Active and passive attention in schizophrenia: An ERP study of information processing in a linguistic task

Biological Psychology 32 (1991) 101-124 0 1991 Elsevier Science Publishers B.V. All rights reserved

101 0301-05

11/91/$03.50

Active and passive attention in schizophrenia: An ERP study of information processing in a linguistic task Penny School

F. Mitchell, of Psychology,

Allison School

Sally Andrews

M. Fox, Stanley of Psychiatry,

*

Unillersity of New South

Wales, Australia

V. Catts, Philip

Unic~ersity of New South

B. Ward and Neil McConaghy

Wales Kensington,

Sydney

2033, Australia

Attentional dysfunctions in schizophrenia were investigated using a sentence priming task. Schizophrenic patients and healthy control subjects were presented with sentences to which they were required to make a response based on either semantic or physical stimulus features. Schizophrenics’ behavioural responses were slower than those of controls, particularly when attending to semantic relationships, but their performance was no less accurate. Both the P300 and the N400 components of the event-related potentials (ERPs) recorded to the sentence completions were attenuated in the schizophrenic sample. The results are interpreted in terms of a deficit in the active maintenance of semantic information in memory and the integration of new information with this representation. Keywords:

Schizophrenia, Attentional processing, N400, P300.

deficits,

Active-attention,

Passive-attention,

Semantic

1. Introduction Schizophrenic patients perform poorly on a wide variety of attentionally demanding tasks which involve “high momentary processing load” (Nuechterlein & Dawson, 1984). The basis of these performance deficits remains unknown, but most formulations advanced to account for them are framed in terms of contemporary capacity models of attention which distinguish between limited capacity, attentionally demanding controlled processes and automatic processes which can operate independently of active attention and resource limitations (Kahneman, 1973). Callaway and Naghdi (1982) suggested that schizophrenics’ cognitive deficits resulted from reduced active attentional capacity. Gjerde (1983) proposed that deficits arose from impaired control functions, causing abnormalities in the mobilization and allocation of attentional resources during * Requests University

for reprints should be addressed of New South Wales, Kensington

to: Dr. Sally Andrews, 2033, Australia.

School

of Psychology,

102

P.F. Mitchell et al. / Actil’e and passi[,e attention in schizophrenia

controlled processing. Both these models assume that deficits will only be evident in tasks which require active attentional processing, and that processes which operate automatically will be relatively unimpaired. Alternatively, schizophrenics’ deficits in attentionally demanding tasks may be a consequence of abnormalities in pre-attentive or automatic processes. There may be a defect in the regulation of external stimulation (Johnson, 1985) or filtering mechanisms governing the access of automatically processed information to conscious awareness (Frith, 1981). These models assume that in schizophrenics, information which is usually processed automatically competes for the limited capacity attentional resources, leading to overload of the attentional system. Because of ambiguities surrounding the term “automatic processes” (Logan, 19861, the present paper will refer instead to “passive” attentional processes, which may not always operate entirely independently of attentional resources (Kahneman & Triesman, 19841, but can be distinguished from “active” attentional processes because they are obligatory, i.e. they occur independently of voluntary control (Schneider, 1985; Shiffrin & Schneider, 1977). The distinction between active and passive attentional processes may be operationalised experimentally by manipulating the task relevance of different stimulus attributes. In the present study this is accomplished using a variant of the sentence priming task, in which a sentence frame is presented one word at a time on a computer monitor, with the final word being either a congruous or an incongruous completion. The sentence “He spread his warm toast with” can be terminated with the congruous word “butter” or the incongruous word “socks”. In normals, responses to the final word are faster for congruous than incongruous completions (e.g. Stanovich & West, 1983). We modified this paradigm by having each sentence frame completed by a pair of words rather than the usual single item. These two words were either identical or not, and they were either both congruous with the preceding sentence frame or both incongruous. For example, the sentence frame “The plumber fixed the” can be followed by the pairs SINK, SINK (Congruous Identical); SINK, DRAIN (Congruous, Non-Identical); SWEAT, SWEAT (Incongruous Identical); or SWEAT, DRIFT (Incongruous, Non-Identical). The contributions of active and passive attentional processes were examined by presenting the same stimulus material in three different conditions. The “semantic task” required subjects to decide whether one or both of the words in the pair resulted in a meaningful sentence. In the “physical task”, subjects had to decide whether or not the final word-pair was identical. In the “no response” condition, subjects were asked to read silently the sentence frame and terminal word-pair and no overt response was required. Processing of both stimulus attributes (congruity and identity) were examined when task-relevant, i.e. the subject of active attentional processing, and when

P.F. Mitchell et (11. / ActiL!e and passbe

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task-irrelevant, i.e. the subject of passive attentional processing. Semantic features are the focus of active attention in the semantic task, whilst in the physical task they are irrelevant to the required response and are assumed to receive only passive processing. Conversely, the physical identity of the word-pairs is the focus of active attention in the physical task, whilst in the semantic task the physical relationship between the words is task-irrelevant and need not be actively attended. As well as the reaction times and errors associated with “semantic” and “physical” judgements, event-related potentials (ERPs) elicited by the sentence completion pairs were recorded in the three task conditions. The no-response condition was included to allow comparison of the present data with previous ERP studies that have used single words rather than word-pairs as completions in sentence priming tasks. A negative component with a peak latency of approximately 400 ms, termed N400, has been observed following words which are semantically incongruent with a preceding sentence context (Kutas & Hillyard, 1980). N400 appears to index the degree of relationship between the sentence and final word as it is systematically related to the predictability of the final word as a completion of the sentence, and is reduced for words which are semantically related to the best completion but which are not sensible completions in themselves (e.g. The picnic was ruined by the umbrella; Kutas & Hillyard, 1984). This evidence has been taken to suggest that N400 reflects primarily a passive semantic priming mechanism (Kutas & Hillyard, 1984). By comparing ERPs generated when semantic relationships are task-relevant versus task-irrelevant the present experiment tests this explanation of the mechanisms underlying N400, and examines whether schizophrenics and controls differ in their ERPs elicited by this manipulation. In the two response conditions in the present study, the ERPs will also be influenced by a late positive component, termed P300, which reflects processes that involve limited-capacity, active attentional resources. (Donchin & Coles, 1988; see also Verleger, 1988). P300 is larger for task-relevant as opposed to task-irrelevant stimuli (e.g. Duncan-Johnson & Donchin, 19771, and P300 amplitude increases as the complexity of the stimulus and the task increases (see Johnson, 1986 for a review). In dual-task paradigms, where subjects perform a primary task and ERPs are recorded to secondary task stimuli, P300 amplitude decreases systematically as the difficulty of the primary task increases (Donchin, Kramer & Wickens, 1986). The reduction presumably reflects reduced availability of attentional resources for the secondary task because of the higher attentional demands of the primary task. Attenuation of the P300 component in the ERPs of schizophrenic subjects has been frequently reported, and may reflect deficits in limitedcapacity active attentional processing (e.g. Mirsky & Duncan, 1986; Pritchard, 1986 for a review).

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In summary, if schizophrenics’ cognitive deficits lie in the attentional system responsible for active control of information processing, behavioural and ERP evidence of deficits in schizophrenics will depend on the attentional demands of the particular task and stimuli. Patients will only show performance deficits and ERP abnormalities in conditions requiring active attention to a stimulus attribute. The two groups will not differ in their response to stimulus manipulations that are irrelevant to the current task demands. If, on the other hand, schizophrenics’ attentional deficits reflect abnormalities in passive attentional processes, schizophrenic deficits will emerge even when the stimulus attribute is not the focus of active attention. Because these predictions rely on different patterns of performance for the two diagnostic groups rather than simply a difference in overall level of performance, it is possible to separate the effects of a “generalized performance deficit” (Chapman & Chapman, 19731, from a specific deficit in processes involving either active or passive attention.

2. Method 2.1. Subjects The schizophrenic sample was selected from patients attending the outpatient department of the Psychiatric Unit at Prince of Wales Hospital, Sydney, who satisfied the diagnostic criteria for schizophrenia of both the International Classification of Diseases, 9th edition (World Health Organization, 1978) and the Diagnostic and Statistical Manual of Mental Diseases, 3rd edition [DSM-III] (American Psychiatric Association, 1980). Diagnoses were made on the basis of clinical data derived from case notes and a semi-structured interview using the Present State Examination (PSE) (Wing, Cooper & Sartorius, 1974). Subject exclusion criteria included a history of drug abuse, clinical symptoms suggestive of a DSM-III Organic Mental Disorder, or neurological signs on clinical examination. Patients were included only if they had been educated in an English speaking country and regarded English as their first language and their symptoms had been stable for several months. The 12 males and 3 females studied ranged in age from 23 to 45 (M = 32.6 years). At the time of testing all patients exhibited signs of chronic schizophrenic illness and were significantly disabled. Nine were dependent on government welfare payments, three were in part-time employment, one worked casually and one was unemployed. Only one patient was in full-time work. The occupational status of those employed was below the level for which they were qualified. However, all patients were in a stable condition and able to be treated as outpatients. Rated according to DSM-III, all were chronic, ten were typed residual, three paranoid and two undifferentiated.

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Thirteen patients were receiving neuroleptics (M = 447 mg chlorpromazine equivalents, range: 293-1422 mg) and two were non-compliant with medication. Control subjects were healthy individuals with no history of psychiatric illness who were matched pair-wise with the patients for age and sex. Their ages ranged from 18 to 42 (M = 30.7 years). Peabody Picture Vocabulary Test (Form L) standard scores for the schizophrenic sample ranged from 79 to 124 with a mean of 102 while those for controls ranged from 106 to 141 with a mean of 119. The current vocabulary performance of the schizophrenics was below that of the controls although the schizophrenic sample still performed in the average range. Furthermore, 6 of the schizophrenic patients had attended a tertiary institution and the remaining 9 had completed high school to matriculation level, suggesting that their premorbid level of functioning was above average. 2.2. Stimuli

Stimuli consisted of sentence frames completed with a pair of words which served as the target pair in the response conditions. Sentence frames consisted of 4-7 words (M = 5.3) and ended with an article or personal pronoun (e.g. THE PATIENT CALLED THE). For each of 120 sentence frames, four terminal words of equivalent word frequency (Carroll, Davies & Richman, 1971) were selected where two of these were congruous with the sentence frame and two were not (e.g. NURSE, DOCTOR, STEAM, CLAY). The sentence frames, and completed sentences resulting from appending each terminal word, were rated by an independent sample of undergraduate students to obtain measures of the judged acceptability of each sentence frame-terminal word combination on a 7-point scale, and of the cloze probability of each completion. The mean cloze probabilities and acceptability ratings were 0.33, and 6.2 respectively for the congruous completions, and 0 and 1.3 for the incongruous completions. Four stimulus lists were constructed utilizing the 120 sentence frames. Each of the four lists consisted of every sentence frame completed with one of four different types of terminal word-pairs; congruous identical words (e.g. DOCTOR, DOCTOR), congruous non-identical words (e.g. DOCTOR, NURSE), incongruous identical words (e.g. STEAM, STEAM), and incongruous non-identical words (e.g. STEAM, CLAY). Each list contained 30 items of each of the four congruity-identity conditions. Across all lists each sentence frame occurred once with each terminal word-pair type ensuring that any effects observed were not due to the particular sentence frames employed. Lists were constructed such that the cloze probabilities and acceptability ratings for each of the four stimulus conditions were as similar as possible across the four lists. Three different random orders of each stimulus list were prepared and each

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subject was presented with the same list in differing orders for all three tasks. The assignment of lists to subjects was counterbalanced within each group. Stimuli were presented in upper case characters on a VT200 terminal controlled by a PDP-11. The words of the sentence appeared in the centre of the screen one at a time except for the terminal pair which were presented simultaneously slightly above and below the central fixation point. The characters were 8 mm tall and subtended a vertical angle of approximately 0.57 degrees. Each word of the sentence frame was presented for 300 ms with an inter-word interval of 240 ms. The terminal word-pair was presented for 500 ms. There was a 3 second interval between sentence presentations. Each trial ranged from 5.90 seconds for a 4 word sentence frame to 7.52 seconds for a 7-word frame. 2.3. Procedure The experimental session was divided into three blocks, one for each condition (no-response, semantic and physical). Blocks consisted of 120 experimental trials. The no-response condition was run first, and the order of the other two conditions was counterbalanced within each group. Twenty practice trials were presented before each response condition. Before testing began, subjects were given a brief description of the procedure and fitted with an Electra-cap (Electra-cap International, Inc. Eaton, OH, U.S.A.) for ERP recording. They were then seated comfortably in a small dimly lit room in a chair with microswitches fitted to both armrests. Subjects were instructed to rest their fingers on the switches, and were told that sentences would appear on the screen, one word at a time, followed by a pair of words one above the other which would sometimes complete the sentence sensibly and sometimes not. In the no-response condition, they were asked to read the sentences silently. In the semantic task, they were asked to decide whether or not at least one of the words in the terminal pair completed the sentence sensibly. If the sentence did make sense, they were instructed to press the microswitch under their dominant hand, and if not, to press the switch under their non-dominant hand. In the physical task, the same switches were used to indicate whether or not the two words in the pair were identical. Subjects were asked to respond as quickly as possible and told that their response time was being recorded. Only trials in which reaction times were within 1860 ms of the onset of the stimulus pair were accepted. Scalp electrical activity was recorded from frontal (Fz), central (Cz) and parietal (Pz) midline sites. Vertical eye movement (VEOG) activity was recorded by an electrode 2 cm below the left eye and horizontal activity (HEOG) by an electrode placed on the outer canthus of the left eye. All electrodes were referenced to linked earlobes and electrode impedance did not exceed 5 kR. Trials in which VEOG or HEOG

P.F. Mitchell et al. /Act&e

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activity exceeded 64 mV or incorrect behavioural responses occurred were excluded from the averages. The EEG was amplified by Grass amplifiers with a bandpass of 0.01-30 Hz, and sampled at 6 ms/point from 240 ms prior to the onset of the terminal pair to 960 ms post-stimulus. 2.4. Data analysis Separate analyses were conducted on the reaction-time, error and ERP amplitude data. Problems in the early stages of testing resulted in the loss of ERP data for 3 subjects from each group. The ERP data were measured by calculating the mean amplitude of the waveform for each subject and each stimulus type within two temporal epochs: 300-500 ms post-stimulus and 500-700 ms post-stimulus. These epochs were selected because in the present data set, ERP differences related to congruity and identity were maximal between 300 and 500 ms post-stimulus, and P300 activity was maximal between 500 and 700 ms. The mean amplitudes over each epoch were analysed separately for the no-response and response conditions using repeated measures analysis-ofvariance models. For the response conditions, factors included diagnostic group, task (semantic/physical), congruity, identity and electrode site. For the no-response condition, factors were diagnostic group, congruity, identity and electrode. When appropriate, degrees of freedom were corrected with the Greenhouse-Geisser procedure to control Type 1 error associated with violations of the assumption of spheric&y (Greenhouse & Geisser, 1959). The order of administration of the semantic and physical task conditions was included as a factor in an initial analysis of each data set. Although there were no main effects of order, this factor did participate in complex higherorder interactions in both the RT and ERP amplitude analyses. As these interaction effects do not have a substantial impact on the interpretation of the data, the analyses reported below excluded the order factor so as to avoid unnecessary complexity.

3. Results 3.1. Behavioural data The mean reaction times CRTs) and error-rates for the healthy control and schizophrenic groups for the semantic and physical tasks are presented in Table 1. The main ANOVA results are presented in Table 2. 3.1.1. Task and stimulus effects Analysis of the RT data revealed significant main effects of task, semantic congruity and physical identity, indicating that response times were faster in

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108

Table 1 Mean reaction times and error-rates (percentage) physical response conditions for the schizophrenic Stimulus

type

Semantic

for each stimulus type in the semantic and control groups

task

Physical

task

Schizophrenics

Controls

Schizophrenics

Controls

Congruous Identical

1102 (11.2)

802 (9.6)

984 (1.9)

774 (3.4)

Congruous Non-identical

1135 (8.3)

825 (6.4)

(3.0)

Incongruous Identical

1273 (13.9)

982 (10.9)

1042

884

(3.4)

(6.6)

Incongruous Non-identical

1347 (11.9)

(8.91

1093 (1.4)

(2.2)

1094

1009

and

857 (5.0)

891

the physical than the semantic task (p < O.OOl>, faster to congruous than incongruous completions (p < O.OOl), and faster to identical than non-identical word pairs (I, < 0.001). There was a significant interaction between the effect of task and congruity (p < O.OOl), reflecting a greater effect of congruity in the semantic task than the physical task. The interaction between task, congruity and identity was also significant (p < 0.001). Separate

Table 2 Summary

of the main results

of the ANOVAs

Reaction

Group (Ci) Task (T) TxG Congruity (Cl CxG Identity (I) IxG TxC TxCxG TxI TxIxG CXI CxIxG TxCxI TxCxIxG * p < 0.05

** p < 0.01

on reaction

times

times and error-rates,

df(1,28)

Error rates

F

P

F

24.07 15.99 4.12 54.39
0.001 ** 0.001 ** 0.052 0.001 **


0.001 ** 0.008 ** 0.001 ** 0.170 0.102 0.139 0.001 **

P 8.81

0.007 * *


0.073 0.001 ** 0.118 0.136 0.030 * 0.016 *

P.F. Mitchell et al. /Active

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109

ANOVAs for each task revealed that the reduction in RT for identical compared with non-identical pairs was larger for congruous than for incongruous completions in the physical task (F(1,29) = 12.72; p < O.OOl>, but not in the semantic task (F(1,29) = 1.71, p = 0.203). Some of the RT effects were paralleled in the analysis of error rates, which showed that more errors were made in the semantic than in the physical task (p < 0.011, and that there was a trend towards more errors in response to incongruous than congruous completions (p = 0.073). However, there was a significant effect of stimulus identity (p < 0.001) which was in the opposite direction to that observed for RT, with more errors being made to identical than non-identical word-pairs. This indicates that the fast responses to identical pairs had only been achieved at the expense of accuracy. A significant interaction between identity and congruity (I, < 0.05) reflected a larger identity effect for incongruous than congruous stimuli. The three-way interaction between task, congruity and identity was significant (p < 0.02) and was examined in separate ANOVAs for each task. These revealed a significant identity by congruity interaction in the physical (F(1,29) = 22.52; p < 0.001) but not the semantic task (F < 1). In the semantic task identical stimuli were associated with more errors than non-identical stimuli whether they were congruous or incongruous. In the physical task, identical stimuli elicited more errors than non-identical stimuli when the word pair was incongruous with the sentence, but the reverse was true for congruous pairs (see Table 1). 3.1.2. Group effects The mean RT for the schizophrenics patients (1134 ms) was significantly longer than for the control subjects (878 ms; (p < 0.001)). The two groups also differed in their relative speed of performance in the two tasks (p = 0.0521, with the schizophrenics performing relatively more slowly in the semantic than the physical task compared with the control subjects. In addition, there was a significant interaction between identity and group (p < O.Ol), with patients showing a larger effect of stimulus identity than the control subjects. No other main effects or interactions differentiated the two subject groups. The error rates for the two groups were very similar (Schizophrenics: 7.0%; Controls 6.7%) and neither this, nor any other error rate effect significantly differentiated the groups. 3.2. VEOG

and ERP data

Figure 1 presents the across-subject averaged waveforms at Fz, Cz, Pz and for VEOG, separately for the schizophrenic and control samples in the no response condition. The waveforms for the semantic and physical tasks are presented in Figs. 2 and 3.

P.F. Mitchell et al. / Active and passice attention in schizophrenia

110

NO

-

RESPONSE

SCHIZOPHRENICS

C3NTRCLS

Fz

-4,uv

-4,uv

I

I

II

I!

I’,

0

300

700

500

‘!I

0

ins CON-NON10

_____

CON-ID

300

500

700

m.9 _

INCON-NONID

_________

INCON-ID

___

Fig. 1. Grand average ERPs of schizophrenic and control subjects at the vertical EOG channel (VEOG) and at the three midline recording sites in the no-response condition. CON-ID = congruous identical stimulus pairs, CON-NONID = congruous nonidentical, INCON-ID = incongruous identical and INCON-NONID = incongruous nonidentical.

The waveforms for the VEOG channel in all three conditions were not substantially different for the two groups in the relevant 300-500 ms and 500-700 ms recording epochs. Though there was a trend for more trials to be

P.F. Mitchell et al. / Actice and passive attention in schizophrenia

SEMANTIC

111

TASK

SCHIZOPHRENICS

CONTRCLS

VEOG.

-4pv I

II

II

!I,

0

300

500

‘I/

0

700

me CON-NONID

_-_-_

CON-IO _

300

500

700

ma INCON-NON10

________. INCCN-IO ___

Fig. 2. Grand average ERPs of schizophrenic and control subjects and at the three midline recording sites in the semantic response for Fig. 1.

at the vertical EOG channel condition. Stimulus codes as

rejected owing to vertical eye-movement for the patients (mean per condition = 10.2) than the controls (mean per condition = 5.1), an ANOVA of the number of VEOG rejections, with group and condition (no-response, seman-

112

P.F. Mitchell et al. / Active and passive attention in schizophrenia

PHYSICAL

TASK

CONTROLS

SCHIZOPHRENICS

0

300

500

700

ms CON-NON10 ____.

CON-ID -

INCON-NONID

_________ INCON-IO -_-

Fig. 3. Grand average ERPs of schizophrenic and control subjects at the vertical EOG channel and at the three midline recording sites in the physical response condition. Stimulus codes as for Fig. 1.

tic, physical) as factors, revealed no significant differences between the groups. It was concluded that differential eye movement artifact did not account for the ERP differences found between the patients and controls.

113

P.F. Mitchell et al. / Actiue and passive attention in schizophrenia 14 12 M

1

lo-

R

0

V 0 L T S

a 64m 2 -~

300-500

500-700

300-500

SCHIZOPHRENICS

CONTROLS STIMULUS

-

CON-ID

m

500-700

CON-NONID

TYPE m

INCON-ID

m

INCON-NONID

Fig. 4. Mean amplitudes (in microvolts) of the ERPs recorded in the 300-500 ms and the 500-700 ms epochs for schizophrenic and control subjects in the no-response condition. Amplitudes are averaged over the three midline sites. Stimulus codes as for Fig. 1.

3.2.1. No-response condition The mean amplitudes across electrode sites for each stimulus type in 300-500 ms and 500-700 ms epochs of the no-response condition presented in Fig. 4. The results of the ANOVAs for mean amplitudes in two epochs of the no-response condition are listed in Table 3, with exception of main effects and interactions involving electrode site which reported in the text. Post-hoc contrasts conducted to determine the source significant electrode site effects are also listed in the text.

Table 3 Summary of the ANOVAS of ERP mean amplitudes in the no-response condition, df(1,21) 300-500 F

500-700

5.35 1.45 4.71 1.27 3.02

IXG

CXI CxIxG


ms and 500-700

ms

P

F

P

0.031 * 0.242 0.042 * 0.272 0.097

4.27 27.55 1.85 3.08 3.50 6.71
0.051 * 0.001 ** 0.189 0.094 0.076 0.017 *


Group (G) Congruity (0 CXG Identity (II

* p < 0.05

ms

in the 300-500

the are the the are of

ms epochs

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3.2.1.1. Stimulus effects There were significant main effects of congruity in both epochs (300-500 ms: p < 0.05; 500-700 ms: p < 0.001). The main effect of identity was significant in the 300-500 ms epoch (p < 0.05) but not in the 500-700 ms epoch. ERPs for incongruous and non-identical stimuli were more negative in amplitude than those for congruous and identical pairs, respectively. The interaction between congruity and identity was significant in the 500-700 ms epoch (p < 0.05) and indicated that incongruous non-identical pairs elicited ERPs that were more negative in amplitude than the other stimulus pairs. 3.2.1.2. Group effects There was a main effect of group in the 500-700 ms epoch (p = 0.051). Control subjects’ ERPs were more positive in overall amplitude than those of the schizophrenic sample in the 500-700 ms epoch. There were no significant group by stimulus interactions. 3.2.1.3. Scalp distribution There was a significant effect of recording site in both epochs (300-500 ms: F(2,42) = 13.19, p < 0.001, E = 0.70; 500-700 ms: F(2,42) = 17.11, p < 0.001, E = 0.661, reflecting more positive amplitudes at posterior sites. An interaction between identity and electrode site (300-500 ms: F(2,42) = 5.61, p < 0.05, E = 0.62; 500-700 ms: F(2,42) = 8.91, p < 0.005, E = 0.73) was due to a larger difference between the ERPs elicited by identical and non-identical pairs at Fz and Cz than at Pz (300-500 ms: F(1,22) = 5.36; p < 0.05; 500-700 ms: F(1,22) = 11.69; p < 0.005). There was an interaction between electrode and congruity in the 500-700 ms epoch (F(2,42) = 5.38, p < 0.05, E = 0.88) owing to a significantly larger congruity effect at Pz than at Cz and Fz (F(1,22) = 9.06; p < 0.01). The interaction between group and electrode site was significant for both epochs (300-500 ms: F(2,42) = 5.86, p < 0.02, E = 0.70; 500-700 ms: F(2,42) = 4.78, p < 0.05, E = 0.661, reflecting overall greater positivity in controls at Pz for both epochs. 3.2.2. Semantic and physical tasks Mean amplitudes in the 300-500 ms and 500-700 ms recording epochs, for both groups in the semantic and physical tasks are presented in Figs. 5 and 6 respectively. The results of the ANOVAs of mean amplitudes for the 300-500 ms and 500-700 ms epochs in the physical and semantic tasks are listed in Table 4, for group, task, congruity and identity effects. Electrode site effects are listed in the text. 3.2.2.1. Task and stimulus effects The main effect significant in both epochs (300-500 ms: p < 0.001; was the effect of physical identity (300-500: p < These effects reflected more negative amplitudes

of semantic congruity was 500-700 ms: p < O.OOl), as 0.001; 500-700: p < 0.001). for incongruous than con-

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in schizophrenia

14 12 M

I

10

-

C R 0 V 0 L T S

a 6-

SEMANTIC

PHYSICAL

SEMANTIC

CONTROLS

SCHIZOPHRENICS STIMULUS -

CON-ID

m

PHYSICAL

IYPE t%d

CON-NONID

INCON-ID

t2QQ

INCON

-NONID

Fig. 5. Mean amplitudes (in microvolts) of the ERPs recorded in the 300-500 ms epoch for schizophrenic and control subjects in the semantic and physical response conditions. Amplitudes are averaged over the three midline recording sites. Stimulus codes as in Fig. 1.

14 12 M

I C R 0 V 0 L T S

10 a 642 O-

SEMANTIC

SEMANTIC

PHYSICAL

STIMULUS -

CON-ID

m

CON-NONID

PHYSICAL CONTROLS

SCHIZOPHRENICS TYPE m

INCON-ID

m

INCON-NONID

Fig. 6. Mean amplitudes (in microvolts) of the ERPs recorded in the 500-700 ms epoch for schizophrenic and control subjects in the semantic and physical response conditions. Amplitudes are averaged over the three midline recording sites. Stimulus codes as in Fig. 1.

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Table 4 Summary of the ANOVAs of ERP mean amplitudes in the 300-500 in the semantic and physical response conditions, df(1,21) 300-500

Group (G) Task (T) TxG Congruity (0 CxG Identity (I) IxG TxC TxCxG TxI TxIxG CXI CxIxG TxCxI TxCxIxG * p < 0.05

ms

500-700

F

P

35.70 4.13 1.oo 50.94 9.18 26.61 2.53 10.44 13.12
0.001 0.055 0.329 0.001 0.007 0.001 0.127 0.004 0.002

0.061 0.100

** * ** ** ** ** **

ms and 500-700

ms epochs

ms

F

P

14.19 8.79
0.001 ** 0.008 ** 0.001 ** 0.001 ** 0.020 * 0.108 0.063 0.066 0.001 ** 0.006 ** 0.070

** p < 0.01.

gruous, and for non-identical than identical stimulus pairs. A significant main effect of task was evident in the 500-700 ms epoch (p < 0.005) with a trend in the same direction for the earlier epoch (p = O.OSS>, reflecting more positive amplitudes in the physical than the semantic task. Significant interactions were found between task and congruity in both epochs (300-500 ms: p < 0.005; 500-700 ms: p < 0.05). The interaction between congruity and identity was significant only in the later epoch (p < 0.001). The higher-order interaction between task, congruity and identity was significant in the 500-700 epoch (p < 0.01) and approached significance in the 300-500 epoch (p = 0.061). Separate ANOVAs were performed for each task in order to examine this three-way interaction in more detail. In the physical task, both the congruity (F(1,21) = 25.55, p < 0.001) and identity (F(1,21) = 18.86, p < 0.001) effects were significant for the 300-500 ms epoch. In the semantic task, there was both a large congruity effect (F(1,21) = 44.98, p < O.OOl>, and a significant identity effect (F(1,21) = 9.55, p < 0.001) for the 300-500 ms epoch. The congruity effect was much more substantial in the semantic task. In the physical task, neither the congruity nor the identity effect were significant for the 500-700 ms epoch, but both the congruity (F(1,21) = 16.74, p < 0.001) and identity effects (F(1,21) = 21.60, p < 0.001) were significant for the 500-700 ms epoch in the semantic task. In addition, the congruity by identity interaction was significant for the 500-700 ms epoch in the semantic task (F(1,21) = 20.67, p < O.OOl), reflect-

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ing substantially more negative mean amplitudes for incongruous non-identical ERPs over this latency range. Thus, the pattern of interactions between task, congruity and identity reflects the larger effect of semantic congruity in the semantic than the physical task in both epochs. The congruity effect was significant in both tasks in the earlier epoch, but only in the semantic task in the 500-700 ms epoch. Physical identity, by contrast, exerted equally strong effects in both tasks in the 300-500 ms epoch. In the 500-700 ms epoch the identity effect was significant in the semantic but not the physical task. In addition, in the semantic but not the physical task, the identity effect was larger for incongruous than congruous word-pairs in the 500-700 ms epoch. 3.2.2.2. Group effects There was a significant difference in the mean amplitude of the ERPs for controls and schizophrenics in both the 300-500 ms (p < 0.001) and the 500-700 ms (p < 0.001) epochs, with greater positivity in the control than the schizophrenic group. The other group differences were concentrated mainly in the 300-500 ms epoch, where the groups differed in the size of the congruity effect (p < 0.01) and in the interaction between congruity and task (p < 0.002). The congruity effect was significantly smaller in schizophrenic patients than controls. Within-group ANOVAs revealed that the congruity effect was significantly larger in the semantic task than the physical task for controls (F(l,ll) = 24.57; p < O.OOl), but the congruity by task interaction was not significant for schizophrenics (F < 1). While the congruity effect was significant in both the semantic (F(l,ll) = 84.43; p < 0.001) and physical task (F(l,ll) = 23.66; p < 0.001) for controls, the schizophrenic patients showed a significant congruity effect only in the physical task (F(l,ll) = 7.15; p < 0.05) not in the semantic task (F(l,ll) = 2.77; p = 0.127). The group by identity interaction was not significant, nor were any of the higher order interactions involving identity in either epoch. 3.2.3. Scalp distribution The main effect of electrode site was significant in both epochs (300-500 ms: F(2,42) = 6.82; p < 0.02, E = 0.60; 500-700 ms: F(2,42) = 14.15; p < 0.001, E = 0.70), r e fl ec t’mg the generally more positive mean amplitudes at Pz and Cz compared with Fz. The task by electrode interaction was significant for the 500-700 ms epoch (F(2,42) = 16.24; p < 0.001, E = 0.69) but not for the 300-500 ms epoch (F < l), reflecting greater parietal positivity in the physical task. The congruity by electrode interaction was significant in both epochs (300-500 ms: F(2,42) = 5.28; p < 0.05, E = 0.87; 500-700 ms: F(2,42) = 4.10; p < 0.05, E = 0.63) and the task by congruity by electrode interaction was significant in the 300-500 ms epoch (F(2,42) = 3.92, p < 0.05, E = 0.93). In addition, the group by congruity by task by electrode interaction was significant in the 300-500 ms epoch (F(2,42) = 3.66, p < 0.05,

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E = 0.93). Post-hoc tests revealed that for controls the congruity effect had the same dominantly centro-parietal distribution in both tasks. In the semantic task the congruity effect was significantly larger at Pz and Cz than it was at Fz (F(l,ll> = 4.76; p = 0.052), and in the physical task the congruity effect was larger at Pz than it was at Cz and Fz (F(l,ll> = 17.44; p < 0.005). For the schizophrenic sample the congruity effect was larger at Pz and Cz than at Fz (F(l,lO) = 5.10; p < 0.05) in the physical task, while in the semantic task the congruity effect did not interact with electrode site (F < 1) (see Figures 2 and 3). The interaction between identity and electrode was significant in the 300-500 ms epoch (F(2,42) = 5.85; p < 0.05, E = 0.64) and the task by identity by electrode interactions were significant in both epochs (300-500 ms: F(2,42) = 4.95; p < 0.05, E = 0.68; 500-700 ms: F(2,42) = 9.08; p < 0.005, E = 0.63). Post-hoc tests showed that in the semantic task, the identity effect was significantly larger at Fz and Cz than at Pz (300-500 ms: F(1,21) = 9.X8; p < 0.005; 500-700 ms: F(1,21) = 7.90; p < 0.01). In the physical task the identity effect did not interact with electrode site in the 300-500 ms epoch (Fs < 1) while in the 500-700 ms epoch the identity effect was again larger at Fz than it was at Cz and Pz (F(1,21) = 6.72; p < 0.05).

4. Discussion The first section of the discussion will focus on interpretation of the stimulus and task effects observed on reaction time and ERP measures, whilst the second section will discuss the significance of the group differences on these measures. 4.1. Task and stimulus

effects

Subjects in both groups made faster responses to semantically congruous than incongruous items. This semantic priming effect was significantly larger in the semantic task than in the physical task, indicating that the priming effect is sensitive to the task relevance of semantic relationships. This implies that active attention to semantic relationships contributes to semantic priming effects over and above the contribution of passive or automatic processes. In addition, reaction times were faster to identical items than to non-identical items for all subjects. This effect was equally strong in both tasks, indicating that directing active attention to physical identity does not enhance its effect on performance. Interpretation of the interaction between identity, congruity and task in the RT data must take into account the speed-accuracy trade-off associated with the identity effect. RTs were faster to identical than to non-identical

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word-pairs in both tasks but, apart from responses to congruous completions in the physical task, shorter RTs were associated with increased errors. This speed-accuracy trade-off implies that subjects did not completely ignore the irrelevant stimulus dimension in either task. However, the effect of identity in the semantic task differed from the effect of congruity in the physical task. In the physical task, subjects were less accurate when they had to give either a “no” response to non-identical congruous stimuli or a “yes” response to identical incongruous stimuli. This suggests that a response conflict occurred when there was a mismatch between the behavioural response appropriate for the task and the response that would have been required if the semantic congruity of the stimuli was the focus of attention. In the semantic task, identical pairs were associated with higher error rates than non-identical pairs whether the final pair was congruous or incongruous with the sentence frame, suggesting that the presentation of an identical pair led to general confusion about which attribute was task relevant and therefore to a decrease in accuracy. While this post-hoc interpretation is clearly speculative, the general implication of the complex interaction is that the interfering effects of semantic information on identity judgements are somewhat different from the interfering effects of physical information on semantic judgements. This suggests that there may be differences in the processing of the two stimulus dimensions. The congruity effect was the most striking feature of the ERP data, especially for control subjects. Incongruous words elicited larger amplitude negativity than congruous words, particularly in the 300-500 ms epoch. The negative component related to congruity ended at about 600 ms for identical pairs, but was more prolonged in association with the non-identical word-pairs in the semantic task and the no-response condition. The congruity effect was widespread over the midline scalp sites with a centro-parietal maximum for controls in both tasks. Thus, the onset latency, duration and scalp topography of the congruity effect are consistent with the effect being due to an N400 component elicited by incongruous stimuli. The N400 component was much larger in the semantic task than in the physical task or no-response condition. This suggests that the effect is sensitive to active attentional processes invoked by task demands. Non-identical items elicited larger amplitude negativity than identical items, but this effect was not enhanced by directing the subjects’ active attention to this stimulus attribute during the physical task. Thus, both ERP and RT data indicate that processing of semantic congruity but not physical identity is enhanced by active attention. Congruity effects were evident in the no-response condition, and were enhanced by actively directing attention to this stimulus attribute in the semantic task. In contrast, identity effects were largely insensitive to active attention and appear to be essentially passive in nature.

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The other major feature of the ERP data was the large positive deflection elicited by most stimuli, which began at about 300 ms and peaked at about 550-600 ms. The amplitude of this positive deflection was largest at Pz, and was larger in response conditions compared to when no response was required. These findings are consistent with identification of this positivity as a P300 component. Could the ERP congruity effect presumed to reflect an N400 component be due to changes in the overlapping P300 component? A number of aspects of the data are inconsistent with this hypothesis. Firstly, a significant congruity effect was evident in the no-response ERPs despite minimal evidence of P300 activity. In addition, for control subjects, P300 amplitude in the semantic task was of similar magnitude for incongruous identical and congruous identical stimuli (see Fig. 2). Since these two ERPs differ markedly in N400 amplitude, it is difficult to see how the congruity effect around N400 can be attributed to the processes reflected in P300 amplitude. Consistent with the present data, other studies in which the simultaneous occurrence of P300 has been avoided, still report a significant N400 effect (Kutas & Hillyard, 19891, and the magnitude of the N400 effect does not differ between conditions that do and do not elicit P300 (Kutas & Hillyard, 1983). In addition, a number of studies have reported no difference between P300 amplitudes for congruous and incongruous stimuli, while N400 is apparent only for the incongruous stimuli (Bentin, McCarthy, & Wood, 1985; Pritchard, Coles, & Donchin, 1982; Rugg, 1985). In summary, in the present experiment the N400 component was superimposed on a broad positive deflection rather than appearing as a clear negative peak. The pattern of behavioural and ERP results obtained for control subjects in this study using word-pair sentence completions was similar to that reported using single-word completions (e.g. Kutas & Hillyard, 1980, 1984; Polich, 1985; Stanovich & West, 1983), suggesting that the use of word-pairs to complete sentence frames resulted in processing that is essentially similar to that involved in processing single-word sentence completions. 4.2. Group differences The behavioural results demonstrate that schizophrenics respond more slowly, but just as accurately, as healthy control subjects. Slower performance has been repeatedly reported in studies of schizophrenics. However, the lack of group differences in accuracy suggests that schizophrenics’ slower responses do not simply reflect low motivation or a lack of task involvement (Roth, Tecce, Pfefferbaum, Rosenbloom & Callaway, 1984) but rather that more time is required to achieve the same level of accuracy as controls. Compared with controls, schizophrenics tended to show longer RTs in the semantic task versus the physical task, indicating that they found this task

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relatively more difficult than the physical task. In addition, schizophrenics showed a larger effect of identity on RT than controls, but did not differ significantly from controls in the magnitude of the semantic congruity effect in either RT or error rate. This result contrasts with the findings of two studies using a single-word priming paradigm, where researchers reported that schizophrenics showed larger RT semantic priming effects than controls (Kwapil, Hegley, Chapman & Chapman, 1990; Manschreck, Maher, Milavetz, Ames, Weisstein & Schneyer, 1988). In contrast to the behavioural data, there were no significant group differences for the effect of physical identity in the ERP data, while schizophrenics had significantly smaller N400 congruity effects than controls in the semantic task. Control subjects showed a significantly larger ERP congruity effect in the semantic than the physical task but the task by congruity interaction was not significant for the schizophrenic sample. While the congruity .effect was significant in both tasks for the controls, it was only significant in the physical task for the patients. The group differences in the effects of semantic congruity and physical identity on ERP amplitude are consistent with the view that schizophrenia involves a deficit in active attentional processes. The lack of enhanced processing of semantic congruity in the semantic task relative to the physical task for schizophrenics suggests a failure to enlist, or to profit from, active attentional processes engaged when a task requires a response based on semantic relationships. Schizophrenics did not differ from controls in the effect of semantic congruity during the physical task, or in the effect of identity in either task, suggesting that passive attentional processing of both attributes was proceeding normally. The conclusion that passive attentional processing is relatively normal is consistent with other ERP data from schizophrenics using semantic priming paradigms in which either no overt response was required or the response did not require active attention to semantic relationships. In the no-response condition of the present experiment, and in a silent reading condition of another study (Andrews, Mitchell, Fox, Catts, Ward & McConaghy, 1990), N400 amplitude did not differ in schizophrenics compared with controls. Similarly, Koyama et al. (1991) found no difference between schizophrenics and healthy controls in the N400 amplitude difference for words preceded by semantically related versus unrelated primes during a lexical decision task. The results of the present study could be interpreted as resulting from group differences in strategies adopted to undertake the task rather than processing capabilities per se, but the behavioural data do not support this explanation. Responses in both the semantic and the physical task were subject to speed-accuracy trade-offs which were identical for the two groups, suggesting that the schizophrenics and controls were applying similar strategies to deal with the demands of the two tasks.

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The conclusion that schizophrenics have a deficit in active attentional processing is supported by the marked attenuation of the P300 component in the schizophrenic group. The finding of reduced P300 amplitude is consistent with the results of previous studies (see Pritchard, 1986 for a review). The present study represents the first report of reduced P300 in schizophrenics using linguistic stimuli and equiprobable response conditions. It might be argued that the patients’ reduced P300 amplitude could account for their reduced N400 amplitude. However, the finding that schizophrenics exhibited an attenuated P300 for every stimulus type, not just for congruous word-pairs, is inconsistent with this view. If the reduction in the congruity effect in the 300-500 ms epoch shown by schizophrenics were a reflection of smaller P300 amplitude, there should be a similar reduction in the identity effect for schizophrenics in the 300-500 ms epoch. However, none of the interactions involving identity and group were significant for this epoch. The present data support the conclusion that the reduced congruity effect in the 300-500 ms epoch for schizophrenics compared with controls is a reflection of a smaller N400 component which appears to be independent of the more general deficit in active attention indexed by the attenuated P300. The different patterns of congruity and identity effects in the ERP data of schizophrenics compared with controls have been interpreted as reflecting a deficit in active allocation of attentional resources during controlled processing. This raises the question of why these deficits were restricted to the semantic task. The semantic task was more difficult than the physical task because the decision regarding semantic congruity of the terminal word-pair with the sentence frame required that the words of the sentence be maintained and integrated in memory. The physical task, by contrast, could be performed solely on the basis of information contained in the terminal word-pair, using information which was physically present at the time a response was initiated. The present results could therefore be interpreted as indicating that schizophrenics have relatively more difficulty with tasks that involve the storage and integration of information over time (e.g. Grove & Andreasen, 198.5) than with tasks in which all of the relevant information is physically present when a decision is being made. Further research using non-linguistic tasks requiring such processing is required to establish whether deficits shown by schizophrenics in the present task are specific to linguistic processing. The specificity of the present findings to patients with schizophrenia and the possible contribution of neuroleptic medication to the results obtained in the present study must also be evaluated. Ratings of psychotic symptoms, particularly thought disorder, should also be included in future studies of active and passive attention in schizophrenia to evaluate the relationship between attentional abnormalities and schizophrenic symptomatology.

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Acknowledgments This research was supported by the National Health and Medical Research Council, the NSW Institute of Psychiatry, and the Rebecca L. Cooper Medical Research Foundation. The technical assistance of Mark Pearson and editorial assistance of Patricia Michie is gratefully acknowledged.

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