Social gaze is a basic building block of socioemotional functioning. Mutual gaze, which occurs when two people’s eyes meet, is a powerful social signal, influencing how we are perceived by others and conveying a great deal of social information (Argyle and Dean, 1965
; Kleinke, 1986
). Holding another’s gaze either for too long or not long enough during an interpersonal interaction may violate social norms and is associated with social deficits (Mirenda et al., 1983
; Kleinke, 1986
). Although neurodegenerative diseases such as FTD and SD are known to impact social and emotional behavior, relatively little is known about whether abnormalities occur in patients’ gaze behavior in social contexts.
The present study was the first to our knowledge to measure dementia patients’ mutual gaze during actual social interactions. This approach revealed subtle yet clear-cut differences in mutual gaze behavior among couples with an AD, SD or FTD patient and between these couples and normal controls. Importantly, because the individual gaze behaviors of non-affected partners did not differ, we can attribute our results to differences in gaze of the dementia patients.
Mutual gaze in dementia
In AD, social behavior is relatively preserved in the early stages of the disease (Seeley et al., 2007
). Consistent with this, we found no differences between the AD patients’ and controls’ gaze behavior whether examined at the couple or the individual level. Moreover, AD couples exhibited levels of mutual gaze that were comparable to those found in past studies of healthy couples (Mirenda et al., 1983
). These findings suggest that in the early stages of AD, despite cognitive decline, social gaze remains intact. For AD patients, normal gaze behavior may help sustain relationships that offer them both functional and emotional support.
In FTD and SD, social and emotional behavior is impoverished, with deficits appearing quite early in the disease (Seeley et al., 2005
). Caregiver reports suggest that FTD patients tend to be affectively aloof, flat and avoidant of social interactions. While some SD patients become cold-hearted (Rankin et al., 2003
), others show emotional warmth, display emotional expressions, and seek out social interactions (Snowden et al., 2001
; Mendez et al., 2006
). Consistent with these clinical descriptions, we found different patterns of mutual gaze in FTD and SD. Compared to SD couples, FTD couples exhibited low levels of mutual gaze, which may reflect a waning interest in other people. When examined at the individual level, a similar pattern of results was found: compared to SD (and also AD) patients, FTD patients gazed at their partners’ eyes significantly less. With SD couples, there was some indication of greater mutual gaze than control couples, but this difference was not found at the individual level, and, thus, we consider it less robust than the differences between FTD and SD.
We speculate that different patterns of neural loss in AD, FTD and SD account for the different levels of mutual gaze that we found among these groups. In the early stages of AD, preservation of frontal and temporal brain regions involved in social gaze likely promotes normal gaze behavior. In FTD and SD, social gaze abnormalities may arise as degeneration progresses throughout the frontal and temporal lobes, regions that play important roles in the initiation and regulation of gaze behavior. In FTD, loss in frontal regions that are important for the control of saccadic eye movements (Schall and Boucher, 2007
) and attention (Tekin and Cummings, 2002
) may render it difficult for patients to pursue and sustain attention on their partners’ eyes (Boxer et al., 2006
). In SD, loss in the temporal lobes and amygdala may interfere with detection of gaze and its social significance (Hooker et al., 2003
; Pelphrey et al., 2004
), thus making it difficult for patients to pick up on nuanced social cues. As SD patients gradually lose their ability to understand concepts and follow complex conversations, they may be more motivated to pay close visual attention to those around them. This may result in gaze that is sustained longer than usual. Although our findings differ from a previously published case report in which diminished eye contact was reported in one SD patient (Edwards-Lee et al., 1997
), it is possible that this patient was in a later stage of disease with more diffuse brain atrophy and more behavioral dysfunction than the SD patients in the present study.
Gaze is a vital part of social interactions. Not only did we find differences among the AD, FTD, and SD patients in their levels of mutual gaze, but across groups we found significant negative correlations between mutual gaze and real-world behavioral impairment. In particular, lower levels of mutual gaze were associated with disinhibition and apathy, socioemotional symptoms that are particularly stressful for caregivers (de Vugt et al., 2006
). In contrast, we found no relationship between gaze and cognitive functioning.
As expected, AD patients displayed levels of physiological reactivity during the conversations that were similar to those of controls. We had predicted that both SD and FTD patients would have diminished reactivity compared to controls. This prediction was supported for SD patients who exhibited significantly lower heart rate and general somatic activity than controls. However, FTD patients evidenced no significant differences in physiological reactivity compared to controls.
The finding that SD patients were less reactive in some physiological domains than controls (despite comparable or even greater levels of mutual gaze) suggests that SD patients may have been less affected by the emotional nature of the conversations. SD patients may be less aware of and less sensitive to negative affect in others because of comprehension difficulties and degeneration of brain structures such as the amygdala, which are important for social behaviors and threat-perception (Aggleton and Passingham, 1981
; Amaral, 2003
). Thus, for SD patients the social world may be less threatening and less likely to produce negative emotional responses and attendant autonomic activation.2
The finding that FTD patients had similar levels of physiological reactivity compared to controls (despite reduced gaze) may underscore the non-specific nature of autonomic activation. We expect that the FTD patients were engaged in non-task-contingent, non-emotional behaviors (e.g. fidgeting, looking around the room) that produced levels of physiological reactivity that were comparable to those of controls.
The study has several limitations. First, gaze behavior was measured by having trained coders rate video recordings. Eye-tracking instrumentation would have allowed for more precise spatial and temporal quantification of gaze (Duchowski, 2003
Second, to rule out the possibility that differences in the emotional quality of the conversations among our groups were responsible for group differences in mutual gaze and physiological reactivity, we analyzed the emotional language used by couples. Although we found no differences in emotional language, it is possible that group differences might have been detected using other measures of emotion (e.g. coding emotional behavior).
Third, we examined physiological reactivity by examining physiological levels averaged across the entire conversations. A more nuanced statistical approach (e.g. time series analyses) would have been sensitive to group differences in the temporal dynamics of physiological reactivity and in specific segments of the conversations (e.g. beginning, end, or during moments of high emotional intensity). We hope to pursue these kinds of issues in future studies when we have larger samples of couples.