Effect of Pupil Size on the Amygdala of the Beholders
Effect of Pupil Size on the Amygdala of the Beholders
Among a range of cognitive functions of the amygdala, recent studies suggest its involvement in identification of the pupil size. To further address its role, we investigated the response of the amygdala to human and cat faces with varied pupil size, taking into account the effect of the gender and subjective attractiveness ratings. Twenty-seven subjects underwent functional magnetic resonance imaging while viewing faces with large and small pupils. Large pupil faces induced increased activation in the amygdala, without interactions with either subject or stimuli gender, although no equivalent activation differences were seen for cat face stimuli. The activation differences were irrespective of the perceived attractiveness, and without explicit knowledge about the manipulation of the pupil size. These data support the idea that the amygdala is responsive not only to explicit or implicit fear, abhorrence or preference, but also to other elements that might suggest heightened vigilance of biologically relevant stimuli, which does not necessarily require subjective awareness.
Face perception is one of the most developed visual perceptual skills in humans, and extensive neuroscience research has focused on visual processing of faces and facial expressions (for review, see Haxby et al., 2000). Among the structures of the face, the eyes are considered to provide much information about a person's state of mind, intentions and identity. Larger ratio of exposed sclera area in the human eyes (Kobayashi and Kohshima, 1997) allows a better gaze direction discrimination or detection of emotion and human infants shift their attention in the direction of another's gaze as early as 3 months of age (Hood et al., 1998). The human amygdala is known to be involved in the process of redirecting gaze toward the eye region (Adolphs et al., 2005), and that its activity is enhanced for emotionally laden (Breiter et al., 1996; Morris et al., 1996; Blair et al., 1999; Hariri et al., 2002; Gläscher et al., 2004; Reinders et al., 2005), or unfamiliar (Dubois et al., 1999) faces. In addition to the researches focused on the eye widening and eye gaze (for review, see Itier and Batty, 2009), recent studies suggest that the human amygdala is engaged in identification of more subtle changes in the eyes that are not considered to necessarily convey emotional expressions, such as the pupil size of others (Harrison et al., 2006; Demos et al., 2008). In studies investigating whether observed pupil size modulates our perception of other's emotional expressions, Harrison et al. (2006) showed that the amygdala is more responsive to smaller pupil faces with sad expressions, but not to those with other expressions. Another study tested the response of the amygdala in male subjects, using female faces as stimuli (Demos et al., 2008), on the contrary, showed that the amygdala is more responsive for faces with larger pupils. The results were inconsistent, and it is less clear under what kind of circumstances the pupil size evokes the response in the amygdala.
While pupil dilation is considered a facial signal indicating heightened vigilance on the part of a conspecifics (Ursin and Kaada, 1960; Applegate et al., 1983), it has also long been thought to convey sexual interests in conspecifics in Western cultures as reflected in an anecdote of Belladonna eye drops (extract of a plant containing atropine) that is known to be employed by women in the Victorian Era and the Italian Renaissance who purposefully dilated their pupils to appear more attractive to male suitors (Demos et al., 2008). Behavioral studies have indeed shown positive correlations between the pupil size of female faces and attractiveness rated by male subjects (Hess, 1965, 1975; Stass and Willis, 1967; Tomlinson et al., 1978; Bull and Shead, 1979), which was not always replicable in corresponding studies in female subjects (Stass and Willis, 1967; Tomlinson et al., 1978; Bull and Shead, 1979). Although Demos et al. (2008) excluded the possible influence of the attractiveness (Winston et al., 2007; Sergerie et al., 2008) in their deliberate study, it is still possible to attribute greater responses in the amygdala of male subjects for larger pupil women faces to implicit preference that is primarily based on sexual interests as indicated by the literature. We, therefore, hypothesized that the amygdala sensitivity for pupil size is gender dependent, and the amygdala might not show greater activity for larger pupils when male faces are shown to male subjects or female or male faces were shown to female subjects, which can explain the incongruent results in the context on neutral facial expressions by Harrison et al. (2006) to some extent.
Alternatively, on the basis of the data showing that the amygdala is responsive to wide-eyed faces with either neutral, fearful or surprised expressions (Morris et al., 1996; Kim et al., 2003, 2004) or that subliminal presentation of larger size of fearful eye whites alone (Whalen et al., 2004) can provoke greater responses in the amygdala, faces with large pupils might induce larger responses irrespective of the gender or even for non-human faces.
Based on the findings that presentation of the smaller pupils in the context of sad facial expressions was associated with significantly greater neural activity in the amygdala, and that subjects' pupils constricted in response to the observed smaller pupils, again, only for faces with sad expressions (Harrison et al., 2006), the activation in the amygdala might be interpreted as reflecting its role in mirroring papillary contagion of observed sad face stimuli. However, in light of the evidence that stimulation of the amygdala is associated with pupillary dilatation (Gastaut et al., 1952; Wilson et al., 1952; Koikegami and Yoshida, 1953) such a direct interpretation might be difficult to explain their findings.
To address these questions, we performed an event-related functional magnetic resonance imaging (fMRI) study, employing both male and female face stimuli shown to both sexes of the subjects. In addition, to further test the generality of its role, we also examined the response of the amygdala to cat face stimuli with large and small pupils.
Abstract and Introduction
Abstract
Among a range of cognitive functions of the amygdala, recent studies suggest its involvement in identification of the pupil size. To further address its role, we investigated the response of the amygdala to human and cat faces with varied pupil size, taking into account the effect of the gender and subjective attractiveness ratings. Twenty-seven subjects underwent functional magnetic resonance imaging while viewing faces with large and small pupils. Large pupil faces induced increased activation in the amygdala, without interactions with either subject or stimuli gender, although no equivalent activation differences were seen for cat face stimuli. The activation differences were irrespective of the perceived attractiveness, and without explicit knowledge about the manipulation of the pupil size. These data support the idea that the amygdala is responsive not only to explicit or implicit fear, abhorrence or preference, but also to other elements that might suggest heightened vigilance of biologically relevant stimuli, which does not necessarily require subjective awareness.
Introduction
Face perception is one of the most developed visual perceptual skills in humans, and extensive neuroscience research has focused on visual processing of faces and facial expressions (for review, see Haxby et al., 2000). Among the structures of the face, the eyes are considered to provide much information about a person's state of mind, intentions and identity. Larger ratio of exposed sclera area in the human eyes (Kobayashi and Kohshima, 1997) allows a better gaze direction discrimination or detection of emotion and human infants shift their attention in the direction of another's gaze as early as 3 months of age (Hood et al., 1998). The human amygdala is known to be involved in the process of redirecting gaze toward the eye region (Adolphs et al., 2005), and that its activity is enhanced for emotionally laden (Breiter et al., 1996; Morris et al., 1996; Blair et al., 1999; Hariri et al., 2002; Gläscher et al., 2004; Reinders et al., 2005), or unfamiliar (Dubois et al., 1999) faces. In addition to the researches focused on the eye widening and eye gaze (for review, see Itier and Batty, 2009), recent studies suggest that the human amygdala is engaged in identification of more subtle changes in the eyes that are not considered to necessarily convey emotional expressions, such as the pupil size of others (Harrison et al., 2006; Demos et al., 2008). In studies investigating whether observed pupil size modulates our perception of other's emotional expressions, Harrison et al. (2006) showed that the amygdala is more responsive to smaller pupil faces with sad expressions, but not to those with other expressions. Another study tested the response of the amygdala in male subjects, using female faces as stimuli (Demos et al., 2008), on the contrary, showed that the amygdala is more responsive for faces with larger pupils. The results were inconsistent, and it is less clear under what kind of circumstances the pupil size evokes the response in the amygdala.
While pupil dilation is considered a facial signal indicating heightened vigilance on the part of a conspecifics (Ursin and Kaada, 1960; Applegate et al., 1983), it has also long been thought to convey sexual interests in conspecifics in Western cultures as reflected in an anecdote of Belladonna eye drops (extract of a plant containing atropine) that is known to be employed by women in the Victorian Era and the Italian Renaissance who purposefully dilated their pupils to appear more attractive to male suitors (Demos et al., 2008). Behavioral studies have indeed shown positive correlations between the pupil size of female faces and attractiveness rated by male subjects (Hess, 1965, 1975; Stass and Willis, 1967; Tomlinson et al., 1978; Bull and Shead, 1979), which was not always replicable in corresponding studies in female subjects (Stass and Willis, 1967; Tomlinson et al., 1978; Bull and Shead, 1979). Although Demos et al. (2008) excluded the possible influence of the attractiveness (Winston et al., 2007; Sergerie et al., 2008) in their deliberate study, it is still possible to attribute greater responses in the amygdala of male subjects for larger pupil women faces to implicit preference that is primarily based on sexual interests as indicated by the literature. We, therefore, hypothesized that the amygdala sensitivity for pupil size is gender dependent, and the amygdala might not show greater activity for larger pupils when male faces are shown to male subjects or female or male faces were shown to female subjects, which can explain the incongruent results in the context on neutral facial expressions by Harrison et al. (2006) to some extent.
Alternatively, on the basis of the data showing that the amygdala is responsive to wide-eyed faces with either neutral, fearful or surprised expressions (Morris et al., 1996; Kim et al., 2003, 2004) or that subliminal presentation of larger size of fearful eye whites alone (Whalen et al., 2004) can provoke greater responses in the amygdala, faces with large pupils might induce larger responses irrespective of the gender or even for non-human faces.
Based on the findings that presentation of the smaller pupils in the context of sad facial expressions was associated with significantly greater neural activity in the amygdala, and that subjects' pupils constricted in response to the observed smaller pupils, again, only for faces with sad expressions (Harrison et al., 2006), the activation in the amygdala might be interpreted as reflecting its role in mirroring papillary contagion of observed sad face stimuli. However, in light of the evidence that stimulation of the amygdala is associated with pupillary dilatation (Gastaut et al., 1952; Wilson et al., 1952; Koikegami and Yoshida, 1953) such a direct interpretation might be difficult to explain their findings.
To address these questions, we performed an event-related functional magnetic resonance imaging (fMRI) study, employing both male and female face stimuli shown to both sexes of the subjects. In addition, to further test the generality of its role, we also examined the response of the amygdala to cat face stimuli with large and small pupils.
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