Denervation of frown muscles with botulinum toxin disrupts facial feedback to central circuitry of emotion

Background: Given that people mimic the emotional expressions of others, feedback from facial muscles has been suggested to play a role in socially-induced affect. Imitation of facial emotion patterns engages limbic regions such as the amygdala which has strong connections to autonomic brainstem regions. Facial feedback could therefore modulate activation of the amygdala and its participation in autonomic manifestations of emotional states. We tested this hypothesis by investigating the neural correlates of intentional facial mimicry after peripheral denervation of emotionally expressive face muscles via botulinum toxin (BTX).

Methods: We used functional magnetic resonance imaging to study the brain responses of healthy volunteers during imitation of angry and sad facial expressions either before (control group) or two weeks after BTX-induced paralysis of the corrugator supercilii muscle (BTX group). As a control condition, subjects were requested to observe the facial expressions without any action. We tested whether the amygdala has a neural response during imitation of angry/sad facial expressions and whether activation would be reduced in subjects with corrugator paralysis. Using connectivity analyses we tested whether reduction of the amygdala response would be associated with a decrease in functional coupling between the amygdala and brainstem regions involved in central autonomic control.

Results: In both groups imitation of both angry and sad expressions showed significant bilateral activation of the amygdale. The group comparison 'control – BTX' revealed an attenuation of the left amygdala response during imitation of angry expressions relative to baseline and relative to the observation condition in the BTX group. Attenuation of amygdala activation was absent during imitation of sadness. A coupling-by-group interaction analysis revealed that the functional connectivity of the left amygdala with the dorsolateral pons was reduced in subjects with corrugator paralysis.

Conclusion: Our data suggest that disruption of afferent input from frown muscles with BTX attenuates amygdala activation and amygdala-brainstem coupling during imitation of angry facial expressions. Given that people tend to automatically mimic the emotional expressions of others, the present study highlights a neural mechanism for the transfer of emotions during social interaction.