In the present study, we demonstrate for the first time that perception–action mechanisms extend to non-volitional responses that engage the autonomic nervous system. Under conditions of normal room illumination, pupil size is predominately under the control of the parasympathetic Edinger–Westphal nuclei in order to optimize ambient lighting and stimulus luminance. The Edinger–Westphal nuclei are also implicated in mechanisms through which non-luminance attributes of visual stimuli, including spatial structure and colour transiently change pupillary responses (Wilhelm et al
; Barbur, 2004
). Higher cortical regions also modulate pupil size via the Edinger–Westphal nuclei, reflecting attributes including the informational value of a stimulus and task difficulty. Two mechanisms are implicated; a direct pathway via descending direct cortical inputs and an indirect pathway via ascending reticular inputs to the Edinger–Westphal nuclei (Steinhauer and Hakerem, 1992
). Our findings extend these observations empirically by demonstrating a behaviourally selective adaptation of Edinger–Westphal responses in a social context and highlight a functional imitative mechanism contributing to social communication.
We show that perceived pupil size is a selective and salient agent in social interaction influencing the vicarious understanding of expressed sadness and inducing a coherent modulation of the observer's own pupil size. Our findings highlight an involuntary, incidental processing and mimicry of pupil size in the context of sadness. It is noteworthy that the neural systems supporting this mechanism encompass cortical regions implicated in cognitive appraisal and detailed visual representation of social signals, the amygdala, a motivational or affective centre and brainstem autonomic nuclei.
The cortex surrounding the STS is implicated in processing of socially meaningful postures and movements such as head position, eye gaze direction, lip reading, hand gestures and biological motion (Allison et al
). Studies on theory of mind extend these findings to suggest that posterior STS is generally sensitive to stimuli that signal dispositions, agency or intentional activity (Frith and Frith, 2003
). Additionally neuroimaging evidence suggests a role for the dorsal anterior cingulate in sympathetic arousal and generation of galvanic skin conductance responses (Critchley et al
). It is interesting that we observed this region to be automatically engaged with decreases in pupil size (a parasympathetic effect) suggesting the possibility of an organ-specific patterned autonomic response.
In a broader context, a discrete set of brain regions are implicated in social cognition including medial prefrontal cortex, STS and, critically, the amygdala (Brothers and Ring, 1993
, Kawashima et al
). Damage to the amygdala in humans impairs social and empathic behaviour and also the explicit recognition of facial expressions of fear (Adolphs et al
) and sadness (Adolphs and Tranel, 2004
). Interestingly, recognition of fear may be enhanced by directing patients with amygdala damage to focus on the eyes (Adolphs et al
). Our data suggest that a similar strategy may ameliorate acquired deficits in sadness perception.
Interestingly, activity within left frontal operculum, an area not typically implicated in social cognition, also reflected pupillary size in the context of perceived sadness. This region, however, is activated during both performance and observation of actions in others (Grezes and Decety, 2001
). Accordingly our observation suggests that the frontal operculum may contribute to empathic understanding of sadness through this mirror system. This contribution may be through either a direct influence of the motor mirror system on pupillary control centres or through an indirect route with activation of the mirror system because of an associated enhanced motor mimicry of the perceived facial expression. Thus, Carr and colleagues (2003
) found frontal operculum activity when subjects were instructed to either mimic emotional facial expressions or simply passively view them. Our regression analysis showing greater activity in the frontal operculum in individuals with higher pupillary contagion scores would support either of these proposed mechanisms.
It is noteworthy that other regions including the cerebellum and right parietal lobe were also recruited in processing of pupillary effects related to sadness. While these regions are not typically included within the social brain network, the activation in our study may reflect the attentional tracking of the salient role of pupils in sadness processing. Further studies are needed to integrate fully these findings with lesion data reporting affective consequences following cerebellar or parietal damage (Adolphs et al
; Schmahmann and Sherman, 1998
Over the variety of analyses performed consistent effects of pupil size were found only for expressions of sadness. Significant neural activity differences were observed for happy and angry (and, to a lesser extent, neutral) expressions, which are likely to arise from neural processing of different observed pupil sizes in these contexts. However, these effects did not extend to associated activity in pupil control centres and, as demonstrated in the separate behavioural experiment, are unlikely to have any meaningful impact on direct judgments of emotion intensity or valence. Further interpretation of the impact of this neural processing on other cognitive, behavioural and physiological functions was outside the scope of the experiment.
Previous studies examining the contributions of specific facial features to the recognition of emotional expressions may inform this relative specificity. Visual scan path studies, for example, show that recognition of sad faces is associated with a greater number and duration of fixations to the eyes region when compared with recognition of happy facial expression, associated with a greater number of fixations around the mouth (Williams et al
). Differentiation of Duchenne, or emotional smiles, from posed or non-emotional smiles, does involve fixations in the eye region. However, the focus is on the crow's feet area, lateral to that used in the recognition of sadness (Williams et al
). Studies identifying salient facial feature information at multiple spatial scales using the ‘bubbles’ technique also support a central contribution of the eye to sadness recognition (Smith et al
). The observation that β-adrenoreceptor blockade specifically impairs the recognition of sad facial expressions, but not the other basic emotions, links sadness perception to central and peripheral correlates of autonomic arousal responses (Harmer et al
). Although not addressed within the present study, we anticipate an opposite effect of pupil size when processing fear. The saliency of the eye region to fear recognition is established (Adolphs et al
), yet it remains uncertain if pupillary signals play a role in this. Nevertheless, lid retraction and facial pallor during the experience of fear indicate a marked enhancement of sympathetic facial responses, leading us to predict a likely association between perceived intensity of fear response and sympathetic pupillary dilatation.
Together, this study provides the first evidence to support a role for the autonomic nervous system in perception–action models of empathy exemplified in the emotion of sadness. Our data suggest that incidental processing of pupil size when viewing faces with sad emotional expressions modulates the perceived intensity of the observed emotion and results in an empathic modulation of the observers’ own pupil size. Owing to the automaticity of pupillary reflexes, we predict that this is likely to be independent of conscious awareness of observed pupil size. Furthermore, observed pupil size modulates activity in brain regions that are central to social cognition and in regions implicated in the mirroring of others actions. We show that the mechanism for the mirrored change in pupil involves the brainstem parasympathetic Edinger–Westphal nuclei. Together these data identify the neural substrates through which automatic mirroring of another's autonomic pupil size may enhance empathic appraisal and understanding of their feelings of sadness.