The current study investigated how early postnatal deprivation to race affects behavioral and amygdala sensitivity to race. Using a unique international adoption design, we could, in a controlled manner, measure how experience with face types influences behavioral and neural processing of emotions of in- and out-group faces. Our findings show that early experience with racial categories tunes face emotion processing toward the more familiar face category, also known as the ORE. We found that complete deprivation to out-group faces early in development was followed by lower recognition accuracy and higher amygdala activation to out-group faces relative to in-group faces. This bias toward in-group faces is associated with the amount of early race deprivation; earlier age of adoption was associated with an attenuated ORE, including higher relative accuracy at identifying expressions of out-group faces as well as reduced amygdala sensitivity. Importantly, differential amygdala response to race was associated with differential behavioral performance to identifying the emotions of in- and out-group faces, suggesting that neural biases to race may manifest behaviorally, highlighting the impactful role that differential amygdala sensitivity plays.
The amygdala is an early developing brain region (Payne et al., 2010
) that is sensitive to emotionally and motivationally salient stimuli in one's environment (Whalen et al., 2001
; Cunningham and Brosch, 2012
), as well as the detection of novel and unusual stimuli (Blackford et al., 2010
). Therefore, the heightened amygdala response observed in the current study may suggest that out-group faces are both relatively novel and particularly salient. These findings are consistent with adult work showing stronger amygdala signal to other-race faces relative to own-race faces (Hart et al., 2000
; Krill and Platek, 2009
), suggesting that other-race faces are particularly salient, perhaps as a result of novelty or unfamiliarity with the out-group. Saliency itself has been shown to increase amygdala responding; saliency may be high during the initial learning phase of in-group membership as has been shown with minimal-group paradigms in adulthood (Van Bavel et al., 2008
). With increased experience, saliency for in-group versus out-group members may switch as the out-group members remain less familiar and the in-group members become more familiar. This perspective is consistent with the perceptual narrowing hypothesis and suggests that early experiences are particularly important for shaping the tuning properties of the system. Thus, the amygdala becomes culturally biased toward or away from racial categories as a function of early exposure to own-race relative to other-race faces. Early deprivation to out-group race renders out-group faces more novel and salient, resulting in poorer emotion recognition and enhanced amygdala responsivity.
Our findings are consistent with previous work showing that infants show differential processing of in- and out-group faces. For instance, Vogel et al. (2012)
found that, by 9 months, infants do not differentiate among faces of the other race, show a decline in the ability to match emotions in other-race faces, and demonstrate differential neural processing to in-group relative to out-group faces. Similar results have been found in monkeys deprived of faces, such that, during the first year of life, monkeys exposed to one species of faces (e.g., human or monkey) at the cost of the other species show a marked decline in the ability to recognize the non-exposed faces (Sugita, 2008
). Together, our findings suggest that the ability to perceive and recognize facial expressions at a level that allows for generalization across racial types develops during the first year of life, and deprivation to other-races (or species) results in a marked decline in the processing of out-group faces.
Early postnatal development may be a sensitive period whereby lack of early exposure to out-group faces limits the encoding of these faces later in development (Sangrigoli et al., 2005
). Indeed, early postnatal development is an important temporal window during which experience warps the face representational system; once in place, the system limits the encoding of new faces and is less sensitive to new inputs (Furl et al., 2002
). Thus, face perception may reflect an experience-expectant process, such that exposure to faces during early postnatal development leads to perceptual (i.e., recognition bias) and neural (i.e., amygdala desensitization) specialization at the cost of non-experienced stimuli (Nelson, 2001
). Our findings provide strong evidence for the perceptual narrowing hypothesis of race perception, such that selective experience with own-race versus other-race faces early in life tunes the system toward the predominant category, leading to a decline in the ability to recognize emotional expressions in other-race faces (Sangrigoli et al., 2005
; Kelly et al., 2007
; Sugita, 2008
; Dahl et al., 2012).
Importantly, youths who had greater early deprivation (i.e., later age of adoption) showed the strongest differential bias to own- and other-race faces, suggesting that the amount of deprivation and the timing at which children are exposed to new faces can affect the tuning of the face perceptual system. Such differential tuning of the face perceptual system leads to greater emotional arousal to other-race faces. Although youths in this study were exposed to other races by childhood, it is possible that the encoding of new faces is already limited by childhood, resulting in a deficit in recognizing emotional expressions in out-group faces. Indeed, European adults who receive extensive interracial contact with Asian individuals (e.g., European individuals living in Singapore) do not show an improved ability to recognize the faces from the other race (Ng and Lindsay, 1994
). Together with our findings, this suggests that the age at which experience with other race faces begins is a crucial factor in face perception and emotional recognition of other-race faces (Sangrigoli and De Schonen, 2004
Of note, our sample of adopted youths is individuals who spent time in institutionalized care as infants. Although this type of rearing provides a racially homogenous environment for youths, institutionalized care is a non-normative developmental experience associated with impairments in emotional processing and heightened amygdala reactivity (Tottenham and Sheridan, 2009
). In addition, our control group consisted of European-American children who had not experienced social deprivation. Although our findings suggest that these non-deprived youths do not show differential behavioral or neural biases to in- and out-group faces, a better control would have consisted of European-American children who had been adopted from within the United States. This control group would have better controlled for the general effects of early adverse care giving. Nonetheless, our findings demonstrate differential responses to in- and out-group faces among youths who experienced early race deprivation. We have no reason to speculate that adverse rearing environments would result in differential processing of race. However, future work that identifies individuals with documentable race deprivation in the absence of social deprivation would confirm this assumption.
In conclusion, our findings highlight the role of experience in the development of the ORE. Complete deprivation to other-race faces in infancy disrupts recognition of emotion and results in heightened amygdala response to out-group faces. These data provide support that early postnatal development may represent a sensitive period for emotion recognition of out-group faces.