Feeling without Seeing? Engagement of Ventral, but Not Dorsal, Amygdala during Unaware Exposure to Emotional Faces Yulia Lerner 1 , Neomi Singer 1 , Tal Gonen 1 , Yonatan Weintraub 1 , Oded Cohen 2 , Nava Rubin 3 , Leslie G. Ungerleider 4 , and Talma Hendler 5 Abstract ■ The ability to selectively perceive items in the environment may be modulated by the emotional content of those items. The neural mechanism that underlies the privileged processing of emo- tionally salient content is poorly understood. Here, using fMRI, we investigated this issue via a binocular rivalry procedure when face stimuli depicting fearful or neutral expressions competed for awareness with a house. Results revealed an interesting dissocia- tion in the amygdala during rivalry condition: Whereas its dorsal component exhibited dominant activation to aware fearful faces, a ventral component was more active during the suppression of fearful faces. Moreover, during rivalry, the dorsal and ventral com- ponents of the amygdala were coupled with segregated cortical activations in the brainstem and medial PFC, respectively. In sum- mary, this study points to a differential involvement of two clusters within the amygdala and their connected networks in naturally occurring perceptual biases of emotional content in faces. ■ INTRODUCTION Our visual system continually receives input from a plethora of environmental entities, but at any point in time, we are only aware of a select subset of these items. An im- portant factor in determining what enters awareness is the relevance and motivational content of a stimulus. Accord- ingly, it is possible that the affective associations of a spe- cific stimulus predefine its processing priority. Indeed, psychophysical studies have described shorter RTs and lower detection thresholds for negative compared with neutral visual content (Klauer, Mierke, & Musch, 2003; Eysenck & Byrne, 1994). This study aimed to examine the role of the amygdala in such emotion-driven visual prioritization. Depending on the state of awareness, an emotional stimulus can evoke different perceptual experiences (Beck & Clark, 1997; Mathews, 1990), associated with distinct neural networks (Phillips et al., 2004; Morris, Ohman, & Dolan, 1998). For example, full awareness of a potentially threatening stimulus, such as a fearful face, which commonly results in the amygdalaʼs activation, has been explained in terms of its evolutionary significance (Wager, Phan, Liberzon, & Taylor, 2003; Phan, Wager, Taylor, & Liberzon, 2002; Aggleton, 2000). However, the role of the amygdala, a core emotional area (Rolls, 2005; LeDoux, 1996), in processing faces unconsciously or under restricted awareness remains under dispute. Whereas some findings have suggested that the amygdala processes the emotional stimuli even unconsciously (Morris et al., 1998; Whalen et al., 1998), other studies have claimed that it is a matter of a perceiverʼs cognitive effort or expectation (Pessoa, Japee, Sturman, & Ungerleider, 2006; Phillips et al., 2004). These contradictory findings may be related to paradigm differences: Manipulation of different stimulus parameters may have altered the stability of participantsʼ perception. In addition, these studies did not account for the naturally occurring dynamics of perceptual selection, which involve internally driven processes. Thus, the ques- tion still remains: When faced with a continuous stream of multiple inputs from the environment, how does our brain select the ones to be processed? Here, we used fMRI with binocular rivalry (BR) to investigate the neural correlates of these perceptual dynamics without changing any external parameters of the stimulus. BR provides a unique stimulation set-up to study internally generated perceptual selection processes. The phenomenon of BR occurs when disparate images are presented to both eyes and cannot be fused into a single percept. This binocular stimulation gives rise to two (or more) different perceptual interpretations that involunta- rily compete for prevalence and that alternate stochastically over time, switching spontaneously every few seconds. Importantly, only the percepts and not the stimuli are 1 Tel Aviv Sourasky Medical Center, 2 Hebrew University of Jerusalem, 3 New York University, 4 National Institute of Mental Health, National Institutes of Health, Bethesda, MD, 5 Tel Aviv University © 2012 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 24:3, pp. 531–542