychiatry. Lippincott Williams and Wilkins, Philadelphia. 2003:444–466. [Google Scholar]
- Kuperberg GR, McGuire PK, David AS. Reduced sensitivity to linguistic context in schizophrenic thought disorder: evidence from on-line monitoring for words in linguistically anomalous sentences. Journal of abnormal psychology. 1998;107(3):423. doi: 10.1037//0021-843x.107.3.423. [DOI] [PubMed] [Google Scholar]
- Lesh TA, Niendam TA, Minzenberg MJ, Carter CS. Cognitive control deficits in schizophrenia: mechanisms and meaning. Neuropsychopharmacology. 2011;36(1):316–338. doi: 10.1038/npp.2010.156. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levy R, Maxwell A. The effect of verbal context on the recall of schizophrenics and other psychiatric patients. The British Journal of Psychiatry. 1968;114(508):311–316. doi: 10.1192/bjp.114.508.311. [DOI] [PubMed] [Google Scholar]
- Liu SK, Chiu C-H, Chang C-J, Hwang T-J, Hwu H-G, Chen WJ. Deficits in sustained attention in schizophrenia and affective disorders: stable versus state-dependent markers. American Journal of Psychiatry. 2002 doi: 10.1176/appi.ajp.159.6.975. [DOI] [PubMed] [Google Scholar]
- Long DL, Johns C, Morris P. Comprehension ability in mature readers. Handbook of psycholinguistics. 2006;2:801–833. [Google Scholar]
- Long DL, Prat C, Johns C, Morris P, Jonathan E. The importance of knowledge in vivid text memory: An individual-differences investigation of recollection and familiarity. Psychonomic Bulletin & Review. 2008;15(3):604–609. doi: 10.3758/PBR.15.3.604. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lopez-Calderon J, Luck SJ. ERPLAB: An Open-Source Toolbox for the Analysis of Event-Related Potentials. Frontiers in human neuroscience. 2014:8. doi: 10.3389/fnhum.2014.00213. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maher BA, Manschreck TC, Rucklos ME. Contextual constraint and the recall of verbal material in schizophrenia: the effect of thought disorder. The British Journal of Psychiatry. 1980;137(1):69–73. doi: 10.1192/bjp.137.1.69. [DOI] [PubMed] [Google Scholar]
- Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN. Wandering minds: the default network and stimulus-independent thought. Science. 2007;315(5810):393–395. doi: 10.1126/science.1131295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mazaheri A, Jensen O. Rhythmic pulsing: linking ongoing brain activity with evoked responses. Frontiers in human neuroscience. 2010:4. doi: 10.3389/fnhum.2010.00177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mittner M, Boekel W, Tucker AM, Turner BM, Heathcote A, Forstmann BU. When the brain takes a break: a model-based analysis of mind wandering. The Journal of Neuroscience. 2014;34(49):16286–16295. doi: 10.1523/JNEUROSCI.2062-14.2014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakano H, Saron C, Swaab TY. Speech and span: Working memory capacity impacts the use of animacy but not of world knowledge during spoken sentence comprehension. Journal of Cognitive Neuroscience. 2010;22(12):2886–2898. doi: 10.1162/jocn.2009.21400. [DOI] [PubMed] [Google Scholar]
- Nestor PG, Faux SF, McCarley RW, Shenton ME, Sands SF. Measurement of visual sustained attention in schizophrenia using signal detection analysis and a newly developed computerized CPT task. Schizophrenia research. 1990;3(5):329–332. doi: 10.1016/0920-9964(90)90018-3. [DOI] [PubMed] [Google Scholar]
- Nieuwland MS, Van Berkum JJ. When peanuts fall in love: N400 evidence for the power of discourse. Journal of Cognitive Neuroscience. 2006;18(7):1098–1111. doi: 10.1162/jocn.2006.18.7.1098. [DOI] [PubMed] [Google Scholar]
- Nuechterlein KH, Edell WS, Norris M, Dawson ME. Attentional vulnerability indicators, thought disorder, and negative symptoms. Schizophrenia bulletin. 1986;12(3):408. doi: 10.1093/schbul/12.3.408. [DOI] [PubMed] [Google Scholar]
- Nuechterlein KH, Green MF, Calkins ME, Greenwood TA, Gur RE, Gur RC, Seidman LJ. Attention/vigilance in schizophrenia: Performance results from a large multi-site study of the Consortium on the Genetics of Schizophrenia (COGS) Schizophrenia research. 2015;163(1):38–46. doi: 10.1016/j.schres.2015.01.017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfurtscheller G, Stancak A, Jr, Neuper C. Event-related synchronization (ERS) in the alpha band—an electrophysiological correlate of cortical idling: a review. International Journal of Psychophysiology. 1996;24(1):39–46. doi: 10.1016/s0167-8760(96)00066-9. [DOI] [PubMed] [Google Scholar]
- Roux F, Uhlhaas PJ. Working memory and neural oscillations: alpha-gamma versus theta- gamma codes for distinct WM information? Trends in cognitive sciences. 2014;18(1):16–25. doi: 10.1016/j.tics.2013.10.010. [DOI] [PubMed] [Google Scholar]
- Samaha J, Bauer P, Cimaroli S, Postle BR. Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction. Proceedings of the National Academy of Sciences. 2015;112(27):8439–8444. doi: 10.1073/pnas.1503686112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sitnikova T, Salisbury DF, Kuperberg G, Holcomb PJ. Electrophysiological insights into language processing in schizophrenia. Psychophysiology. 2002;39(06):851–860. doi: 10.1111/1469-8986.3960851. [DOI] [PubMed] [Google Scholar]
- Smallwood J, McSpadden M, Schooler JW. When attention matters: The curious incident of the wandering mind. Memory & Cognition. 2008;36(6):1144–1150. doi: 10.3758/MC.36.6.1144. [DOI] [PubMed] [Google Scholar]
- Stawarczyk D, Majerus S, Maquet P, D’Argembeau A. Neural correlates of ongoing conscious experience: both task-unrelatedness and stimulus-independence are related to default network activity. PloS one. 2011;6(2):e16997. doi: 10.1371/journal.pone.0016997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swaab TY, Boudewyn MA, Long DL, Luck SJ, Kring AM, Ragland JD, Carter CS. Spared and Impaired Spoken Discourse Processing in Schizophrenia: Effects of Local and Global Language Context. The Journal of Neuroscience. 2013;33(39):15578–15587. doi: 10.1523/JNEUROSCI.0965-13.2013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swaab TY, Ledoux K, Camblin CC, Boudewyn MA. Language-related ERP components Oxford Handbook of Event-Related Potential Components. New York: Oxford University Press; 2012. [Google Scholar]
- Uzzaman S, Joordens S. The eyes know what you are thinking: eye movements as an objective measure of mind wandering. Consciousness and cognition. 2011;20(4):1882–1886. doi: 10.1016/j.concog.2011.09.010. [DOI] [PubMed] [Google Scholar]
- Van Berkum JJA, Hagoort P, Brown CM. Semantic integration in sentences and discourse: Evidence from the N400. Journal of Cognitive Neuroscience. 1999;11(6):657–671. doi: 10.1162/089892999563724. [DOI] [PubMed] [Google Scholar]
- Van Petten C, Weckerly J, McIsaac HK, Kutas M. Working memory capacity dissociates lexical and sentential context effects. Psychological science. 1997;8(3):238–242. [Google Scholar]
- Van Winsum W, Sergeant J, Geuze R. The functional significance of event-related desynchronization of alpha rhythm in attentional and activating tasks. Electroencephalography and clinical Neurophysiology. 1984;58(6):519–524. doi: 10.1016/0013-4694(84)90042-7. [DOI] [PubMed] [Google Scholar]