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Interactive effects of background facial emotion stimulus and target salience on sustained attention performance in schizophrenia
Schizophrenia Research 135 (2012) 90–94
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Interactive effects of background facial emotion stimulus and target salience on sustained attention performance in schizophrenia Sung-Hyouk Park a,⁎, Jin-Chan Noh b, Jin Hun Kim c, Jaewon Lee b, Jin Young Park b, d, Young-Ryeol Lee b, Chan-Hyung Kim d, Kwang-Hyuk Lee e a
Department of Psychiatry, Chookryoung Evangelical Hospital, Namyangju, Gyeonggi, South Korea Department of Psychiatry, Gongju National Hospital, Gongju, Chungnam, South Korea Department of Psychiatry, Ansan Hyo Silver Hospital, Ansan, Gyeonggi, South Korea d Department of Psychiatry, Yonsei University College of Medicine, Seoul, South Korea e Academic Clinical Psychiatry, Department of Neuroscience, School of Medicine and Biomedical Sciences, University of Sheffield, Sheffield, United Kingdom b c
a r t i c l e
i n f o
Article history: Received 29 March 2011 Received in revised form 26 October 2011 Accepted 14 November 2011 Available online 3 December 2011 Keywords: Schizophrenia Attention Face Emotion Salience
a b s t r a c t Schizophrenia impairs both facial emotion processing and sustained attention. Through separate studies, it is known that the presence of a task-irrelevant facial stimulus disproportionately interferes with performance, whereas increasing the salience of task stimulus improves performance during a sustained attention task in patients with schizophrenia. We wished to investigate a potential interaction effect of background facial emotion expression (black and white happy faces vs. grey oval) and target stimulus salience (bright white vs. grey) using the Continuous Performance Test-Identical Pairs version (CPT-IP) in patients with schizophrenia. Thirty-six patients with schizophrenia and 28 healthy control subjects completed 4 different versions of the CPT-IP. We found that healthy controls exhibited higher signal detection sensitivity (d′) when salient target stimuli were presented on the facial background than when the same stimuli were presented on the greyoval background. By contrast, patients were not affected by background stimuli when target number stimuli were salient. When target number stimuli were not salient, both patients and controls showed higher d′ in the grey-oval background condition compared with the facial background condition. This study highlight the significance of stimulus salience during CPT-IP in schizophrenia as background stimuli did not produce a differential effect on performance. Our results suggest that, in the situations where facial emotion stimuli are present, patients' sustained attention can be deteriorated and that the use of salient materials is important in improving performance in schizophrenia. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Sustained attention refers to the ability to remain vigilant over a long period of time in order to prepare and maintain readiness for responses. Patients with schizophrenia exhibit a sustained attention deficit across various stages of the illness (Wohlberg and Kornetsky, 1973; Asarnow and MacCrimmon, 1978; Nuechterlein et al., 1992; Addington and Addington, 1997; Liu et al., 2002). Sustained attention deficit can result in an inability to follow social and work-related conversations and important instructions regarding treatment in patients with schizophrenia (Keefe and Eesley, 2006). Consistent with this, previous studies have shown that sustained attention deficit is closely related to functional outcome in schizophrenia (Green et al., 2000).
⁎ Corresponding author at: Department of Psychiatry, Chookryoung Evangelical Hospital, 174-3, Oebang-ri, Sudong-myeon, Namyangju, Gyeonggi, 472-853, South Korea. Tel.: + 82 31 592 6661; fax: + 82 31 592 6755. E-mail address: [email protected] (S.-H. Park). 0920-9964/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2011.11.019
The continuous performance test (CPT) is one of the most widely used measures of sustained attention deficit in schizophrenia (Nuechterlein, 1983; Cornblatt and Erlenmeyer-Kimling, 1985; Nuechterlein et al., 1986; Cornblatt et al., 1989; Nestor et al., 1990; Mass et al., 2000; Liu et al., 2002; Lee and Park, 2006; Park et al., 2011). The test requires subjects to focus their attention continuously in order to respond whenever the letter X appears (CPT-X), or to respond only when the letter A precedes the letter X (CPT-AX) (Wohlberg and Kornetsky, 1973). During these CPTs, subjects are required to sustain their attention to stimuli presented on a blank screen. Considering that problems in emotional and social functioning are a critical feature of schizophrenia, it is important to understand sustained attention deficit in a social context. The association between neurocognitive and emotional/social deficits has been investigated in previous studies (Kee et al., 1998; Cohen et al., 2006; Sergi et al., 2006). For example, Kee et al. (1998) reported that performance on the Span of Apprehension task, a measure of early visual processing, was correlated with performance on a facial emotion identification task. Furthermore, there is evidence that
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neurocognitive deficits are closely related to social deficits (Green et al., 2000; Velligan et al., 2000; Cohen et al., 2006, but see Addington and Addington, 1997 for evidence against this). However, there have been few studies demonstrating the link between neurocognitive and emotional deficits through an experimental manipulation. We have recently examined CPT-AX performance in the context of facial emotion processing in schizophrenia (Park et al., 2011). In that study, we wished to examine a potential interaction between sustained attention and emotion processing in patients. We presented CPT-AX number stimuli superimposed on the nose of background facial expressions (happy, sad or neutral), because faces provide the most common source of social context. Patients showed a steeper signal detection sensitivity decline when happy faces were presented as background stimuli. By contrast, healthy controls' sensitivity was not affected by background facial emotion stimuli. Our study suggests that the need for continuous emotional processing, especially for happy faces, imposes a significant burden on CPT-AX performance in patients with schizophrenia. It is important to consider why patients showed a significant performance decline when our target number stimuli were superimposed onto happy faces. Our number stimuli had a grayscale intensity of 40% in order to increase task difficulty (i.e., grey target color against grey facial background). Hence, the effect of lowering target luminance would be similar to those observed with the degraded-stimulus CPT, by increasing demand on early visual stimulus-encoding and analysis processes. However, this does not explain why patients showed a performance decline only when background happy faces (but not sad or neutral faces) were used as background. We suspect that the distraction effect of happy faces may have an interaction effect with target stimulus salience. In fact, there are some previous studies showing that patients benefited more than healthy controls when a target stimulus was preceded by a salient cue in a CPT-AX (red ‘A’ followed by target ‘X’) (Lee and Park, 2006). Hence, we hypothesized that patients would not show a decline in performance when target stimuli were salient, but they would show a performance deficit when target stimuli were nonsalient. In the present study, we have extended our previous study to investigate the role of background facial expressions (facial oval vs. grey oval) and target stimulus salience (bright white vs. grey) using the CPT-Identical Pairs version (CPT-IP). The CPT-IP requires subjects to respond as quickly as possible to any consecutive presentation of identical stimuli (Cornblatt et al., 1988). We used background happy faces only, because presenting happy faces as background produced a significant CPT performance decline in schizophrenia patients in our previous study (Park et al., 2011). To manipulate target stimulus salience, we set the grayscale intensity of target stimuli to 0% (salient bright white against grey background) or 40% (non-salient grey). 2. Methods
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Twenty-eight healthy control participants (14 males and 14 females) were recruited from hospital personnel. They were carefully interviewed by a trained psychiatrist (JCN) to exclude any Axis I disorder in themselves or first-degree relatives. Neither mean age nor years of education were significantly different between the groups (see Table 1 for details). After complete description of the study to the participants, written informed consent was obtained. The study was approved by Gongju National Hospital Institutional Research Ethics Review Board. 2.2. CPT-IP We used a block design. In a 2 by 2 factorial task design, there were four separate experimental conditions: the CPT-IP with facial background and grey number stimulus condition, the CPT-IP with facial background and bright white number stimulus condition, the CPT-IP with grey-oval background and grey number stimulus condition, and the CPT-IP with grey-oval background and bright white number stimulus condition. In each condition, there were 540 trials lasting 9 min. Of these, 81 (15%) number stimuli were target stimuli. Subjects had a break between the conditions. The order of the conditions was counterbalanced across participants in each group. Background face stimuli were all happy faces and chosen from Ekman and Friesen's Pictures of Facial Affect (Ekman and Friesen, 1976). Hair features and clothing were occluded to form an oval shape (Tsoi et al., 2008). During facial background conditions, number stimuli appeared on the nose of the background facial stimulus (see Fig. 1). Two-digit numbers were used as target and non-target stimuli. The grey-oval background stimulus was constructed to be the same size as the facial stimuli and had an average luminance of all facial stimuli. Subjects were asked to press the left mouse button whenever there was any consecutive presentation of identical number stimuli. Stimuli were presented at a constant rate of one per second as with other CPT studies in schizophrenia (Cornblatt et al., 1989; Kurtz et al., 2001). During facial background conditions, each pair of stimuli (a number and a face oval) appeared for the first 50 ms followed by just the face for the remaining 950 ms to allow a response to be made to the target. The background face therefore remained on the screen for the entire trial duration of 1 s. During grey-oval background conditions, a grey oval background was used, instead of the background face. Subjects sat approximately 60 cm from the screen. The large diameter of the face oval and grey-oval was 160 mm and the small diameter of them was 120 mm. The face oval and the grey-oval stimuli were presented in the center of screen. The number stimuli were presented in size 25 Arial font. A PC running E-Prime 2.0 (Psychology software Table 1 Demographic data.
2.1. Participants
Normal control (n = 28)
Schizophrenic patient (n = 36)
Analysis
Thirty-six patients with schizophrenia (18 males and 18 females) were recruited from Gongju National Hospital, Gongju, Chungnam, South Korea. A diagnosis of schizophrenia was confirmed using the Structured Clinical Interview for Axis I DSM–IV Disorders — Patient Edition (SCID–I/P)(First et al., 1996). Exclusion criteria were diagnosis of an Axis I disorder other than schizophrenia, neurological disorders, or mental retardation. At the time of testing, patients were treated with atypical (n = 33) or both typical and atypical neuroleptics (n = 3) at an average dose of 539.33 ± 328.85 chloropromazine equivalents per day. Schizophrenia symptoms were rated using the Scale for the Assessment of Negative Symptoms (Andreasen, 1984a) and the Scale for the Assessment of Positive Symptoms (Andreasen, 1984b).
N(%), mean (SD)
N(%), mean (SD)
χ² , t
p-value
14/14 33.11 14.36 84.23
18/18 36.33 13.72 86.41 9.81 6.42 40.53 6.03
χ² = 0.00 t = 1.66 t = − 1.14 t = 1.70
1 0.10 0.25 0.09
Sex (m/f) Age Education (yr) EHI SANS SAPS GAF score Admission number DOI (yr)
(50/50) (8.58) (1.76) (4.67)
(50/50) (6.96) (2.48) (5.37) (5.00) (2.85) (5.42) (4.08)
10.0 (5.57)
Abbreviation: EHI, Edinburgh Handedness Inventory; SANS, Scale for the Assessment of Negative Symptoms; SAPS, Scale for the Assessment of Positive Symptoms; GAF, Global Assessment of Functioning scale; DOI, Duration Of Illness.
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stimulus recognition, i.e., the ability to distinguish target from nontarget. A higher d′ value indicates better performance. We first present 3-way repeated measure ANOVA results for d′ and reaction time. The between-subject factor was group (patients vs. controls). The within-subject factors were background (face oval vs. grey oval) and luminance of stimuli (bright white vs. grey). 3. Results 3.1. Sensitivity (d′)
Fig. 1. Stimuli and trial sequence in the CPT-IP.Facial stimuli used as background are copyrighted by Paul Ekman, Ph.D.
tools, Inc., Pittsburgh, PA; http://pstnet.com) controlled experimental events and recorded data. 2.3. Data analysis We calculated d′ as a signal detection sensitivity index. The calculation of d′ was based on the formula reported in the paper by Macmillan and Creelman (1990). Because our data included the hit rate of 1.0 and false alarm rate of 0, calculating d′ would produce the problem of division by zero. To avoid the problem of division by zero, it is necessary to adjust hit and false alarm rate (Corwin, 1994). The sensitivity measure d′ refers to the sensory dimension of
The main effect of group was significant, indicating that d′ of patients was significantly lower than that of control subjects (F1,62 = 68.332, p b 0.001). Neither the main effect of background (F1,62 = 2.810, p = 0.099) nor the main effect of luminance was significant (F1,62 = 0.109, p = 0.743) (Table 2). There was a significant interaction between background and group on d′ (F1,62 = 4.778, p = 0.033). Post hoc analysis revealed that the d′ of patients was lower with facial background condition compared with the grey-oval background condition (p b 0.01), whereas d′ of controls was not different between the two background conditions (p = 0.735). The interaction between target number luminance and group was not significant (F1,62 = 0.532, p = 0.468). A significant interaction effect that did not involve the group factor was the interaction between background and stimulus luminance (F1,62 = 35.155, p b 0.001). Post hoc analysis showed that d′ was lower with face oval background than with grey-oval background when number stimuli were in grey (p b 0.001). d′ was higher when bright white (vs. grey) target stimuli were presented on the facial background (p b 0.001). The reverse was also significant: d′ was higher when grey (vs. bright white) target stimuli were presented on the grey-oval background (p = 0.024). There was a significant 3-way interaction between background, target luminance, and group (F1,62 = 7.065, p = 0.010). Post hoc analysis revealed that healthy controls exhibited a cross-over interaction effect between background and luminance (Fig. 2): Their d′ was higher with grey-oval background than with facial background in the grey number stimulus conditions (p= 0.024). The reverse was also significant: their d′ was higher when bright white number stimuli were presented on the facial background than on the grey-oval background (p b 0.001). By contrast, patients with schizophrenia were not affected by background stimuli when the number stimuli were salient (i.e., no significant d′ difference between the facial background condition and the grey-oval background condition). When the number stimuli were in grey, patients showed higher d′ in the grey-oval background condition than in the facial background condition (p = 0.002), as was seen in controls. 3.2. Reaction time There was a significant main effect of group, suggesting that reaction time of patients was longer than that of controls (F1,62 = 48.579, p b 0.001). The main effect of background was significant (F1,62 = 11.337, p b 0.001), indicating that reaction time for the facial
Table 2 CPT performance indices in each experimental condition. Hit rate Experimental condition Facial background Grey stimulus Facial background Bright white stimulus Grey-oval background Grey stimulus Grey-oval background Bright white stimulus
SPR (n = 36) NC(n = 28) SPR (n = 36) NC (n = 28) SPR (n = 36) NC (n = 28) SPR (n = 36) NC (n = 28)
Abbreviation: SPR, Schizophrenia; NC, normal control.
False alarm rate
Sensitivity (d′)
Reaction time (ms)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
0.515 0.932 0.563 0.930 0.635 0.939 0.631 0.929
(0.231) (0.063) (0.233) (0.052) (0.243) (0.066) (0.235) (0.053)
0.012 0.012 0.010 0.004 0.010 0.016 0.011 0.023
(0.016) (0.040) (0.012) (0.014) (0.012) (0.073) (0.010) (0.099)
2.490 4.122 2.673 4.434 2.868 4.422 2.797 4.067
(0.858) (0.710) (0.819) (0.623) (0.980) (0.938) (0.849) (0.751)
558.553 442.843 528.131 427.746 527.703 428.606 520.669 425.595
(84.493) (58.264) (71.022) (49.436) (70.772) (43.703) (68.708) (50.340)
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Fig. 2. Signal detection sensitivity (d′) in 4 task conditions in patients with schizophrenia and healthy controlsError bars show 95% confidence intervals.Abbreviations: FG, Facial background and grey number condition; FB, Facial background and bright-white number condition; GG, Grey-oval background and grey number condition; GB, Grey-oval background and bright-white number condition.
background condition was longer than that for the grey-oval background condition. The main effect of stimulus luminance was also significant (F1,62 = 10.086, p = 0.002), suggesting that reaction time to grey stimuli was longer than that for bright white stimuli. There was a significant interaction between background and luminance of number stimuli (F1,62 = 5.157, p = 0.027). Post hoc analysis showed that reaction time was significantly longer when the grey number stimuli were presented on the facial background compared with the grey-oval background condition (p b 0.001). By contrast, there was no significant difference in reaction time according to background in the bright white stimulus conditions (p = 0.396). Neither the interaction between luminance of number stimuli and group (F1,62 = 1.223, p = 0.273) nor the interaction between background and group (F1,62 = 1.821, p = 0.182) was significant. The 3-way interaction between background, luminance of stimuli, and group was not significant (F1,62 = 0.523, p = 0.472). 4. Discussion In the present study, we investigated the impact of stimulus salience (bright white vs. grey) on different background stimuli (facial emotion expressions vs. grey-oval) using the CPT-Identical Pairs version (CPT-IP). We found that when the number stimuli were not salient (in grey), patients with schizophrenia, similar to healthy subjects, showed lower signal detection sensitivity (d′) in the facial background condition, compared with the grey-oval background condition. However, when the number stimuli were salient (in bright white), patients were not differentially affected by background stimuli. These findings suggest that increased stimulus salience may be helpful for patients to overcome the interfering effect of facial background stimuli during the CPT-IP. This is consistent with a previous study where the stimulus salience aided CPT-AX performance in patients with schizophrenia (Lee and Park, 2006). Our study extended the effect of stimulus salience to an experimental situation where socially-relevant, facial emotion expressions were involved. CPT performance is affected by the relationship between target and non-target stimuli and the nature of cognitive operations that are required (Cohen and Salloway, 1997). In order to lower the discriminability of target and non-target stimuli, previous studies have used various distracters. Patients with schizophrenia exhibited especially poor CPT performance with distracters (Franke et al., 1994; Egan et al., 2000; Cosway et al., 2002). In our study, the background happy faces would function as distracters, as in our previous study(Park et al., 2011). Our finding of a significant interaction between background and group suggests that patients were more vulnerable to the distracting effect of background happy faces. This distraction
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effect was consistent with previous studies using number stimuli in a CPT (Franke et al., 1994; Egan et al., 2000; Cosway et al., 2002). Cognitive operations required in performing the CPT-IP are more demanding than in performing the CPT-AX, because targets can be changed from trial to trial in the CPT-IP, whereas the target in the CPT-AX (‘A’ followed by ‘X’) is fixed during the task (Franke et al., 1994). Hence, compared with the CPT-AX, the CPT-IP is highly sensitive in detecting a subtle performance deficit in various high-risk populations (Cornblatt et al., 1988; Cornblatt et al., 1989). During the CPT-IP, subjects should keep every stimulus presented in working memory until it can be compared with the one immediately following it (Cornblatt and Keilp, 1994). We suggest that the need for continuous emotional processing imposes a significant burden on CPT-IP performance in patients with schizophrenia. Interestingly, when the luminance of stimuli was modulated in a sustained attention task, non-clinical subjects showed improved performance when stimulus luminance was decreased (Blanco and Leiros, 2000). We found similar results in healthy control subjects, in which their d′ was higher when grey target stimuli were presented on the grey-oval background, compared with when bright-white target stimuli were presented on the same background stimuli. It has been suggested that, with a decrease of stimulus luminance, subjects may devote more attentional resources to the task in order to compensate lower visual quality (Blanco and Leiros, 2000). Another interesting finding in our present study was that healthy controls exhibited higher signal detection sensitivity (d′) when salient target stimuli were presented on the facial background than when the same stimuli were presented on the grey-oval background. Relatively improved CPT-IP performance in a variety of distraction conditions, compared with a non-distraction condition, has been reported by a number of studies (Cornblatt et al., 1988; Franke et al., 1994; Cosway et al., 2002; Gooding et al., 2006). Hence, in our study, control subjects might have allocated more attentional resources to the more demanding CPT-IP with facial background conditions than grey-oval background conditions. We have recently examined the effects of different background facial expressions (happy, neutral or sad) during a CPT-AX and found that happy faces produced a steeper signal detection sensitivity decline in patients (Park et al., 2011). However, because we did not include a non-facial background condition, it was not possible to address whether the presence of facial emotion background stimuli actually decreased CPT-AX performance. In our current study, because we used non-facial emotion background conditions, we could confirm that patients exhibited poorer CPT performance when happy faces were presented as background, compared with when the grey-oval stimulus was presented as background. An important question would be why patients were affected by background happy faces, whereas healthy controls were not. It is possible that the difficulty in happy face recognition in schizophrenia (Tsoi et al., 2008) took processing resources away from CPT-IP performance (Park et al., 2011). There are some limitations to this study. In this study, we used background happy faces only, and we did not include neutral faces. Hence, we are unable to tell whether our results were due to the attention-orienting nature of faces, or due to happy facial emotion expressions. However, our previous study found that happy faces (but not neutral faces) as background produced a significant distraction effect in patients in the same experimental set-up (Park et al., 2011). Furthermore, it was not practical to include neutral faces due to experimental time constraints, because participants already performed 4 tasks, each of them lasting 9 min. Another limitation of our study relates to the issue of generalized versus specific deficits in schizophrenia research. Since the facial emotion stimuli are more complex and visually distracting than the grey-oval background stimulus, our results can be attributed to the complexity of stimuli instead of their emotional content. This can be addressed in future studies.
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In conclusion, to our knowledge, the present study is the first to show that sustained attention in patients with schizophrenia may be aggravated in the presence of a facial background and the use of salient target stimuli may reduce the interfering effect of facial background. Hence, this study highlights the significance of stimulus salience during CPT-IP in schizophrenia. Role of funding source Funding has played no role in the realization of this report.
Contributors Sung-Hyouk Park and Jin Hun Kim designed the study. Jin-Chan Noh, Jaewon Lee, and Jin Young Park assisted with participant recruitment and administration of research protocol. Sung-Hyouk Park, and Kwang-Hyuk Lee wrote the protocol. Jaewon Lee, Jin Young Park, Young-Ryeol Lee, and Chan-Hyung Kim participated in the literature search and the discussion. All authors contributed to and have approved the final manuscript.
Conflict of interest All authors declare that they have no conflicts of interest relating to this study.
Acknowledgments The authors would like to thank Paul Ekman, Ph.D., for permission to use facial images. We thank all patients and controls who participated in the study.
References Addington, J., Addington, D., 1997. Attentional vulnerability indicators in schizophrenia and bipolar disorder. Schizophr. Res. 23, 197–204. Andreasen, N.C., 1984a. Scale for the Assessment of Negative Symptoms (SANS). University of Iowa, Iowa city. Andreasen, N.C., 1984b. Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa, Iowa city. Asarnow, R.F., MacCrimmon, D.J., 1978. Residual performance deficit in clinically remitted schizophrenics: a marker of schizophrenia? J. Abnorm. Psychol. 87, 597–608. Blanco, M.J., Leiros, L.I., 2000. Temporal variation in the luminance level of stimuli displayed on a cathode-ray tube monitor: effects on performance on a visual vigilance task. Ergonomics 43, 239–251. Cohen, R.A., Salloway, S., 1997. Neuropsychiatric Aspects of Disorders of Attention. In: Yudofsky, S.C., Hales, R.E. (Eds.), The American Psychiatric Press Textbook of Neuropsychiatry. American Psychiatric Press, Washington, DC, pp. 413–446. Cohen, A.S., Forbes, C.B., Mann, M.C., Blanchard, J.J., 2006. Specific cognitive deficits and differential domains of social functioning impairment in schizophrenia. Schizophr. Res. 81, 227–238. Cornblatt, B.A., Erlenmeyer-Kimling, L., 1985. Global attentional deviance as a marker of risk for schizophrenia: specificity and predictive validity. J. Abnorm. Psychol. 94, 470–486. Cornblatt, B.A., Keilp, J.G., 1994. Impaired attention, genetics, and the pathophysiology of schizophrenia. Schizophr. Bull. 20, 31–46. Cornblatt, B.A., Risch, N.J., Faris, G., Friedman, D., Erlenmeyer-Kimling, L., 1988. The Continuous Performance Test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families. Psychiatry Res 26, 223–238. Cornblatt, B.A., Lenzenweger, M.F., Erlenmeyer-Kimling, L., 1989. The continuous performance test, identical pairs version: II. Contrasting attentional profiles in schizophrenic and depressed patients. Psychiatry Res. 29, 65–85. Corwin, J., 1994. On measuring discrimination and response bias: unequal numbers of targets and distractors and two class of distractors. Neuropsychology 8, 110–117.
Cosway, R., Byrne, M., Clafferty, R., Hodges, A., Grant, E., Morris, J., et al., 2002. Sustained attention in young people at high risk for schizophrenia. Psychol. Med. 32, 277–286. Egan, M.F., Goldberg, T.E., Gscheidle, T., Weirich, M., Bigelow, L.B., Weinberger, D.R., 2000. Relative risk of attention deficits in siblings of patients with schizophrenia. Am. J. Psychiatry 157, 1309–1316. Ekman, P., Friesen, W.V., 1976. Pictures of Facial Affect. Consulting Psychologists Press, Palo Alto, CA. First, M., Spitzer, R.L., Gibbon, M., Williams, J.B.W., 1996. Structured Clinical Interview for DSM-IV Axis I Disorders: Patient Edition (SCID-I/P). Version 2. New York State Psychiatric Institute Biometric Research, New York. Franke, P., Maier, W., Hardt, J., Hain, C., Cornblatt, B.A., 1994. Attentional abilities and measures of schizotypy: their variation and covariation in schizophrenic patients, their siblings, and normal control subjects. Psychiatry Res. 54, 259–272. Gooding, D.C., Matts, C.W., Rollmann, E.A., 2006. Sustained attention deficits in relation to psychometrically identified schizotypy: evaluating a potential endophenotypic marker. Schizophr. Res. 82, 27–37. Green, M.F., Kern, R.S., Braff, D.L., Mintz, J., 2000. Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the "right stuff"? Schizophr. Bull. 26, 119–136. Kee, K.S., Kern, R.S., Green, M.F., 1998. Perception of emotion and neurocognitive functioning in schizophrenia: what's the link? Psychiatry Res. 81, 57–65. Keefe, R.S.E., Eesley, C.E., 2006. Neurocognitive impariments. In: Lieberman, J.A., Stroup, T.S., Perkins, D.O. (Eds.), Textbook of schizophrenia. American Psychiatric Publishing, Washington, DC, pp. 245–260. Kurtz, M.M., Ragland, J.D., Bilker, W., Gur, R.C., Gur, R.E., 2001. Comparison of the continuous performance test with and without working memory demands in healthy controls and patients with schizophrenia. Schizophr. Res. 48, 307–316. Lee, J., Park, S., 2006. The role of stimulus salience in CPT-AX performance of schizophrenia patients. Schizophr. Res. 81, 191–197. Liu, S.K., Chiu, C.H., Chang, C.J., Hwang, T.J., Hwu, H.G., Chen, W.J., 2002. Deficits in sustained attention in schizophrenia and affective disorders: stable versus statedependent markers. Am. J. Psychiatry 159, 975–982. Macmillan, N.A., Creelman, C.D., 1990. Response bias: characteristics of detection theory, threshold theory, and "nonparametric" indexes. Psychol. Bull. 107, 401–413. Mass, R., Wolf, K., Wagner, M., Haasen, C., 2000. Differential sustained attention/vigilance changes over time in schizophrenics and controls during a degraded stimulus Continuous Performance Test. Eur. Arch. Psychiatry Clin. Neurosci. 250, 24–30. Nestor, P.G., Faux, S.F., McCarley, R.W., Shenton, M.E., Sands, S.F., 1990. Measurement of visual sustained attention in schizophrenia using signal detection analysis and a newly developed computerized CPT task. Schizophr. Res. 3, 329–332. Nuechterlein, K.H., 1983. Signal detection in vigilance tasks and behavioral attributes among offspring of schizophrenic mothers and among hyperactive children. J. Abnorm. Psychol. 92, 4–28. Nuechterlein, K.H., Edell, W.S., Norris, M., Dawson, M.E., 1986. Attentional vulnerability indicators, thought disorder, and negative symptoms. Schizophr. Bull. 12, 408–426. Nuechterlein, K.H., Dawson, M.E., Gitlin, M., Ventura, J., Goldstein, M.J., Snyder, K.S., et al., 1992. Developmental Processes in Schizophrenic Disorders: longitudinal studies of vulnerability and stress. Schizophr. Bull. 18, 387–425. Park, S.H., Kim, J.J., Kim, C.H., Kim, J.H., Lee, K.H., 2011. Sustained attention in the context of emotional processing in patients with schizophrenia. Psychiatry Res. 187, 18–23. Sergi, M.J., Rassovsky, Y., Nuechterlein, K.H., Green, M.F., 2006. Social perception as a mediator of the influence of early visual processing on functional status in schizophrenia. Am. J. Psychiatry 163, 448–454. Tsoi, D.T., Lee, K.H., Khokhar, W.A., Mir, N.U., Swalli, J.S., Gee, K.A., et al., 2008. Is facial emotion recognition impairment in schizophrenia identical for different emotions? A signal detection analysis. Schizophr. Res. 99, 263–269. Velligan, D.I., Bow-Thomas, C.C., Mahurin, R.K., Miller, A.L., Halgunseth, L.C., 2000. Do specific neurocognitive deficits predict specific domains of community function in schizophrenia? J. Nerv. Ment. Dis. 188, 518–524. Wohlberg, G.W., Kornetsky, C., 1973. Sustained attention in remitted schizophrenics. Arch. Gen. Psychiatry 28, 533–537.
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Interactive effects of background facial emotion stimulus and target salience on sustained attention performance in schizophrenia Sung-Hyouk Park a,⁎, Jin-Chan Noh b, Jin Hun Kim c, Jaewon Lee b, Jin Young Park b, d, Young-Ryeol Lee b, Chan-Hyung Kim d, Kwang-Hyuk Lee e a
Department of Psychiatry, Chookryoung Evangelical Hospital, Namyangju, Gyeonggi, South Korea Department of Psychiatry, Gongju National Hospital, Gongju, Chungnam, South Korea Department of Psychiatry, Ansan Hyo Silver Hospital, Ansan, Gyeonggi, South Korea d Department of Psychiatry, Yonsei University College of Medicine, Seoul, South Korea e Academic Clinical Psychiatry, Department of Neuroscience, School of Medicine and Biomedical Sciences, University of Sheffield, Sheffield, United Kingdom b c
a r t i c l e
i n f o
Article history: Received 29 March 2011 Received in revised form 26 October 2011 Accepted 14 November 2011 Available online 3 December 2011 Keywords: Schizophrenia Attention Face Emotion Salience
a b s t r a c t Schizophrenia impairs both facial emotion processing and sustained attention. Through separate studies, it is known that the presence of a task-irrelevant facial stimulus disproportionately interferes with performance, whereas increasing the salience of task stimulus improves performance during a sustained attention task in patients with schizophrenia. We wished to investigate a potential interaction effect of background facial emotion expression (black and white happy faces vs. grey oval) and target stimulus salience (bright white vs. grey) using the Continuous Performance Test-Identical Pairs version (CPT-IP) in patients with schizophrenia. Thirty-six patients with schizophrenia and 28 healthy control subjects completed 4 different versions of the CPT-IP. We found that healthy controls exhibited higher signal detection sensitivity (d′) when salient target stimuli were presented on the facial background than when the same stimuli were presented on the greyoval background. By contrast, patients were not affected by background stimuli when target number stimuli were salient. When target number stimuli were not salient, both patients and controls showed higher d′ in the grey-oval background condition compared with the facial background condition. This study highlight the significance of stimulus salience during CPT-IP in schizophrenia as background stimuli did not produce a differential effect on performance. Our results suggest that, in the situations where facial emotion stimuli are present, patients' sustained attention can be deteriorated and that the use of salient materials is important in improving performance in schizophrenia. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Sustained attention refers to the ability to remain vigilant over a long period of time in order to prepare and maintain readiness for responses. Patients with schizophrenia exhibit a sustained attention deficit across various stages of the illness (Wohlberg and Kornetsky, 1973; Asarnow and MacCrimmon, 1978; Nuechterlein et al., 1992; Addington and Addington, 1997; Liu et al., 2002). Sustained attention deficit can result in an inability to follow social and work-related conversations and important instructions regarding treatment in patients with schizophrenia (Keefe and Eesley, 2006). Consistent with this, previous studies have shown that sustained attention deficit is closely related to functional outcome in schizophrenia (Green et al., 2000).
⁎ Corresponding author at: Department of Psychiatry, Chookryoung Evangelical Hospital, 174-3, Oebang-ri, Sudong-myeon, Namyangju, Gyeonggi, 472-853, South Korea. Tel.: + 82 31 592 6661; fax: + 82 31 592 6755. E-mail address: [email protected] (S.-H. Park). 0920-9964/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2011.11.019
The continuous performance test (CPT) is one of the most widely used measures of sustained attention deficit in schizophrenia (Nuechterlein, 1983; Cornblatt and Erlenmeyer-Kimling, 1985; Nuechterlein et al., 1986; Cornblatt et al., 1989; Nestor et al., 1990; Mass et al., 2000; Liu et al., 2002; Lee and Park, 2006; Park et al., 2011). The test requires subjects to focus their attention continuously in order to respond whenever the letter X appears (CPT-X), or to respond only when the letter A precedes the letter X (CPT-AX) (Wohlberg and Kornetsky, 1973). During these CPTs, subjects are required to sustain their attention to stimuli presented on a blank screen. Considering that problems in emotional and social functioning are a critical feature of schizophrenia, it is important to understand sustained attention deficit in a social context. The association between neurocognitive and emotional/social deficits has been investigated in previous studies (Kee et al., 1998; Cohen et al., 2006; Sergi et al., 2006). For example, Kee et al. (1998) reported that performance on the Span of Apprehension task, a measure of early visual processing, was correlated with performance on a facial emotion identification task. Furthermore, there is evidence that
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neurocognitive deficits are closely related to social deficits (Green et al., 2000; Velligan et al., 2000; Cohen et al., 2006, but see Addington and Addington, 1997 for evidence against this). However, there have been few studies demonstrating the link between neurocognitive and emotional deficits through an experimental manipulation. We have recently examined CPT-AX performance in the context of facial emotion processing in schizophrenia (Park et al., 2011). In that study, we wished to examine a potential interaction between sustained attention and emotion processing in patients. We presented CPT-AX number stimuli superimposed on the nose of background facial expressions (happy, sad or neutral), because faces provide the most common source of social context. Patients showed a steeper signal detection sensitivity decline when happy faces were presented as background stimuli. By contrast, healthy controls' sensitivity was not affected by background facial emotion stimuli. Our study suggests that the need for continuous emotional processing, especially for happy faces, imposes a significant burden on CPT-AX performance in patients with schizophrenia. It is important to consider why patients showed a significant performance decline when our target number stimuli were superimposed onto happy faces. Our number stimuli had a grayscale intensity of 40% in order to increase task difficulty (i.e., grey target color against grey facial background). Hence, the effect of lowering target luminance would be similar to those observed with the degraded-stimulus CPT, by increasing demand on early visual stimulus-encoding and analysis processes. However, this does not explain why patients showed a performance decline only when background happy faces (but not sad or neutral faces) were used as background. We suspect that the distraction effect of happy faces may have an interaction effect with target stimulus salience. In fact, there are some previous studies showing that patients benefited more than healthy controls when a target stimulus was preceded by a salient cue in a CPT-AX (red ‘A’ followed by target ‘X’) (Lee and Park, 2006). Hence, we hypothesized that patients would not show a decline in performance when target stimuli were salient, but they would show a performance deficit when target stimuli were nonsalient. In the present study, we have extended our previous study to investigate the role of background facial expressions (facial oval vs. grey oval) and target stimulus salience (bright white vs. grey) using the CPT-Identical Pairs version (CPT-IP). The CPT-IP requires subjects to respond as quickly as possible to any consecutive presentation of identical stimuli (Cornblatt et al., 1988). We used background happy faces only, because presenting happy faces as background produced a significant CPT performance decline in schizophrenia patients in our previous study (Park et al., 2011). To manipulate target stimulus salience, we set the grayscale intensity of target stimuli to 0% (salient bright white against grey background) or 40% (non-salient grey). 2. Methods
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Twenty-eight healthy control participants (14 males and 14 females) were recruited from hospital personnel. They were carefully interviewed by a trained psychiatrist (JCN) to exclude any Axis I disorder in themselves or first-degree relatives. Neither mean age nor years of education were significantly different between the groups (see Table 1 for details). After complete description of the study to the participants, written informed consent was obtained. The study was approved by Gongju National Hospital Institutional Research Ethics Review Board. 2.2. CPT-IP We used a block design. In a 2 by 2 factorial task design, there were four separate experimental conditions: the CPT-IP with facial background and grey number stimulus condition, the CPT-IP with facial background and bright white number stimulus condition, the CPT-IP with grey-oval background and grey number stimulus condition, and the CPT-IP with grey-oval background and bright white number stimulus condition. In each condition, there were 540 trials lasting 9 min. Of these, 81 (15%) number stimuli were target stimuli. Subjects had a break between the conditions. The order of the conditions was counterbalanced across participants in each group. Background face stimuli were all happy faces and chosen from Ekman and Friesen's Pictures of Facial Affect (Ekman and Friesen, 1976). Hair features and clothing were occluded to form an oval shape (Tsoi et al., 2008). During facial background conditions, number stimuli appeared on the nose of the background facial stimulus (see Fig. 1). Two-digit numbers were used as target and non-target stimuli. The grey-oval background stimulus was constructed to be the same size as the facial stimuli and had an average luminance of all facial stimuli. Subjects were asked to press the left mouse button whenever there was any consecutive presentation of identical number stimuli. Stimuli were presented at a constant rate of one per second as with other CPT studies in schizophrenia (Cornblatt et al., 1989; Kurtz et al., 2001). During facial background conditions, each pair of stimuli (a number and a face oval) appeared for the first 50 ms followed by just the face for the remaining 950 ms to allow a response to be made to the target. The background face therefore remained on the screen for the entire trial duration of 1 s. During grey-oval background conditions, a grey oval background was used, instead of the background face. Subjects sat approximately 60 cm from the screen. The large diameter of the face oval and grey-oval was 160 mm and the small diameter of them was 120 mm. The face oval and the grey-oval stimuli were presented in the center of screen. The number stimuli were presented in size 25 Arial font. A PC running E-Prime 2.0 (Psychology software Table 1 Demographic data.
2.1. Participants
Normal control (n = 28)
Schizophrenic patient (n = 36)
Analysis
Thirty-six patients with schizophrenia (18 males and 18 females) were recruited from Gongju National Hospital, Gongju, Chungnam, South Korea. A diagnosis of schizophrenia was confirmed using the Structured Clinical Interview for Axis I DSM–IV Disorders — Patient Edition (SCID–I/P)(First et al., 1996). Exclusion criteria were diagnosis of an Axis I disorder other than schizophrenia, neurological disorders, or mental retardation. At the time of testing, patients were treated with atypical (n = 33) or both typical and atypical neuroleptics (n = 3) at an average dose of 539.33 ± 328.85 chloropromazine equivalents per day. Schizophrenia symptoms were rated using the Scale for the Assessment of Negative Symptoms (Andreasen, 1984a) and the Scale for the Assessment of Positive Symptoms (Andreasen, 1984b).
N(%), mean (SD)
N(%), mean (SD)
χ² , t
p-value
14/14 33.11 14.36 84.23
18/18 36.33 13.72 86.41 9.81 6.42 40.53 6.03
χ² = 0.00 t = 1.66 t = − 1.14 t = 1.70
1 0.10 0.25 0.09
Sex (m/f) Age Education (yr) EHI SANS SAPS GAF score Admission number DOI (yr)
(50/50) (8.58) (1.76) (4.67)
(50/50) (6.96) (2.48) (5.37) (5.00) (2.85) (5.42) (4.08)
10.0 (5.57)
Abbreviation: EHI, Edinburgh Handedness Inventory; SANS, Scale for the Assessment of Negative Symptoms; SAPS, Scale for the Assessment of Positive Symptoms; GAF, Global Assessment of Functioning scale; DOI, Duration Of Illness.
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stimulus recognition, i.e., the ability to distinguish target from nontarget. A higher d′ value indicates better performance. We first present 3-way repeated measure ANOVA results for d′ and reaction time. The between-subject factor was group (patients vs. controls). The within-subject factors were background (face oval vs. grey oval) and luminance of stimuli (bright white vs. grey). 3. Results 3.1. Sensitivity (d′)
Fig. 1. Stimuli and trial sequence in the CPT-IP.Facial stimuli used as background are copyrighted by Paul Ekman, Ph.D.
tools, Inc., Pittsburgh, PA; http://pstnet.com) controlled experimental events and recorded data. 2.3. Data analysis We calculated d′ as a signal detection sensitivity index. The calculation of d′ was based on the formula reported in the paper by Macmillan and Creelman (1990). Because our data included the hit rate of 1.0 and false alarm rate of 0, calculating d′ would produce the problem of division by zero. To avoid the problem of division by zero, it is necessary to adjust hit and false alarm rate (Corwin, 1994). The sensitivity measure d′ refers to the sensory dimension of
The main effect of group was significant, indicating that d′ of patients was significantly lower than that of control subjects (F1,62 = 68.332, p b 0.001). Neither the main effect of background (F1,62 = 2.810, p = 0.099) nor the main effect of luminance was significant (F1,62 = 0.109, p = 0.743) (Table 2). There was a significant interaction between background and group on d′ (F1,62 = 4.778, p = 0.033). Post hoc analysis revealed that the d′ of patients was lower with facial background condition compared with the grey-oval background condition (p b 0.01), whereas d′ of controls was not different between the two background conditions (p = 0.735). The interaction between target number luminance and group was not significant (F1,62 = 0.532, p = 0.468). A significant interaction effect that did not involve the group factor was the interaction between background and stimulus luminance (F1,62 = 35.155, p b 0.001). Post hoc analysis showed that d′ was lower with face oval background than with grey-oval background when number stimuli were in grey (p b 0.001). d′ was higher when bright white (vs. grey) target stimuli were presented on the facial background (p b 0.001). The reverse was also significant: d′ was higher when grey (vs. bright white) target stimuli were presented on the grey-oval background (p = 0.024). There was a significant 3-way interaction between background, target luminance, and group (F1,62 = 7.065, p = 0.010). Post hoc analysis revealed that healthy controls exhibited a cross-over interaction effect between background and luminance (Fig. 2): Their d′ was higher with grey-oval background than with facial background in the grey number stimulus conditions (p= 0.024). The reverse was also significant: their d′ was higher when bright white number stimuli were presented on the facial background than on the grey-oval background (p b 0.001). By contrast, patients with schizophrenia were not affected by background stimuli when the number stimuli were salient (i.e., no significant d′ difference between the facial background condition and the grey-oval background condition). When the number stimuli were in grey, patients showed higher d′ in the grey-oval background condition than in the facial background condition (p = 0.002), as was seen in controls. 3.2. Reaction time There was a significant main effect of group, suggesting that reaction time of patients was longer than that of controls (F1,62 = 48.579, p b 0.001). The main effect of background was significant (F1,62 = 11.337, p b 0.001), indicating that reaction time for the facial
Table 2 CPT performance indices in each experimental condition. Hit rate Experimental condition Facial background Grey stimulus Facial background Bright white stimulus Grey-oval background Grey stimulus Grey-oval background Bright white stimulus
SPR (n = 36) NC(n = 28) SPR (n = 36) NC (n = 28) SPR (n = 36) NC (n = 28) SPR (n = 36) NC (n = 28)
Abbreviation: SPR, Schizophrenia; NC, normal control.
False alarm rate
Sensitivity (d′)
Reaction time (ms)
Mean
(SD)
Mean
(SD)
Mean
(SD)
Mean
(SD)
0.515 0.932 0.563 0.930 0.635 0.939 0.631 0.929
(0.231) (0.063) (0.233) (0.052) (0.243) (0.066) (0.235) (0.053)
0.012 0.012 0.010 0.004 0.010 0.016 0.011 0.023
(0.016) (0.040) (0.012) (0.014) (0.012) (0.073) (0.010) (0.099)
2.490 4.122 2.673 4.434 2.868 4.422 2.797 4.067
(0.858) (0.710) (0.819) (0.623) (0.980) (0.938) (0.849) (0.751)
558.553 442.843 528.131 427.746 527.703 428.606 520.669 425.595
(84.493) (58.264) (71.022) (49.436) (70.772) (43.703) (68.708) (50.340)
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Fig. 2. Signal detection sensitivity (d′) in 4 task conditions in patients with schizophrenia and healthy controlsError bars show 95% confidence intervals.Abbreviations: FG, Facial background and grey number condition; FB, Facial background and bright-white number condition; GG, Grey-oval background and grey number condition; GB, Grey-oval background and bright-white number condition.
background condition was longer than that for the grey-oval background condition. The main effect of stimulus luminance was also significant (F1,62 = 10.086, p = 0.002), suggesting that reaction time to grey stimuli was longer than that for bright white stimuli. There was a significant interaction between background and luminance of number stimuli (F1,62 = 5.157, p = 0.027). Post hoc analysis showed that reaction time was significantly longer when the grey number stimuli were presented on the facial background compared with the grey-oval background condition (p b 0.001). By contrast, there was no significant difference in reaction time according to background in the bright white stimulus conditions (p = 0.396). Neither the interaction between luminance of number stimuli and group (F1,62 = 1.223, p = 0.273) nor the interaction between background and group (F1,62 = 1.821, p = 0.182) was significant. The 3-way interaction between background, luminance of stimuli, and group was not significant (F1,62 = 0.523, p = 0.472). 4. Discussion In the present study, we investigated the impact of stimulus salience (bright white vs. grey) on different background stimuli (facial emotion expressions vs. grey-oval) using the CPT-Identical Pairs version (CPT-IP). We found that when the number stimuli were not salient (in grey), patients with schizophrenia, similar to healthy subjects, showed lower signal detection sensitivity (d′) in the facial background condition, compared with the grey-oval background condition. However, when the number stimuli were salient (in bright white), patients were not differentially affected by background stimuli. These findings suggest that increased stimulus salience may be helpful for patients to overcome the interfering effect of facial background stimuli during the CPT-IP. This is consistent with a previous study where the stimulus salience aided CPT-AX performance in patients with schizophrenia (Lee and Park, 2006). Our study extended the effect of stimulus salience to an experimental situation where socially-relevant, facial emotion expressions were involved. CPT performance is affected by the relationship between target and non-target stimuli and the nature of cognitive operations that are required (Cohen and Salloway, 1997). In order to lower the discriminability of target and non-target stimuli, previous studies have used various distracters. Patients with schizophrenia exhibited especially poor CPT performance with distracters (Franke et al., 1994; Egan et al., 2000; Cosway et al., 2002). In our study, the background happy faces would function as distracters, as in our previous study(Park et al., 2011). Our finding of a significant interaction between background and group suggests that patients were more vulnerable to the distracting effect of background happy faces. This distraction
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effect was consistent with previous studies using number stimuli in a CPT (Franke et al., 1994; Egan et al., 2000; Cosway et al., 2002). Cognitive operations required in performing the CPT-IP are more demanding than in performing the CPT-AX, because targets can be changed from trial to trial in the CPT-IP, whereas the target in the CPT-AX (‘A’ followed by ‘X’) is fixed during the task (Franke et al., 1994). Hence, compared with the CPT-AX, the CPT-IP is highly sensitive in detecting a subtle performance deficit in various high-risk populations (Cornblatt et al., 1988; Cornblatt et al., 1989). During the CPT-IP, subjects should keep every stimulus presented in working memory until it can be compared with the one immediately following it (Cornblatt and Keilp, 1994). We suggest that the need for continuous emotional processing imposes a significant burden on CPT-IP performance in patients with schizophrenia. Interestingly, when the luminance of stimuli was modulated in a sustained attention task, non-clinical subjects showed improved performance when stimulus luminance was decreased (Blanco and Leiros, 2000). We found similar results in healthy control subjects, in which their d′ was higher when grey target stimuli were presented on the grey-oval background, compared with when bright-white target stimuli were presented on the same background stimuli. It has been suggested that, with a decrease of stimulus luminance, subjects may devote more attentional resources to the task in order to compensate lower visual quality (Blanco and Leiros, 2000). Another interesting finding in our present study was that healthy controls exhibited higher signal detection sensitivity (d′) when salient target stimuli were presented on the facial background than when the same stimuli were presented on the grey-oval background. Relatively improved CPT-IP performance in a variety of distraction conditions, compared with a non-distraction condition, has been reported by a number of studies (Cornblatt et al., 1988; Franke et al., 1994; Cosway et al., 2002; Gooding et al., 2006). Hence, in our study, control subjects might have allocated more attentional resources to the more demanding CPT-IP with facial background conditions than grey-oval background conditions. We have recently examined the effects of different background facial expressions (happy, neutral or sad) during a CPT-AX and found that happy faces produced a steeper signal detection sensitivity decline in patients (Park et al., 2011). However, because we did not include a non-facial background condition, it was not possible to address whether the presence of facial emotion background stimuli actually decreased CPT-AX performance. In our current study, because we used non-facial emotion background conditions, we could confirm that patients exhibited poorer CPT performance when happy faces were presented as background, compared with when the grey-oval stimulus was presented as background. An important question would be why patients were affected by background happy faces, whereas healthy controls were not. It is possible that the difficulty in happy face recognition in schizophrenia (Tsoi et al., 2008) took processing resources away from CPT-IP performance (Park et al., 2011). There are some limitations to this study. In this study, we used background happy faces only, and we did not include neutral faces. Hence, we are unable to tell whether our results were due to the attention-orienting nature of faces, or due to happy facial emotion expressions. However, our previous study found that happy faces (but not neutral faces) as background produced a significant distraction effect in patients in the same experimental set-up (Park et al., 2011). Furthermore, it was not practical to include neutral faces due to experimental time constraints, because participants already performed 4 tasks, each of them lasting 9 min. Another limitation of our study relates to the issue of generalized versus specific deficits in schizophrenia research. Since the facial emotion stimuli are more complex and visually distracting than the grey-oval background stimulus, our results can be attributed to the complexity of stimuli instead of their emotional content. This can be addressed in future studies.
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In conclusion, to our knowledge, the present study is the first to show that sustained attention in patients with schizophrenia may be aggravated in the presence of a facial background and the use of salient target stimuli may reduce the interfering effect of facial background. Hence, this study highlights the significance of stimulus salience during CPT-IP in schizophrenia. Role of funding source Funding has played no role in the realization of this report.
Contributors Sung-Hyouk Park and Jin Hun Kim designed the study. Jin-Chan Noh, Jaewon Lee, and Jin Young Park assisted with participant recruitment and administration of research protocol. Sung-Hyouk Park, and Kwang-Hyuk Lee wrote the protocol. Jaewon Lee, Jin Young Park, Young-Ryeol Lee, and Chan-Hyung Kim participated in the literature search and the discussion. All authors contributed to and have approved the final manuscript.
Conflict of interest All authors declare that they have no conflicts of interest relating to this study.
Acknowledgments The authors would like to thank Paul Ekman, Ph.D., for permission to use facial images. We thank all patients and controls who participated in the study.
References Addington, J., Addington, D., 1997. Attentional vulnerability indicators in schizophrenia and bipolar disorder. Schizophr. Res. 23, 197–204. Andreasen, N.C., 1984a. Scale for the Assessment of Negative Symptoms (SANS). University of Iowa, Iowa city. Andreasen, N.C., 1984b. Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa, Iowa city. Asarnow, R.F., MacCrimmon, D.J., 1978. Residual performance deficit in clinically remitted schizophrenics: a marker of schizophrenia? J. Abnorm. Psychol. 87, 597–608. Blanco, M.J., Leiros, L.I., 2000. Temporal variation in the luminance level of stimuli displayed on a cathode-ray tube monitor: effects on performance on a visual vigilance task. Ergonomics 43, 239–251. Cohen, R.A., Salloway, S., 1997. Neuropsychiatric Aspects of Disorders of Attention. In: Yudofsky, S.C., Hales, R.E. (Eds.), The American Psychiatric Press Textbook of Neuropsychiatry. American Psychiatric Press, Washington, DC, pp. 413–446. Cohen, A.S., Forbes, C.B., Mann, M.C., Blanchard, J.J., 2006. Specific cognitive deficits and differential domains of social functioning impairment in schizophrenia. Schizophr. Res. 81, 227–238. Cornblatt, B.A., Erlenmeyer-Kimling, L., 1985. Global attentional deviance as a marker of risk for schizophrenia: specificity and predictive validity. J. Abnorm. Psychol. 94, 470–486. Cornblatt, B.A., Keilp, J.G., 1994. Impaired attention, genetics, and the pathophysiology of schizophrenia. Schizophr. Bull. 20, 31–46. Cornblatt, B.A., Risch, N.J., Faris, G., Friedman, D., Erlenmeyer-Kimling, L., 1988. The Continuous Performance Test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families. Psychiatry Res 26, 223–238. Cornblatt, B.A., Lenzenweger, M.F., Erlenmeyer-Kimling, L., 1989. The continuous performance test, identical pairs version: II. Contrasting attentional profiles in schizophrenic and depressed patients. Psychiatry Res. 29, 65–85. Corwin, J., 1994. On measuring discrimination and response bias: unequal numbers of targets and distractors and two class of distractors. Neuropsychology 8, 110–117.
Cosway, R., Byrne, M., Clafferty, R., Hodges, A., Grant, E., Morris, J., et al., 2002. Sustained attention in young people at high risk for schizophrenia. Psychol. Med. 32, 277–286. Egan, M.F., Goldberg, T.E., Gscheidle, T., Weirich, M., Bigelow, L.B., Weinberger, D.R., 2000. Relative risk of attention deficits in siblings of patients with schizophrenia. Am. J. Psychiatry 157, 1309–1316. Ekman, P., Friesen, W.V., 1976. Pictures of Facial Affect. Consulting Psychologists Press, Palo Alto, CA. First, M., Spitzer, R.L., Gibbon, M., Williams, J.B.W., 1996. Structured Clinical Interview for DSM-IV Axis I Disorders: Patient Edition (SCID-I/P). Version 2. New York State Psychiatric Institute Biometric Research, New York. Franke, P., Maier, W., Hardt, J., Hain, C., Cornblatt, B.A., 1994. Attentional abilities and measures of schizotypy: their variation and covariation in schizophrenic patients, their siblings, and normal control subjects. Psychiatry Res. 54, 259–272. Gooding, D.C., Matts, C.W., Rollmann, E.A., 2006. Sustained attention deficits in relation to psychometrically identified schizotypy: evaluating a potential endophenotypic marker. Schizophr. Res. 82, 27–37. Green, M.F., Kern, R.S., Braff, D.L., Mintz, J., 2000. Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the "right stuff"? Schizophr. Bull. 26, 119–136. Kee, K.S., Kern, R.S., Green, M.F., 1998. Perception of emotion and neurocognitive functioning in schizophrenia: what's the link? Psychiatry Res. 81, 57–65. Keefe, R.S.E., Eesley, C.E., 2006. Neurocognitive impariments. In: Lieberman, J.A., Stroup, T.S., Perkins, D.O. (Eds.), Textbook of schizophrenia. American Psychiatric Publishing, Washington, DC, pp. 245–260. Kurtz, M.M., Ragland, J.D., Bilker, W., Gur, R.C., Gur, R.E., 2001. Comparison of the continuous performance test with and without working memory demands in healthy controls and patients with schizophrenia. Schizophr. Res. 48, 307–316. Lee, J., Park, S., 2006. The role of stimulus salience in CPT-AX performance of schizophrenia patients. Schizophr. Res. 81, 191–197. Liu, S.K., Chiu, C.H., Chang, C.J., Hwang, T.J., Hwu, H.G., Chen, W.J., 2002. Deficits in sustained attention in schizophrenia and affective disorders: stable versus statedependent markers. Am. J. Psychiatry 159, 975–982. Macmillan, N.A., Creelman, C.D., 1990. Response bias: characteristics of detection theory, threshold theory, and "nonparametric" indexes. Psychol. Bull. 107, 401–413. Mass, R., Wolf, K., Wagner, M., Haasen, C., 2000. Differential sustained attention/vigilance changes over time in schizophrenics and controls during a degraded stimulus Continuous Performance Test. Eur. Arch. Psychiatry Clin. Neurosci. 250, 24–30. Nestor, P.G., Faux, S.F., McCarley, R.W., Shenton, M.E., Sands, S.F., 1990. Measurement of visual sustained attention in schizophrenia using signal detection analysis and a newly developed computerized CPT task. Schizophr. Res. 3, 329–332. Nuechterlein, K.H., 1983. Signal detection in vigilance tasks and behavioral attributes among offspring of schizophrenic mothers and among hyperactive children. J. Abnorm. Psychol. 92, 4–28. Nuechterlein, K.H., Edell, W.S., Norris, M., Dawson, M.E., 1986. Attentional vulnerability indicators, thought disorder, and negative symptoms. Schizophr. Bull. 12, 408–426. Nuechterlein, K.H., Dawson, M.E., Gitlin, M., Ventura, J., Goldstein, M.J., Snyder, K.S., et al., 1992. Developmental Processes in Schizophrenic Disorders: longitudinal studies of vulnerability and stress. Schizophr. Bull. 18, 387–425. Park, S.H., Kim, J.J., Kim, C.H., Kim, J.H., Lee, K.H., 2011. Sustained attention in the context of emotional processing in patients with schizophrenia. Psychiatry Res. 187, 18–23. Sergi, M.J., Rassovsky, Y., Nuechterlein, K.H., Green, M.F., 2006. Social perception as a mediator of the influence of early visual processing on functional status in schizophrenia. Am. J. Psychiatry 163, 448–454. Tsoi, D.T., Lee, K.H., Khokhar, W.A., Mir, N.U., Swalli, J.S., Gee, K.A., et al., 2008. Is facial emotion recognition impairment in schizophrenia identical for different emotions? A signal detection analysis. Schizophr. Res. 99, 263–269. Velligan, D.I., Bow-Thomas, C.C., Mahurin, R.K., Miller, A.L., Halgunseth, L.C., 2000. Do specific neurocognitive deficits predict specific domains of community function in schizophrenia? J. Nerv. Ment. Dis. 188, 518–524. Wohlberg, G.W., Kornetsky, C., 1973. Sustained attention in remitted schizophrenics. Arch. Gen. Psychiatry 28, 533–537.