In this study we used a face emotion labeling task to compare children with NP-BD (i.e., episodic mania with elevated and/or grandiose mood), to those with SMD (i.e., chronic irritability, marked reactivity, and hyperarousal, but no episodic mania; Leibenluft et al., 2003
), and controls. We sought to determine if children with NP-BD and SMD differ in their ability to label emotional facial expressions, if face-processing deficits in these patients were specific to particular emotions, and if impaired face labeling was associated with psychosocial dysfunction.
Regarding our first research aim, we found that, compared to controls, both NP-BD and SMD youth displayed face-processing deficits, but the patient samples did not differ from each other. Specifically, both NP-BD and SMD subjects required significantly greater intensity of emotional expression than did controls before the first response and before correctly identifying the facial expression. The finding that our patient samples require more intense displays of face emotion is important because subtle displays of emotion are common in social interactions, and facial expressions change rapidly during social interactions (Addington & Addington, 1998
; De Sonneville et al., 2002
). These results extend previous work with NP-BD children (McClure et al., 2005
; Rich et al., 2006
) by documenting that face-processing deficits are also present in SMD youth. These results are also consistent with another study that used a task of face emotion labeling and found that NP-BD and SMD youth were equally deficient in labeling face emotions compared to controls and youth with ADHD and anxiety/depression, who themselves were not impaired (Guyer et al., 2007
). Although methodological differences between that study and our current study may limit the complete integration of these results, it is notable that two different paradigms found NP-BD and SMD youth to be equally impaired when processing faces.
Because the rate of ADHD in both patient samples is high, one might have predicted that NP-BD and SMD youth would have responded more quickly (i.e., impulsively) than controls to the faces. We found just the opposite, in that the time to first response was longer in both patient samples than in controls. This result, coupled with the similar accuracy rates among our three samples, suggests that NP-BD and SMD youth were in fact attending to the faces. In addition, it is possible that the group differences in response point reflect slowed motor responsivity in patients, rather than a face-labeling deficit per se. Although we cannot rule this out, the fact that the subjects’ later responding was not found across all emotion types (i.e., subjects were deficient on happy, surprised, fearful, and disgusted faces, but not sad faces) does not seem to indicate an overall slowness to respond. In sum, we believe that our results support the conclusions that, (a) compared to controls, NP-BD and SMD youth require significantly greater intensity of emotional expression before they can identify a facial emotion, and (b) our findings do not simply reflect inattention or motor slowness in patients.
Our data here should be interpreted in light of other research comparing SMD and NP-BD youth. Previous studies, coupled with the data presented here, demonstrate shared and
divergent affective, behavioral, cognitive, and psychophysiological impairments in NP-BD versus SMD youth. Indeed, the question of the nosological relationship between SMD and NP-BD may have a dimensional, rather than categorical, answer, because BD is a multigenic illness with many affective and behavioral diagnostic symptoms (Althoff, Faraone, Rettew, Morley, & Hudziak, 2005
; Kowatch, Youngstrom, Danielyan, & Findling, 2005
). Overall, research to date largely supports the notion that SMD is distinct from NP-BD: children with SMD have an elevated risk for MDD at age 18 (Brotman et al., 2006
); youth with NP-BD are more likely than those with SMD to have a family history of BD (Brotman et al., 2007
); and SMD and NP-BD youth differ in response flexibility deficits and in the brain mechanisms mediating response to frustration (Dickstein et al., 2007
; Rich et al., 2007
). Nonetheless, the fact that both SMD and NP-BD exhibit face-labeling deficits, and that those deficits are not present in other psychopathological groups (Guyer et al., 2007
), indicates that SMD and NP-BD may ultimately be found to be on the same pathophysiological continuum.
Our results may also suggest avenues for beginning to distinguish the neural substrates of SMD and NP-BD. Pathophysiological differences may be apparent even when behavioral differences are absent, because the same behavioral deficit may be mediated by different brain mechanisms (Wilkinson & Halligan, 2004
). Thus, despite the comparable performance between SMD and NP-BD youth in this study, face-processing tasks may identify different neural correlates of these two disorders. There is substantial overlap between the neural regions implicated in the pathophysiology of pediatric BD and those involved in processing face emotions. For example, in BD youth, volumetric and functional aberrations have been documented in the amygdala (Blumberg et al., 2005
; Blumberg, Kaufman et al., 2003
; Chang et al., 2005
; Chen et al., 2004
; Delbello, Zimmerman, Mills, Getz, & Strakowski, 2004
; Dickstein et al., 2005
; Rich et al., 2006
), orbitofrontal cortex (Rich et al., 2006
; Wilke, Kowatch, Delbello, Mills, & Holland, 2004
), cingulate (Chang et al., 2004
; Kaur et al., 2005
; Wilke et al., 2004
), insula (Chang et al., 2004
), putamen (Blumberg, Martin, et al., 2003
; Chang et al., 2004
; Delbello et al., 2004
), and basal ganglia (Wilke et al., 2004
; Leibenluft et al., 2007
). These same neural regions have been shown to assist in the processing of emotional facial expressions (Adolphs et al., 1999
; Blair, Morris, Frith, Perrett, & Dolan, 1999
; Gorno-Tempini et al., 2001
; Killgore & Yurgelun-Todd, 2004
; Morris et al., 1996
; Phillips et al., 1997
; Sprengelmeyer, Rausch, Eysel, & Przuntek, 1998
; Yang et al., 2002
; Whalen et al., 1998
). Functional magnetic resonance imaging studies utilizing face-processing tasks may identify the neural correlates of NP-BD and SMD and clarify the extent to which the pathophysiology of these two disorders overlaps or differs.
A second goal of this study was to determine if face-labeling deficits were specific to certain emotional expressions. We predicted that, given their history of mania, NP-BD youth might show particular sensitivity to happy faces. We also predicted that, because SMD youth display severe behavioral dysregulation and irritability similar to that seen in psychopathic youths, SMD youth would display aberrant identification of fearful and sad faces similar to psychopathic youths (Blair et al., 1997
; Stevens et al., 2001
). In general, these predictions were not supported. Of the six emotional expressions used in this task, both samples of patients were significantly impaired on four (happy, surprised, fearful, and disgusted), and there was a strong trend for impairment on a fifth (anger). Only sad faces failed to elicit NP-BD or SMD deficits. Our results indicate that the difficulty identifying facial emotions in NP-BD and SMD youth is evident across multiple emotions, and is best characterized as a general face emotion identification impairment, as opposed to being specific to certain emotions.
As previously noted, another study from our group found no face emotion identification deficits in youth with ADHD or comorbid depression and anxiety (Guyer et al., 2007
). However, the literature has not been entirely consistent on this point. That is, some studies find that ADHD youth display a generalized face-labeling deficit across emotions when face stimuli are paired with voice recordings (Cadesky, Mota, & Schachar, 2000
; Corbett & Glidden, 2000
). Similarly, other studies suggest that some childhood psychopathologies may be associated with deficits recognizing specific emotions; for example, threatening faces (i.e., fearful and angry) in depressed children (Lenti, Giacobbe, & Pegna, 2000
), angry faces with maltreated (Pollak & Kistler, 2002
; Pollak, Cicchetti, Hornung, & Reed, 2000
) and physically abused children (Pollak & Tolley-Schell, 2003
), and distressed faces (i.e., fearful and sad) in children with psychopathy (Blair et al., 1997
; Stevens et al., 2001
). Clearly, direct comparisons of different childhood psychopathologies (e.g., youth with anxiety, depression, ADHD, ODD, BD, and SMD), using an identical face-processing task, are needed to clarify the specificity of face-processing deficits between diagnoses.
Elucidating face-processing impairments in BD may also be achieved using developmental studies that compare children and adults on identical tasks. Comparable to the face emotion labeling difficulties we identified in NP-BD youth, prior work finds that adults with BD have face emotion labeling deficits that do not appear to be emotion specific (Bozikas et al., 2006
; Getz et al., 2003
; Lembke et al., 2002
; Yurgelun-Todd et al., 2000
). For example, whereas two studies suggest that adults with BD may show enhanced recognition of disgust (Harmer et al., 2002
) and sad faces (Lennox, Jacob, Calder, Lupson, & Bullmore, 2004
), other studies find BD adults to be deficient in their identification of these specific face emotions (Bozikas et al., 2006
; Getz et al., 2003
; Lembke et al., 2002
). Further, when identifying happy faces, studies have found BD adults both to be deficient (Bozikas et al., 2006
; Getz et al., 2003
) and comparable to controls (Yurgelun-Todd et al., 2000
The inconsistency of the data in BD adults, coupled with minimal data on BD youth, makes it difficult to draw conclusions regarding the developmental progression of face-processing deficits in individuals with BD. In contrast, there may be differences in face processing between youth and adults with BD. These may reflect a variety of developmental factors, including adults’ more extended exposure to social interactions (which may improve face-processing skills), longer use of psychotropic medications (which may lessen the neurochemical or neurophysiological dysfunction associated with impaired face processing), or developmental changes in brain function. At the same time, in this study we did not find an age effect on our results, and a prior study with BD adults found that impaired face affect identification was not related to age of onset or duration of illness (Bozikas et al., 2006
). The lack of age effects may reflect the fact that by 6 years of age, the recognition of basic emotions such as happy, angry, scared, and sad, appears to be fully developed (Markham & Adams, 1992
; McClure, 2000
), and there is not substantial improvement in face emotion identification accuracy after age 10 (Harrigan, 1984
). A longitudinal study of children at risk for BD, or a comparison of subjects with early-onset BD to those with adult-onset BD, would begin to elucidate the developmental progression of deficient face emotion processing in individuals with BD.
An additional line of future research may explore the role of gender in BD youth when processing faces. Consistent with a prior review in healthy youth (McClure, 2000
), we found that, in NP-BD youth and controls, males may require more intense displays of facial expression for accurate emotion identification than do females. Gender-related differences were not identified in SMD youth. Studies with large samples are necessary to explore further the role of gender in NP-BD face-labeling deficits.
Our third goal in this study was to examine associations between social impairment and face-labeling deficits. Two aspects of social function were measured: social reciprocity and a general measure of social interactions with peers and family. In the NP-BD sample, we found a negative correlation between delayed face emotion identification and parentreported social reciprocity (e.g., social awareness, social information processing, and capacity for reciprocal social responses). These results expand upon a prior study of parent-reported poor social skills in BD youth (Goldstein et al., 2006
In contrast, in the SMD sample we found an association between delayed face emotion identification, in particular of fearful and happy faces, and impaired family function. The relationship between impaired face processing and family dysfunction may be bidirectional. Consistent with prior work (Cicchetti & Curtis, 2005
; Pollak & Kistler, 2002
; Pollak, Klorman, Thatcher, & Cicchetti, 2001
; Marshall & Fox, 2004
; Parker & Nelson, 2005
), adverse environmental conditions, such as family dysfunction, may result in the impaired face emotion processing seen in SMD youth. Indeed, recent work suggests that aberrant social environments may impact adversely the development of neuropeptide systems central to social and emotional development (Fries, Ziegler, Kurian, Jacoris, & Pollak, 2005
). Conversely, impaired identification of facial emotions may lead to problematic family interactions in SMD children. Our results suggest that psychotherapeutic interventions might target NP-BD and SMD children’s face-labeling deficits, perhaps in the form of psychoeducation and practicing face emotion identification, in an effort to improve social function.
One potential limitation of our study is the varied mood states of our NP-BD subjects. However, consistent with previous data (McClure et al., 2005
; Rich et al., 2006
), we found that euthymic NP-BD patients were impaired in face emotion recognition when compared to controls. Another limitation is the high rates of co-occurring diagnoses, particularly ADHD and ODD, in our NP-BD sample, although this rate is typical of that seen in other samples of BD children (Biederman, Faraone, Chu, & Wozniak, 1999
). When we compared NP-BD subjects with and without comorbid ADHD or ODD, we did not find between-group differences in response point. However, small sample sizes limit the interpretation of these negative results. Comparable examinations in the SMD sample were not possible due to the high rates of ADHD and ODD in this group; indeed, SMD, ODD, and ADHD can be viewed as different approaches to describing closely related clinical phenomena. Future studies should compare BD children with and without comorbid conditions (e.g., ADHD, ODD, anxiety) to children with ADHD, ODD, and anxiety.
In conclusion, the current study extends prior work on face-processing deficits in bipolar youth by documenting face-labeling deficits in SMD children, that is, those in whom the BD diagnosis is controversial. Our results indicate that NP-BD and SMD youth require significantly greater intensity of facial expression before correctly identifying an emotion, in particular disgust, surprise, fear, and happiness. Finally, we provide evidence of an association between impaired face labeling and impaired social reciprocity in NP-BD youth and impaired family function in SMD youth.