Modulation of amygdala activity for emotional faces due to botulinum toxin type A injections that prevent frowning

Abstract

According to the facial feedback hypothesis, when we see an angry or happy face, we contract or flex the relevant muscles to recreate the expression to assist in identifying and experiencing the emotion reflected. We investigated the facial feedback hypothesis by using botulinum toxin type A (onabotulinumtoxinA; onabotA) injections to induce temporary paralysis in the glabellar muscles (responsible for frowning) and measured functional brain activity during the processing of emotional faces. Ten females viewed pictures of happy and angry faces during two functional magnetic resonance imaging (fMRI) scan sessions: one prior (Pre) to onabotA and one following (Active) onabotA injections. We found Pre vs. Active onabotA modulation of activity in the amygdala for both happy and angry faces, as well as modulation of activity in the fusiform gyrus for happy faces. Consistent with our predictions, preventing frowning through inhibition of glabellar muscle contraction altered amygdala processing for emotional faces. The modulation of amygdala and fusiform gyrus activity following onabotA may reflect compensatory processes in a neuroanatomical circuit involved in emotional processing that is engaged when facial feedback is impaired. These data contribute to a growing literature suggesting that inhibition of glabellar muscle contraction alters neural activity for emotional processing.Clinical Trials.gov registration number: NCT03373162.

Figure 1

Schematic of study design.

Figure 2

OnabotulinumtoxinA injection sites. This figure was modified from Blumenfeld and colleagues under a Creative Commons license (CC BY-NC 4.0).

Figure 3

(A) Mean of percent pleasantness rating for happy and angry faces. Pleasantness ratings were higher for happy than angry faces and performance did not differ for ONABOTA-Pre and ONABOTA-Active injection. (B) In our a priori anatomical analysis of the amygdalae, we observed pre-post BOLD increase in left amygdala for both happy and angry faces. C) Likewise, we observed a BOLD increase in right fusiform gyrus for happy faces following the ONABOTA injection. Error bars show standard error of the mean. * indicates p < 0.05, # indicates p = 0.06.

Figure 4

Neuroanatomical circuit involved in the processing of emotional faces. Orange lines represent the sensory trigeminal innervating the brain stem and synapsing on the trigeminal nucleus. The blue lines highlight the flow of information along key regions in the circuit. Sensory neurons in the trigeminal nucleus caudalis have reciprocal connections with sensory and limbic structures and are often monosynaptic^,–. These include trigemino-amygdala, trigemino-hypothalamus, trigemino-thalamus, and trigemino-locus coeruleus connections. Layers of the skull: white, scalp; pink, periosteum; grey, bone; blue, meninges (dura, arachnoid, pia); SpV: spinal tract of the trigeminal nucleus; SSN: superior salivary nucleus;VPM: ventral posteromedial nucleus. This figure was created in Adobe Illustrator (versions 2015 and 2021).