Elsevier

Journal of Psychiatric Research

Volume 80, September 2016, Pages 93-96
Journal of Psychiatric Research

Emotional proprioception: Treatment of depression with afferent facial feedback

https://doi.org/10.1016/j.jpsychires.2016.06.009Get rights and content

Abstract

We develop the concept of emotional proprioception, whereby the muscles of facial expression play a central role in encoding and transmitting information to the brain’s emotional circuitry, and describe its underlying neuroanatomy. We explore the role of facial expression in both reflecting and influencing depressed mood. The circuitry involved in this latter effect is a logical target for treatment with botulinum toxin, and we review the evidence in support of this strategy. Clinical trial data suggest that botulinum toxin is effective in treating depression. We discuss the clinical and theoretical implications of these data. This novel treatment approach is just one example of the potential importance of the cranial nerves in the treatment of depression.

Introduction

We and others have recently found that botulinum toxin A (BT) injected into the brow muscles has significant antidepressant effects as compared to placebo in randomized controlled studies (Wollmer et al., 2012, Finzi and Rosenthal, 2014, Magid et al., 2014). Although these findings may seem surprising at first glance, they might have been predicted by a line of thought going back over a century. While it is evident that our emotions influence our facial expressions, the reverse is less obvious. Yet Charles Darwin (Darwin, 1998) proposed this to be so over a century ago, and William James agreed (James, 1890).

Both of these scientists made special reference to this facial feedback effect, which we are calling emotional proprioception, in relation to depression. Darwin, for example, first observed the omega sign between the eyebrows, shaped like the last letter of the Greek alphabet (Ω) - a result of the corrugator muscles contracting and producing two vertical slits between the eyebrows, joined at the top by a horizontal crease. He recognized the omega sign as an indicator of melancholy and noted its disappearance when patients recovered. James famously stated that he did not cry because he was sad; rather, he was sad because he cried. In both instances the hypothesis was that the external representations of sorrow or grief were actually signaling back to the emotional centers of the brain, causing or exacerbating feelings of distress.

Over the ensuing decades experimental psychologists pursued what became known as the facial feedback hypothesis, and produced numerous results suggesting that Darwin and James were correct. Signaling between the emotional centers of the brain and the facial muscles is bidirectional (Adelmann and Zajonc, 1989, Niedenthal, 2007). The goals of this article are: 1. To develop the concept of emotional proprioception (EP) and describe its underlying neuroanatomy; 2. To show how modulating EP can be beneficial in treating depression and perhaps other distressed states; and 3. To suggest that such interventions may be regarded as just one of several ways in which influencing cranial nerve function may have antidepressant effects.

Section snippets

Facial feedback hypothesis

It took about a century after Darwin’s seminal observations for researchers to systematically investigate what happens to emotional states in the brain when, either consciously, or unconsciously, the musculature of facial expression is activated.

Early research revealed that people rated cartoons as funnier when smiling than when frowning (Cupchik and Leventhal, 1974). Likewise, people also rated negative imagery as more aggressive when frowning, than when smiling (Laird, 1974). Critics of these

Emotional proprioception

Afferent nerve fibers appear to relay emotional information to the brain on a moment to moment basis, signaling our emotional state.

We propose that the brain utilizes facial muscle expression to provide such emotional proprioception (Finzi, 2013a). When we paralyze muscle fibers with BT this may signal to trigeminal nerve endings- possibly those involved in registering pain, position and muscle tension- a relief of physical stress, resulting in decreased emotional stress.

A link between

Evidence for antidepressant effects of botulinum toxin A

In an initial case series, one of us (EF) injected BT into the frown of ten depressed patients, eight of whom went into remission after one treatment (Finzi and Wasserman, 2006, Finzi, 2013b). The study was limited by its small size, lack of controls, and lack of blinding. In three subsequent randomized, double blind and placebo controlled trials, we and other researchers have found response rates of 50–60% in major depression, with about one-third of patients going into remission (Wollmer

Possible underlying neuroanatomical circuitry involved in botulinum toxin antidepressant effect

In order to understand the EP pathway that may be at work in this antidepressant effect it is worth noting that muscular activity in the region of the brow influences proprioceptive fibers of the optic branch of the trigeminal nerve. This in turn may activate the ventromedial PFC via the mesencephalic trigeminal nucleus and locus ceruleus, the latter of which has direct connections with both the amygdala and the PFC (Matsuo et al., 2015) – structures critical for emotional regulation.

We

Further implications

The concept of EP as a target for therapeutic intervention leads to two lines of speculation as to how else we might be to help able patients suffering from emotional disorders. First, what other emotional conditions might benefit from intervention with BT? And second, might the influence of this one particular cranial nerve, the trigeminal, be just one example of therapeutic benefits of modifying cranial nerve functions? Let us deal with each of these ideas in turn.

First, expressions of

Conclusions

In summary, EP is a useful concept for understanding the influence that facial muscles have on the emotional centers of the brain. We suggest that BT may be considered a potential Rx for depression. As more data accumulate, we will learn when and how best to deploy this new tool.

These studies of BT in depression also provide new horizons for other uses of this protein, and might stimulate us to give further consideration to the antidepressant uses of the cranial nerves.

Conflict of interest

Eric Finzi is a paid consultant of Allergan. Norman E. Rosenthal has no conflicts of interest to report.

Funding

No funding has been received for this article.

Contributors

Eric Finzi, Norman E. Rosenthal.

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