- Email: [email protected]
Deficits in facial affect recognition in unaffected siblings of Xhosa schizophrenia patients: Evidence for a neurocognitive endophenotype
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Schizophrenia Research 99 (2008) 270 – 273 www.elsevier.com/locate/schres
Deficits in facial affect recognition in unaffected siblings of Xhosa schizophrenia patients: Evidence for a neurocognitive endophenotype Jukka M. Leppänen a,⁎, Dana J.H. Niehaus b , Liezl Koen b , Elsa Du Toit b , Renata Schoeman b , Robin Emsley b a
Human Information Processing Laboratory, Department of Psychology, FIN-33014 University of Tampere, Tampere, Finland b Ngaphakathi Workgroup, Department of Psychiatry, University of Stellenbosch, South Africa Received 7 August 2007; received in revised form 19 October 2007; accepted 2 November 2007 Available online 4 December 2007
Abstract The present study in an African Xhosa sample examined whether familial vulnerability to schizophrenia is associated with deficits in facial affect recognition. Healthy comparison subjects, unaffected siblings of schizophrenia patients, and schizophrenia patients were tested with a task requiring rapid recognition of matched positive (happy), negative (angry), and neutral facial expressions. Siblings and patients demonstrated impaired recognition of negative relative to positive facial expressions whereas comparison subjects recognized negative and positive expressions at an equal level of accuracy. These results suggest that deficits in the processing negative affect from social cues are transmitted in families and may represent a heritable endophenotype of schizophrenia. © 2007 Elsevier B.V. All rights reserved. Keywords: Schizophrenia; Facial expression; Recognition; Endophenotype
1. Introduction Schizophrenia is associated with deficits in the processing of affective information from facial expressions and other social cues (Bediou et al., 2005; Edwards et al., 2001). These deficits may contribute to poor social functioning in schizophrenia patients (Brekke et al., 2005), and have been identified as an important target for clinical intervention (Wolwer et al., 2005).
⁎ Corresponding author. Tel.: +358 3 3551 6537; fax: +358 3 3551 7710. E-mail address: [email protected] (J.M. Leppänen). 0920-9964/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2007.11.003
There has been increasing interest in the possibility that instead of secondary factors associated with chronic illness, deficits in the recognition of affective cues may in fact reflect a heritable endophenotype that is related to a genetic vulnerability to schizophrenia (Gur et al., 2007). A critical feature of such endophenotypic deficits is that they are found not only in affected individuals, but also in unaffected relatives of schizophrenia patients. A few studies have examined facial affect recognition in relatives of schizophrenia patients but, to date, the evidence for clear vulnerability-linked deficits is scarce (Bölte and Poustka, 2003; Kee et al., 2004; Toomey et al., 1999). One possible explanation for the lack of clear findings is that rather than a broad
J.M. Leppänen et al. / Schizophrenia Research 99 (2008) 270–273
impairment in facial affect recognition, schizophrenia vulnerability may be associated with a more selective deficit with greater impairments for negative than positive facial expressions (Bediou et al., 2005; Edwards et al., 2001). To examine the possibility that such deficits are more likely to be revealed through measures that allow for separate assessment of the recognition of positive and negative facial expressions than measures that rely on average indices of affect recognition performance, and to extend the investigation of vulnerability-linked neurocognitive deficits to nonCaucasian populations, we investigated emotion recognition in unaffected siblings of schizophrenia patients in an African Xhosa sample. We specifically tested the hypothesis that unaffected siblings exhibit a pattern of impaired recognition of angry relative to happy facial expressions, and that this finding would be similar to that found in patients affected by schizophrenia (Leppänen et al., 2006). 2. Methods and materials 71 participants were included: 22 healthy comparison subjects, 23 siblings of schizophrenia patients, and 36 patients with schizophrenia. Schizophrenia patients were recruited from clinics in the wider Cape Town area, South Africa, as part of a large genetic study. To be included, participants had to be at least 18 years of age, of Xhosa origin (4/4 grandparents reported as Xhosa), reside in the Cape Town metropolitan area, and fulfill a diagnosis of schizophrenia according to DSM-IV-TR criteria (for details of clinical assessment, see Niehaus et al., 2005). Participants in the unaffected sibling group shared both biological parents with a patient diagnosed with schizophrenia. Healthy controls were recruited via word-of-mouth from the same geographical area as the patients and siblings. Exclusion criteria for siblings and controls included a history of psychiatric disorders or treatment (Sheehan et al., 1998), mental retardation, visual or auditory impairment, or significant medical illness (n = 7 excluded). One additional participant from the control group was excluded due to family history of psychiatric illnesses (n = 1). Demographic information for patients, siblings, and comparison subjects are presented in Table 1. The three groups differed significantly in gender distribution, but differences in age and level of education were not statistically significant. Written informed consent was obtained from all participants according to guidelines of the institutional review board of the University of Stellenbosch. Participants completed two computerized tasks assessing facial affect recognition and visual attention.
271
Table 1 Demographic information for schizophrenic patients, unaffected siblings and healthy comparison subjects (standard deviations are shown in parentheses) Variable
Patients
Siblings
Controls
Statistical test
Sex
10F/26M
15F/8M
11F/11M
Age
41.8 (10.4)
36.0 (13.0)
40.9 (10.3)
Education
5.5 (3.1)
6.2 (2.9)
6.0 (3.1)
χ2 = 8.4, df = 2, p b .02 F(2, 78) = 2.0, p = .14 F(2, 75) = 0.4, p = .65
The data from the visual attention task are not reported here. The affect recognition task was intended to measure rapid perceptual discrimination of matched positive (happy), negative (angry), and neutral facial expressions and has been described in detail elsewhere (Leppänen et al., 2006). A task with short stimuluspresentation duration (200 ms) was used to better approximate the automatic nature of facial affect perception and the brief duration of facial expressions in everyday life. Participants were presented with low (closed-mouth) and high-intensity (open-mouth) happy and angry expressions, and closed- and open-mouth neutral expressions selected from the MacBrain Face Stimulus Set1. The facial images were presented in random order in the center of the computer with a 200ms stimulus presentation time and a 2800-ms interstimulus interval (using E-prime software, Psychology Software Tools, Inc.). A total of 64 happy, 64 angry, and 64 neutral facial expressions were presented (4 repetitions of each individual facial expression picture). The subjects were asked to respond by pressing one of the choice buttons (on a computer mouse) when a happy or angry face was presented, and not to respond when a neutral face was presented. The buttons were labeled from left to right in two different orders; happy–angry and angry–happy, counterbalanced across the subjects. Prior to the actual testing, sufficient amount of practice runs were performed in order to prepare each participant for the task. 3. Results Table 2 presents the proportion of hits (correct responses) and false alarms (classification of non-target expressions incorrectly as targets) for happy and angry 1
Development of the MacBrain Face Stimulus Set was overseen by Nim Tottenham and supported by the John D. and Catherine T. MacArthur Foundation Research Network on Early Experience and Brain Development.
272
J.M. Leppänen et al. / Schizophrenia Research 99 (2008) 270–273
Table 2 Percentages of hits, false alarms and corrected hit probabilities (hits minus false alarms) for happy and angry facial expressions in schizophrenia patients, siblings of schizophrenia patients, and healthy comparison subjects Group Patients
Siblings
Controls
Variable
Mean
(SD)
Mean
(SD)
Mean
(SD)
Happy Hits False Alarms Hits-false alarms
.82 .14 .68
(.21) (.16) (.31)
.95 .04 .91
(.07) (.05) (.08)
.90 .06 .84
(.17) (.10) (.26)
Angry Hits False Alarms Hits-false alarms
.73 .15 .58
(.21) (.17) (.29)
.85 .15 .70
(.19) (.20) (.31)
.88 .08 .80
(.18) (.12) (.23)
facial expressions. Assessment of affect recognition accuracy was based on a composite measure (corrected hit probability), calculated as hits minus false alarms. Corrected hit probabilities are insensitive to biases in the use of response categories and, therefore, preferable to raw hit rates as a measure of recognition accuracy (Swets, 1986). To examine whether unaffected siblings differed from comparison subjects on facial affect recognition, the accuracy data were entered into a 2 × 2 × 2 ANOVA with Group (controls vs. siblings) and Gender as between-subject factors and Facial Expression (happy vs. angry) as a within subject factor. The ANOVA yielded a significant Group × Facial Expression interaction on the recognition accuracy scores, F(1, 41) = 6.8, p b .02. This interaction reflected the fact that the hit probabilities for angry (M = .80, SD = .23) and happy (M = .84, SD = .26) did not differ significantly in the comparison group, t(21) = 0.8, whereas a pattern of lower hit rates for angry (M = .70, SD = .31) relative to happy (M = .91, SD = .08) expressions was observed in the sibling group, t(22) = 3.7, p b .002. A similar pattern of lower accuracy scores for angry (M = .58, SD = .29) relative to happy (M = .68, SD = .31) expressions was observed in patients, t(35) = 2.4, p b .03. Comparison of recognition scores across groups revealed that both siblings, F(1, 40) = 4.7, p b .04, and patients, F(1, 54) = 6.2, p b .02, had lower scores for angry expressions than comparison subjects.2 There was no significant differ2 The difference between the sibling and the control group in the recognition of angry expressions became significant only when age was included as a covariate in the analysis, presumably because of the slight differences in mean age between the groups and a negative correlation between age and affect recognition accuracy (Pearson r − .33, p b .03).
ence in the recognition of happy expressions between siblings and comparison subjects, p N .10, or between patients and comparison subjects, p N .05. The overall ANOVA comparing comparison subjects and siblings also revealed a significant main effect of Gender on recognition accuracy scores, F(1, 41) = 6.3, p b .02, reflecting higher accuracy in female (M = .87, SD = .15) compared to male (M = .73, SD = .22) participants. Given the gender difference in the recognition accuracy, a secondary analysis was conducted to confirm that the differential pattern of affect recognition in the sibling group was not driven by the preponderance of female participants in this group. These analyses showed that the lower scores for angry relative to happy expressions was observed in both female, t(14) = 2.3, p b .04, and male, t(7) = 3.1, p b .02, participants in the sibling group whereas, in the control group, no differences were observed for either female or male participants, ps N .30. 4. Discussion The performance of unaffected siblings on an affect recognition task was similar in pattern to that observed in patients with schizophrenia. Siblings and patients both exhibited a pattern of lower recognition accuracy scores for angry compared to happy facial expressions, while healthy comparison subjects recognized angry and happy expressions at an equal level of accuracy. Our results are consistent with the hypothesis that deficits in facial affect recognition are in fact linked with familial vulnerability to schizophrenia and not entirely attributable to secondary factors associated with having a chronic illness (e.g., medication). The fact that there was a deficit in the recognition of negative but not positive facial expressions further suggests that the vulnerability-linked deficits may reflect functional aberrations in relatively specialized neural systems. The processing of negative (threat-related) and positive (safety-related) affective cues is subserved by partially separable neural systems (e.g., Williams et al., 2006). There are also indications that vulnerability to schizophrenia is associated with abnormal activity in those brain systems that are particularly important for the processing of negative affect (i.e., the amygdala, see Gur et al., 2002; Habel et al., 2004; Phillips et al., 1999). However, it is noteworthy that a pattern of deficient recognition of negative facial expressions and intact recognition of positive facial expressions may also arise from general deficits in early-stage visual processing, given a priori differences in discriminability of positive and negative facial expressions (Johnston et al., 2001).
J.M. Leppänen et al. / Schizophrenia Research 99 (2008) 270–273
Further research is required to directly examine the neural basis of the affect recognition deficits in unaffected relatives of schizophrenia patients. It is also important to note that studies with unaffected family members are limited in that the contribution of genetic factors and factors associated with shared rearing environment are confounded, and the sibling and the patient group cannot be considered statistically independent. Regardless of these limitations, the present study provides an important piece of evidence to support the hypothesis that affect recognition deficits are transmitted in families and represent a potential endophenotypic marker of schizophrenia-vulnerability. Role of the funding source N/A
Contributors J.M.L., D.J.H.N, and L.K. designed the study and wrote the protocol. D.J.H.N and L.K. and R.S. collected the data. J.M.L., D.J.H. N. and R.A.E. analyzed data. J.M.L. wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.
Conflict of interest The authors declare that they have no conflicts of interest.
Acknowledgements N/A
References Bediou, B., Franck, N., Saoud, M., Baudouin, J.-Y., Tiberghien, G., Dalery, J., et al., 2005. Effects of emotion and identity on facial affect processing in schizophrenia. Psychiatry Res. 133, 149–157. Brekke, J., Kay, D.D., Lee, K.S., Green, M.F., 2005. Biosocial pathways to functional outcome in schizophrenia. Schizophr. Res. 80, 213–225. Bölte, S., Poustka, F., 2003. The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychol. Med. 33, 907–915. Edwards, J., Pattison, P.E., Jackson, H.J., Wales, R.J., 2001. Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophr. Res. 48, 235–253.
273
Gur, R.E., McGrath, C., Chan, R.M., Schroeder, L., Turner, T., Turetsky, B.I., et al., 2002. An fMRI study of facial emotion processing in patients with schizophrenia. Am. J. Psychiatry 159, 1992–1999. Gur, R.E., Calkins, M.E., Gur, R.C., Horan, W.P., Nuechterlein, K.H., Seidman, L.J., et al., 2007. The consortium on the genetics of schizophrenia: neurocognitive endophenotypes. Schizophr. Bull. 33, 49–68. Habel, U., Klein, M., Shah, N.J., Toni, I., Zilles, K., Falkai, P., et al., 2004. Genetic load on amygdala hypofunction during sadness in nonaffected brothers of schizophrenia patients. Am. J. Psychiatry 161, 1806–1813. Johnston, P.J., Katsikitis, M., Carr, V.J., 2001. A generalised deficit can account for problems in facial emotion recognition in schizophrenia. Biol. Psychol. 58, 203–227. Kee, K.S., Horan, W.P., Mintz, J., Green, M.F., 2004. Do the siblings of schizophrenia patients demonstrate affect perception deficits? Schizophr. Res. 67, 87–94. Leppänen, J.M., Niehaus, D.J., Koen, L., Du Toit, E., Schoeman, R., Emsley, R., 2006. Emotional face processing deficit in schizophrenia: a replication study in a South African Xhosa population. Schizophr. Res. 84, 323–330. Niehaus, D.J.H., Koen, L., Laurent, C., Muller, J., Deleuze, J.-F., Mallet, J., et al., 2005. Positive and negative symptoms in affected sib pairs with schizophrenia: implications for genetic studies in an African Xhosa sample. Schizophr. Res. 79, 239. Phillips, M.L., Williams, L., Senior, C., Bullmore, E.T., Brammer, M.J., Andrew, C., et al., 1999. A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics. Psychiatry Res. Neuroimaging 92, 11–31. Sheehan, D.V., Lecrubier, Y., Harnett-Sheehan, K., Amorim, P., Janavs, J., Weiller, E., et al., 1998. The Mini International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview. J. Clin. Psychiatry 59 (suppl 20), 22–33. Swets, J.A., 1986. Indices of discrimination or diagnostic accuracy: their ROCs and implied models. Psychol. Bull. 99, 100–117. Toomey, R., Seidman, L.J., Lyons, M.J., Faraone, S.V., Tsuang, M.T., 1999. Poor perception of nonverbal social-emotional cues in relatives of schizophrenic patients. Schizophr. Res. 40, 121–130. Williams, L.M., Palmer, D., Liddell, B.J., Song, L., Gordon, E., 2006. The ‘when’ and ‘where’ of perceiving signals of threat versus nonthreat. NeuroImage 31, 458–467. Wolwer, W., Frommann, N., Halfmann, S., Piaszek, A., Streit, M., Gaebel, W., 2005. Remediation of impairments in facial affect recognition in schizophrenia: efficacy and specificity of a new training program. Schizophr. Res. 80, 295–303.
Schizophrenia Research 99 (2008) 270 – 273 www.elsevier.com/locate/schres
Deficits in facial affect recognition in unaffected siblings of Xhosa schizophrenia patients: Evidence for a neurocognitive endophenotype Jukka M. Leppänen a,⁎, Dana J.H. Niehaus b , Liezl Koen b , Elsa Du Toit b , Renata Schoeman b , Robin Emsley b a
Human Information Processing Laboratory, Department of Psychology, FIN-33014 University of Tampere, Tampere, Finland b Ngaphakathi Workgroup, Department of Psychiatry, University of Stellenbosch, South Africa Received 7 August 2007; received in revised form 19 October 2007; accepted 2 November 2007 Available online 4 December 2007
Abstract The present study in an African Xhosa sample examined whether familial vulnerability to schizophrenia is associated with deficits in facial affect recognition. Healthy comparison subjects, unaffected siblings of schizophrenia patients, and schizophrenia patients were tested with a task requiring rapid recognition of matched positive (happy), negative (angry), and neutral facial expressions. Siblings and patients demonstrated impaired recognition of negative relative to positive facial expressions whereas comparison subjects recognized negative and positive expressions at an equal level of accuracy. These results suggest that deficits in the processing negative affect from social cues are transmitted in families and may represent a heritable endophenotype of schizophrenia. © 2007 Elsevier B.V. All rights reserved. Keywords: Schizophrenia; Facial expression; Recognition; Endophenotype
1. Introduction Schizophrenia is associated with deficits in the processing of affective information from facial expressions and other social cues (Bediou et al., 2005; Edwards et al., 2001). These deficits may contribute to poor social functioning in schizophrenia patients (Brekke et al., 2005), and have been identified as an important target for clinical intervention (Wolwer et al., 2005).
⁎ Corresponding author. Tel.: +358 3 3551 6537; fax: +358 3 3551 7710. E-mail address: [email protected] (J.M. Leppänen). 0920-9964/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2007.11.003
There has been increasing interest in the possibility that instead of secondary factors associated with chronic illness, deficits in the recognition of affective cues may in fact reflect a heritable endophenotype that is related to a genetic vulnerability to schizophrenia (Gur et al., 2007). A critical feature of such endophenotypic deficits is that they are found not only in affected individuals, but also in unaffected relatives of schizophrenia patients. A few studies have examined facial affect recognition in relatives of schizophrenia patients but, to date, the evidence for clear vulnerability-linked deficits is scarce (Bölte and Poustka, 2003; Kee et al., 2004; Toomey et al., 1999). One possible explanation for the lack of clear findings is that rather than a broad
J.M. Leppänen et al. / Schizophrenia Research 99 (2008) 270–273
impairment in facial affect recognition, schizophrenia vulnerability may be associated with a more selective deficit with greater impairments for negative than positive facial expressions (Bediou et al., 2005; Edwards et al., 2001). To examine the possibility that such deficits are more likely to be revealed through measures that allow for separate assessment of the recognition of positive and negative facial expressions than measures that rely on average indices of affect recognition performance, and to extend the investigation of vulnerability-linked neurocognitive deficits to nonCaucasian populations, we investigated emotion recognition in unaffected siblings of schizophrenia patients in an African Xhosa sample. We specifically tested the hypothesis that unaffected siblings exhibit a pattern of impaired recognition of angry relative to happy facial expressions, and that this finding would be similar to that found in patients affected by schizophrenia (Leppänen et al., 2006). 2. Methods and materials 71 participants were included: 22 healthy comparison subjects, 23 siblings of schizophrenia patients, and 36 patients with schizophrenia. Schizophrenia patients were recruited from clinics in the wider Cape Town area, South Africa, as part of a large genetic study. To be included, participants had to be at least 18 years of age, of Xhosa origin (4/4 grandparents reported as Xhosa), reside in the Cape Town metropolitan area, and fulfill a diagnosis of schizophrenia according to DSM-IV-TR criteria (for details of clinical assessment, see Niehaus et al., 2005). Participants in the unaffected sibling group shared both biological parents with a patient diagnosed with schizophrenia. Healthy controls were recruited via word-of-mouth from the same geographical area as the patients and siblings. Exclusion criteria for siblings and controls included a history of psychiatric disorders or treatment (Sheehan et al., 1998), mental retardation, visual or auditory impairment, or significant medical illness (n = 7 excluded). One additional participant from the control group was excluded due to family history of psychiatric illnesses (n = 1). Demographic information for patients, siblings, and comparison subjects are presented in Table 1. The three groups differed significantly in gender distribution, but differences in age and level of education were not statistically significant. Written informed consent was obtained from all participants according to guidelines of the institutional review board of the University of Stellenbosch. Participants completed two computerized tasks assessing facial affect recognition and visual attention.
271
Table 1 Demographic information for schizophrenic patients, unaffected siblings and healthy comparison subjects (standard deviations are shown in parentheses) Variable
Patients
Siblings
Controls
Statistical test
Sex
10F/26M
15F/8M
11F/11M
Age
41.8 (10.4)
36.0 (13.0)
40.9 (10.3)
Education
5.5 (3.1)
6.2 (2.9)
6.0 (3.1)
χ2 = 8.4, df = 2, p b .02 F(2, 78) = 2.0, p = .14 F(2, 75) = 0.4, p = .65
The data from the visual attention task are not reported here. The affect recognition task was intended to measure rapid perceptual discrimination of matched positive (happy), negative (angry), and neutral facial expressions and has been described in detail elsewhere (Leppänen et al., 2006). A task with short stimuluspresentation duration (200 ms) was used to better approximate the automatic nature of facial affect perception and the brief duration of facial expressions in everyday life. Participants were presented with low (closed-mouth) and high-intensity (open-mouth) happy and angry expressions, and closed- and open-mouth neutral expressions selected from the MacBrain Face Stimulus Set1. The facial images were presented in random order in the center of the computer with a 200ms stimulus presentation time and a 2800-ms interstimulus interval (using E-prime software, Psychology Software Tools, Inc.). A total of 64 happy, 64 angry, and 64 neutral facial expressions were presented (4 repetitions of each individual facial expression picture). The subjects were asked to respond by pressing one of the choice buttons (on a computer mouse) when a happy or angry face was presented, and not to respond when a neutral face was presented. The buttons were labeled from left to right in two different orders; happy–angry and angry–happy, counterbalanced across the subjects. Prior to the actual testing, sufficient amount of practice runs were performed in order to prepare each participant for the task. 3. Results Table 2 presents the proportion of hits (correct responses) and false alarms (classification of non-target expressions incorrectly as targets) for happy and angry 1
Development of the MacBrain Face Stimulus Set was overseen by Nim Tottenham and supported by the John D. and Catherine T. MacArthur Foundation Research Network on Early Experience and Brain Development.
272
J.M. Leppänen et al. / Schizophrenia Research 99 (2008) 270–273
Table 2 Percentages of hits, false alarms and corrected hit probabilities (hits minus false alarms) for happy and angry facial expressions in schizophrenia patients, siblings of schizophrenia patients, and healthy comparison subjects Group Patients
Siblings
Controls
Variable
Mean
(SD)
Mean
(SD)
Mean
(SD)
Happy Hits False Alarms Hits-false alarms
.82 .14 .68
(.21) (.16) (.31)
.95 .04 .91
(.07) (.05) (.08)
.90 .06 .84
(.17) (.10) (.26)
Angry Hits False Alarms Hits-false alarms
.73 .15 .58
(.21) (.17) (.29)
.85 .15 .70
(.19) (.20) (.31)
.88 .08 .80
(.18) (.12) (.23)
facial expressions. Assessment of affect recognition accuracy was based on a composite measure (corrected hit probability), calculated as hits minus false alarms. Corrected hit probabilities are insensitive to biases in the use of response categories and, therefore, preferable to raw hit rates as a measure of recognition accuracy (Swets, 1986). To examine whether unaffected siblings differed from comparison subjects on facial affect recognition, the accuracy data were entered into a 2 × 2 × 2 ANOVA with Group (controls vs. siblings) and Gender as between-subject factors and Facial Expression (happy vs. angry) as a within subject factor. The ANOVA yielded a significant Group × Facial Expression interaction on the recognition accuracy scores, F(1, 41) = 6.8, p b .02. This interaction reflected the fact that the hit probabilities for angry (M = .80, SD = .23) and happy (M = .84, SD = .26) did not differ significantly in the comparison group, t(21) = 0.8, whereas a pattern of lower hit rates for angry (M = .70, SD = .31) relative to happy (M = .91, SD = .08) expressions was observed in the sibling group, t(22) = 3.7, p b .002. A similar pattern of lower accuracy scores for angry (M = .58, SD = .29) relative to happy (M = .68, SD = .31) expressions was observed in patients, t(35) = 2.4, p b .03. Comparison of recognition scores across groups revealed that both siblings, F(1, 40) = 4.7, p b .04, and patients, F(1, 54) = 6.2, p b .02, had lower scores for angry expressions than comparison subjects.2 There was no significant differ2 The difference between the sibling and the control group in the recognition of angry expressions became significant only when age was included as a covariate in the analysis, presumably because of the slight differences in mean age between the groups and a negative correlation between age and affect recognition accuracy (Pearson r − .33, p b .03).
ence in the recognition of happy expressions between siblings and comparison subjects, p N .10, or between patients and comparison subjects, p N .05. The overall ANOVA comparing comparison subjects and siblings also revealed a significant main effect of Gender on recognition accuracy scores, F(1, 41) = 6.3, p b .02, reflecting higher accuracy in female (M = .87, SD = .15) compared to male (M = .73, SD = .22) participants. Given the gender difference in the recognition accuracy, a secondary analysis was conducted to confirm that the differential pattern of affect recognition in the sibling group was not driven by the preponderance of female participants in this group. These analyses showed that the lower scores for angry relative to happy expressions was observed in both female, t(14) = 2.3, p b .04, and male, t(7) = 3.1, p b .02, participants in the sibling group whereas, in the control group, no differences were observed for either female or male participants, ps N .30. 4. Discussion The performance of unaffected siblings on an affect recognition task was similar in pattern to that observed in patients with schizophrenia. Siblings and patients both exhibited a pattern of lower recognition accuracy scores for angry compared to happy facial expressions, while healthy comparison subjects recognized angry and happy expressions at an equal level of accuracy. Our results are consistent with the hypothesis that deficits in facial affect recognition are in fact linked with familial vulnerability to schizophrenia and not entirely attributable to secondary factors associated with having a chronic illness (e.g., medication). The fact that there was a deficit in the recognition of negative but not positive facial expressions further suggests that the vulnerability-linked deficits may reflect functional aberrations in relatively specialized neural systems. The processing of negative (threat-related) and positive (safety-related) affective cues is subserved by partially separable neural systems (e.g., Williams et al., 2006). There are also indications that vulnerability to schizophrenia is associated with abnormal activity in those brain systems that are particularly important for the processing of negative affect (i.e., the amygdala, see Gur et al., 2002; Habel et al., 2004; Phillips et al., 1999). However, it is noteworthy that a pattern of deficient recognition of negative facial expressions and intact recognition of positive facial expressions may also arise from general deficits in early-stage visual processing, given a priori differences in discriminability of positive and negative facial expressions (Johnston et al., 2001).
J.M. Leppänen et al. / Schizophrenia Research 99 (2008) 270–273
Further research is required to directly examine the neural basis of the affect recognition deficits in unaffected relatives of schizophrenia patients. It is also important to note that studies with unaffected family members are limited in that the contribution of genetic factors and factors associated with shared rearing environment are confounded, and the sibling and the patient group cannot be considered statistically independent. Regardless of these limitations, the present study provides an important piece of evidence to support the hypothesis that affect recognition deficits are transmitted in families and represent a potential endophenotypic marker of schizophrenia-vulnerability. Role of the funding source N/A
Contributors J.M.L., D.J.H.N, and L.K. designed the study and wrote the protocol. D.J.H.N and L.K. and R.S. collected the data. J.M.L., D.J.H. N. and R.A.E. analyzed data. J.M.L. wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.
Conflict of interest The authors declare that they have no conflicts of interest.
Acknowledgements N/A
References Bediou, B., Franck, N., Saoud, M., Baudouin, J.-Y., Tiberghien, G., Dalery, J., et al., 2005. Effects of emotion and identity on facial affect processing in schizophrenia. Psychiatry Res. 133, 149–157. Brekke, J., Kay, D.D., Lee, K.S., Green, M.F., 2005. Biosocial pathways to functional outcome in schizophrenia. Schizophr. Res. 80, 213–225. Bölte, S., Poustka, F., 2003. The recognition of facial affect in autistic and schizophrenic subjects and their first-degree relatives. Psychol. Med. 33, 907–915. Edwards, J., Pattison, P.E., Jackson, H.J., Wales, R.J., 2001. Facial affect and affective prosody recognition in first-episode schizophrenia. Schizophr. Res. 48, 235–253.
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