In this article, we demonstrated that the amygdala differentially responds to masked fearful and happy faces and that this discrimination was markedly different depending on the context within which the masked faces were presented. The current data replicate findings from previous backward masking studies showing increased amygdala activation to fearful faces when masked with neutral faces (Morris et al.
; Whalen et al.
; Rauch et al.
; Etkin et al.
; Pessoa et al.
; Williams et al.
). Furthermore, we have extended these findings by showing a selective decrease in amygdala activation to fearful faces when they were masked with non-face pattern images. The present data extend the results of our previous backward masking study (Whalen et al. 1998
) in two ways: First, we demonstrated a significant increase in amygdala activation to face-masked fearful vs
happy faces that were presented for 17 ms (compared to 33 ms in our original study), and second, we demonstrated this effect in a cohort consisting of male and female subjects, whereas our previous report studied only male subjects.
Our data from the pattern-masked condition highlight the fact that the amygdala is differentially activated by masked fearful vs happy faces, but the nature of this response is dependent on the type of mask stimulus used. This interactive effect of mask type and target face expression on amygdala activity was unexpected. Clearly, the basis of amygdala responses in the pattern-mask condition must begin with the fearful faces, but the observed signal decreases might reflect some interaction with other neural systems responding to the pattern mask. Similarly, amygdala signal increases observed in the neutral face mask condition may be influenced by both the fearful target face as well as the neutral face mask. However, the fact that we observed that the same area of the amygdala was responsive to both face- and pattern-masked fearful faces suggests that there are shared underlying neural processes involved in both conditions, which implies that the amygdala may be sensitive to masked fearful faces per se regardless of mask type.
Amygdala responses in the present experiment could be related to different proposed mechanisms of backward masking. One mechanism suggests that masking works via stimulus substitution
(see Bachmann and Allik, 1976
; Bachmann et al. 2005
for extensive discussion). By this account, the mask substitutes for the target stimulus at some level of neural representation and, thus, the first target stimulus never reaches the level of subjective awareness (Bachmann and Allik, 1976
; Rolls and Tovee, 1994
; Di Lollo et al.
). Such an account would predict similar neural responses to the emotional target stimulus per se
regardless of the mask stimulus.
An alternative proposed mechanism is known as stimulus integration
(Bachmann and Allik, 1976
; Bachmann et al. 2005
). By this account the target stimulus is amalgamated with the mask, perceived as a single object, and is therefore not reported. This account would suggest that neural responses to masked fearful faces should depend on the mask being a stimulus that can be interpreted differently based on the presence of these hidden targets (e.g. a neutral face).
Though neither of these theories necessarily implicates amygdala involvement, the differential amygdala responses observed in the face vs
pattern mask condition could be consistent with the stimulus integration account, as amygdala signal increases were observed to masked fear only in the face-masked condition. This interpretation is consistent with a recent report showing that masked fearful faces can influence the interpretation of the face mask stimulus. Specifically, surprised faces were used as the mask stimulus and were interpreted more negatively when they were used to mask fearful faces compared to happy faces (Li et al.
). Future studies could seek to extend this effect to neutral face masks.
However, the stimulus integration account of the present effects is complicated by the fact that amygdala activity did discriminate between the fearful and happy conditions in the pattern mask condition. Specifically, we observed a decrease in amygdala activation to pattern-masked fearful vs happy faces, compared with the baseline level of activity (i.e. fixation blocks) supporting the notion that the amygdala is sensitive to the masked fearful face stimuli per se.
The observed BOLD signal decreases are, of course, not an unambiguous response pattern. We can say with certainty that amygdala activity discriminated between fear and happy without the benefit of a neutral face mask. One possibility is that the amygdala activation to pattern-masked fearful faces becomes actively suppressed, perhaps because this initial signal does not make sense in the non-face context. That is, the mismatch between the information that was being processed with awareness (pattern masks) and without awareness (fearful faces) may have led to the suppression of amygdala activation. Such an account accords with models of backward masking supposing that target and mask stimuli produce direct neural competition (Keysers and Perrett, 2002
). It is not clear that BOLD signal decreases necessarily reflect diminished neuronal activity. For example, Maier and colleagues (Maier et al.
) have demonstrated that cortical BOLD signal decreases in area V1 dissociate from neuronal activity under certain psychological states (e.g. decreased BOLD but sustained neuronal activity was observed during perceptual suppression in monkeys). If this effect in cortex can be generalized to a subcortical structure like the amygdala, our data suggest the possibility that a subpopulation of neurons in the amygdala that are responsive to masked fearful faces may show sustained neuronal activity but exhibit decreased BOLD signal to pattern-masked fearful faces. If this phenomenon is related to the mismatch between the information from the mask and the target, future studies could examine the selective decrease in amygdala BOLD signal to pattern-masked fearful faces while manipulating the degree of congruency between the faces and the masks.
The observed effects are not likely due to any difference in the detectability of the fearful stimuli in the face vs
pattern mask condition, since (i) subjectively aware subjects were excluded from the analyses, (ii) exclusion of subjects who were objectively aware did not change the results and (iii) the degree of objective awareness did not predict the strength of amygdala activity in either condition. We would concede though that since we deliberately chose to assess amygdala responses to masked stimuli in naïve subjects during passive viewing (rather than in subjects who are made aware of the presence of the masked faces and are instructed to actively search for the target faces during scanning; e.g. Pessoa et al.
), we cannot rule out the possibility that some level of awareness across both conditions could have impacted our results. We assume that our objective test of awareness following scanning is a reasonable metric for identifying which individual subjects were more likely to have been aware during the earlier naïve presentations and as noted above, these data were unrelated to amygdala responses to masked fearful faces.
Also, it should be noted that we did not observe significant correlations between amygdala activity to masked fearful faces and anxiety measures or the degree of objective awareness, though previous studies have observed such relationships (Etkin et al.
; Pessoa et al.
). This discrepancy may well be due to differences in the experimental designs (block vs
event-related, passive viewing vs
active task, inclusion of non-masked conditions), and is open to further scientific inquiry.
Taken together, the present data show that amygdala activity is influenced by the fearful target stimulus as well as the interaction of the fearful face with neutral face mask. More generally, the current findings show that implicit amygdala BOLD responses to crude representations of biologically relevant stimuli can interact with the explicit processing of contextual stimuli (e.g. mask stimuli, present study; additional task demands, Pessoa et al.
). In terms of amygdala function, the present backward masking data are consistent with other experimental techniques, namely binocular rivalry (Williams et al.
), continuous flash suppression (Jiang and He, 2006
), chimerical faces (Morris et al.
) and low spatial frequency information (Vuilleumier et al.
) that also support a fundamental and automatic role for the amygdala in the assessment of biologically relevant predictive stimuli (LeDoux, 1996