Discussion
The aim of the present study was to investigate two important aspects of eye-gaze processing in euthymic bipolar patients. Specifically, the ability to infer the mental state and intention of others from the eyes (reading the mind in the eyes) and the tendency to follow the direction of another individual’s gaze (social attention) were assessed. Results showed that, compared to controls, euthymic BD patients performed significantly worse on the reading the mind in the eyes test. On the other hand, no significant differences in social attention were found on the eye-gaze cueing tasks.
Problems of euthymic BD patient in inferring the mental state of others from the eyes are of clinical concern as they are likely to play a significant role in the social difficulties that this group is known to be at risk for [3]. Indeed, the ability to understand nonverbal information about emotion and intention are believed to be factors necessary for an adequate social functioning [47]. However, literature about theory of mind in euthymic patients as measured by the reading the mind in the eyes test did not yield a consistent pattern of results. While one study suggests that euthymic BD patients have lower performance than controls [6], other shows no differences between patients and controls [24]. Therefore our results are consistent with the former study but in contrast with the latter. These discordant results may depend on sample characteristics; as compared to our study and that of Bora and colleagues [6], in the Martino and colleagues study [24] patients had more years of education (11.77, 11.44, and 13.8 years, respectively) and they were characterized by shorter duration of illness (15.31, 15, and 11.4 years, respectively).
Regarding social attention orienting, we did not find differences between the groups. This result could be possibly explained by a sufficient level of remission of social attention in euthymic bipolar patients. However, since no previous study has investigated social attention in bipolar disorder during mania and/or depression, these findings could be alternatively attributed to the intact ability in BD to follow the direction of another individual’s gaze. Further research is necessary to shed light on this issue.
Our finding that euthymic BD patients had an impairment in the ability to infer the mental state of others from the eyes, but a preserved tendency to follow the direction of another’s gaze is consistent with the current theory regarding fast and slow systems of social cognition [48-50]. The fast system involves the superior colliculus, pulvinar nucleus, and amygdala, which are sensitive to observed gaze directions, emotion-related signals, social salient information, and sexually dominated processes. The slow system, on the other hand, involves several cortical networks that include the superior temporal sulcus, frontal eye field, lateral intraparietal area, or other areas in the frontal–parietal attention network. This slow system mainly processes eye postures, face identity, intentionality, and other complex social information. We suspect that the attentional orienting in response to gaze cue may be involved in both fast and slow systems, whereas the ability to judging mental state from the eyes may be involved only in the slow system. Thus, the results of the present study might suggest that euthymic BD patients are impaired in slow but not in fast systems of social cognition. Consistent with this view are the evidence showing during remission of BD a normalization of amygdala response [51, 52] but an abnormal activity of brain areas normally implicated in the slow system of social cognition such as the superior temporal sulcus [53] and the ventrolateral prefrontal cortex [17-20] .
As in their original version, in the present study, we used pictures of eye regions of the face and schematic face for the reading the mind in the eyes test and eye-gaze cueing task, respectively. Therefore the different results showed in the two test may be, at least in part, due to the social meaningfulness of stimuli used. Maybe euthymic bipolar patients are only impaired in processing photorealistic eye-gaze but not schematic faces. There are evidence suggesting that that schematic face and images of real faces are processed similarly evoking similar cueing effects [54] and theory of mind / “socialness” [55, 56]. However, the impact of the different stimulus parameters has never directly compared in euthymic bipolar disorder. Further research will be necessary to shed light on this issue.