Neural mechanism of unconscious perception of surprised facial expression

Abstract

Previous functional neuroimaging studies have uncovered partly separable neural substrates for perceiving different facial expressions presented below the level of conscious awareness. However, as one of the six basic emotions, the neural mechanism of unconsciously perceiving surprised faces has not yet been investigated. Using a backward masking procedure, we studied the neural activities in response to surprised faces presented below the threshold of conscious visual perception by means of functional magnetic resonance imaging (fMRI). Eighteen healthy adults were scanned while viewing surprised faces, which presented for 33 ms and immediately “masked” by a neutral face for 467 ms. As a control, they viewed masked happy or neutral faces as well. In comparison to both control conditions, masked surprised faces yielded significantly greater activation in the parahippocampal gyrus and fusiform gyrus, which associated previously with novelty detection. In the present study, automatic activation of these areas to masked surprised faces was investigated as a function of individual differences in the ability of identifying and differentiating one's emotions, as assessed by the 20-item Toronto Alexithymia Scale (TAS-20). The correlation results showed that, the subscale, Difficulty Identifying Feelings, was negatively correlated with the neural response of these areas to masked surprised faces, which suggest that decreased activation magnitude in specific brain regions may reflect increased difficulties in recognizing one's emotions in everyday life. Additionally, we confirmed activation of the right amygdala and right thalamus to the masked surprised faces, which was previously proved to be involved in the unconscious emotional perception system.

Introduction

Previous studies suggest that emotional processing includes two separate but simultaneously activated neural pathways, one operates at the explicit conscious level, and the other operates implicitly, below the level of conscious awareness (Morris et al., 1998, Whalen et al., 1998). It is proposed that the former pathway sends information along a series of high-order cortical processing areas to provide an extensive analysis of the situation and generate potential response alternatives, whereas the latter operates subcortically, below the level of conscious awareness, and information related to biologically relevant stimuli is transmitted from primary sensory cortices via the thalamus to the amygdala, providing a rapid, yet unrefined, assessment of potential emotional and motivational significance of the stimulus( LeDoux, 1996, Killgore and Yurgelun-Todd, 2004).

Neuroimaging studies demonstrate that initial responses to affective stimuli are automatic and do not require awareness (Zajonc, 1980), and an aversively conditioned masked target can elicit an emotional response from subjects without being consciously perceived (Morris et al., 1998). LeDoux (LeDoux, 1996) has proposed that the amygdala might survey emotionally valenced stimuli without awareness. Consistent with this notion, Paul J. Whalen et al. found that although subjects reported seeing only neutral faces, activation magnitude of the amygdala was significantly higher during viewing of masked fearful faces than during the viewing of masked happy faces (Whalen et al., 1998). Similar results were found in many examples of tasks executed below the level of awareness (Critchley et al., 2000, Morris et al., 1999, Whalen et al., 1998, Williams et al., 2004). Furthermore, the degree of activation of the right amygdala was negatively correlated with that of the right ventral PFC when angry faces were presented below the level of conscious perception (Nomura et al., 2004, Suslow et al., 2006). Killgore and Yurgelun-Todd (2004) indicated that masked happy faces were associated with significant bilateral activation within the anterior cingulated gyrus and amygdala, whereas masked sadness yielded only limited activation within the left anterior cingulated gyrus (Killgore and Yurgelun-Todd, 2004). Besides, unconscious perception of disgusted faces recruits basal ganglia, thalamus, fusiform gyrus, and the temporo-occipital region (Lawrence et al., 2007). However, as one of the six basic emotions (happiness, surprise, fear, sadness, anger, and disgust), the neural mechanism of unconsciously perceiving surprised faces has not yet been investigated.

The facial expression of surprise has a distinct characterization and can be recognized universally (Ekman, 1992). Psychological theories conceive surprise as an adaptive mechanism to restructure and extend cognitive concepts after analyzing an unexpected event (Schutzwolh, 1998), and it provides important indicators of emotion with respect to unexpectedness and novelty (Darwin, 1999, Schroeder et al., 2004). Darwin suggests that surprise is excited by something unexpected or unknown, so we desire, when startled, to perceive the cause as quickly as possible (Darwin, 1999). Therefore we wonder whether there is a neural system that operates subcortically, below the threshold of conscious awareness, providing rapid assessment of potential emotional and motivational significance about novelty and unexpectedness in the environment. Schroeder et al. (2004) demonstrated that perceptions of surprised facial expressions yielded consistently increased signals in the parahippocampal region, an area associated previously with novelty detection. However, the neural mechanism of unconsciously perceiving surprised faces remains poorly understood. Since surprise has no definite positive or negative valance (Ekman and Friesen, 1975), several studies focus on the different activation patterns based upon whether subjects were given positive or negative experimental stimuli. Kim et al. (2004) indicated that negatively cued surprised faces produced greater ventral amygdala activation compared to positively cued surprised faces. In the current study, however, there is not any valence cue for subjects to identify masked surprised faces, and we could exclude other emotional factors like subjects' preference to valence faces, therefore we suggest that the blood oxygen level dependent (BOLD) signal under unconscious perception of surprised face may be investigated as a function of individual differences in the ability of identifying and differentiating one's emotions, as assessed by the 20-item Toronto Alexithymia Scale (TAS-20) (Bagby et al., 1994a, Bagby et al., 1994b, Bach et al., 1996). This self-report rating scale assesses three subscales: difficulty identifying feelings, difficulty describing feelings, and externally oriented thinking. Difficulties in describing feelings should be related to impairments in the higher cortical areas responsible for conceptual encoding and speech production, whereas externally oriented thinking appears to be associated with external cognitive styles which were characterized by low interest for analytical thinking and should be primarily related to higher order cortical impairment (Suslow et al., 2006). Therefore, the score of the subscale, difficulty identifying feelings, was used to identify subject-specific differences in affective identifying ability associated with the neural activity magnitude to masked surprised faces.

The present study aimed to identify the neural mechanisms involved in unconscious perception of surprised faces, and the correlation between the neural activity to masked surprised faces and scores for difficulties in identifying feelings. Since novelty and unexpectedness were assumed to be the elicitors of surprise facial expression, we hypothesized that the parahippocampal gyrus and fusiform gyrus, which have been suggested to be implicated in the response to novel stimuli (Stern et al., 1996, Koutstaal et al., 2001, Sperling et al., 2001, Eyler Zorrilla et al., 2003), might participate in perceiving surprised faces at the unconscious level. Furthermore, based on the assumption of two neural systems for emotional perception (Morris et al., 1998, Whalen et al., 1998), the amygdala and thalamus were hypothesized to play a role in the emotional perception system when surprised faces are presented at the unconscious level. To test this hypothesis, we used functional magnetic resonance imaging (fMRI) and a backward masking procedure similar to that of previous studies to investigate the neural basis of unconscious perception of surprised facial expression.