In 1862, the French neurologist and physiologist G.-B. Duchenne de Boulogne published a remarkable treatise on facial expressions. His work was the first to systematically examine the contributions of small groups of cranial muscles to the expressions that communicate the rich experience of human emotion. Duchenne reasoned that “one would be able, like nature herself, to paint the expressive lines of the emotions of the soul on the face of man.” In so doing, he sought to understand how the coordinated contractions of groups of muscles express distinct, pan-cultural emotional states. To achieve this goal, he pioneered the use of transcutaneous electrical stimulation (called “faradization” after the British chemist and physicist Michael Faraday) to activate single muscles and small groups of muscles in the face, dorsal surface of the head, and neck. Duchenne also documented the faces of his subjects with another technological innovation: photography (see figure A). His seminal contribution was the identification of muscles and muscle groups, such as the obicularis oculi, that cannot be activated by force of the will, but only “put into play by the sweet emotions of the soul.” Duchenne concluded that the emotion-driven contraction of these muscle groups surrounding the eyes, together with the zygomaticus major, communicates the genuine experience of happiness, joy and laughter. The smile characteristic of these emotional states has therefore been termed the “Duchenne smile” by subsequent investigators.

In normal individuals, such as the Parisian shoemaker illustrated here (figure A), the difference between a forced smile (produced by voluntary contraction or electrical stimulation of facial muscles) and a spontaneous, “emotional” smile testifies to the convergence of descending motor signals from different forebrain centers onto premotor and motor neurons in the brainstem that control the facial musculature. In contrast to the Duchenne smile, the contrived smile of volition (sometimes called a “pyramidal smile”) is driven by the motor cortex, which communicates with the brainstem and spinal cord via the pyramidal tracts. The Duchenne smile is motivated by accessory motor areas in the prefrontal cortex and ventral parts of the basal ganglia that access brainstem nuclei via multisynaptic, “extrapyramidal” pathways through the brainstem reticular formation.

Studies of patients with specific neurological injury to these separate descending systems of control have further differentiated the forebrain centers responsible for control of the muscles of facial expression (figure B). Patients with unilateral facial paralysis due to damage of descending pathways from the motor cortex (upper motor neuron syndrome; see Chapter 17) are unable to move their lower facial muscles on one side, either voluntarily or in response to commands, a condition called voluntary facial paresis (figure B, left panels). Nonetheless, many such individuals produce symmetrical involuntary facial movements when they laugh, frown, or cry in response to amusing or distressing stimuli. In such patients, pathways from regions of the forebrain other than the classical motor cortex in the frontal lobe remain available to activate facial movements in response to stimuli with emotional significance. A much less common form of neurological injury, called emotional facial paresis, demonstrates the opposite set of impairments, i.e., loss of the ability to express emotions by using the muscles of the face without loss of volitional control (figure B, right panels). Such individuals are able to produce symmetrical pyramidal smiles, but fail to display spontaneous emotional expressions involving the facial musculature contralateral to the lesion. These two systems are diagrammed in figure C.

(A) Duchenne and one of his subjects undergoing “faradization” of the muscles of facial expression (1). Bilateral electrical stimulation of the zygomaticus major mimicked a genuine expression of happiness (2), although closer examination shows insufficient contraction of the obicularis oculi (surrounding the eyes) compared to spontaneous laughter (3). Stimulation of the brow and neck produced an expression of “terror mixed with pain, torture … that of the damned” (4); however, the subject reported no discomfort or emotional experience consistent with the evoked contractions.

(B) Left panels: Mouth of a patient with a lesion that destroyed descending fibers from the right motor cortex displaying voluntary facial paresis. When asked to show her teeth, the patient was unable to contract the muscles on the left side of her mouth (upper left), yet her spontaneous smile in response to a humorous remark is nearly symmetrical (lower left). Right panels: Face of a child with a lesion in the left forebrain that interrupted descending pathways from nonclassical motor cortical areas, producing emotional facial paresis. When asked to smile volitionally, the contractions of the facial muscles are nearly symmetrical (upper right). In spontaneous response to a humorous comment, however, the right side of the patient's face fails to express emotion (lower right). (C) The complementary deficits demonstrated in figure B are explained by selective lesions of one of two anatomically and functionally distinct sets of descending projections that motivate the muscles of facial expression.