Monkeys are perceptually tuned to facial expressions that exhibit a theta-like speech rhythm

Abstract

Human speech universally exhibits a 3- to 8-Hz rhythm, corresponding to the rate of syllable production, which is reflected in both the sound envelope and the visual mouth movements. Artificial perturbation of the speech rhythm outside the natural range reduces speech intelligibility, demonstrating a perceptual tuning to this frequency band. One theory posits that the mouth movements at the core of this speech rhythm evolved through modification of ancestral primate facial expressions. Recent evidence shows that one such communicative gesture in macaque monkeys, lip-smacking, has motor parallels with speech in its rhythmicity, its developmental trajectory, and the coordination of vocal tract structures. Whether monkeys also exhibit a perceptual tuning to the natural rhythms of lip-smacking is unknown. To investigate this, we tested rhesus monkeys in a preferential-looking procedure, measuring the time spent looking at each of two side-by-side computer-generated monkey avatars lip-smacking at natural versus sped-up or slowed-down rhythms. Monkeys showed an overall preference for the natural rhythm compared with the perturbed rhythms. This lends behavioral support for the hypothesis that perceptual processes in monkeys are similarly tuned to the natural frequencies of communication signals as they are in humans. Our data provide perceptual evidence for the theory that speech may have evolved from ancestral primate rhythmic facial expressions.

Fig. 1.

Example of a frame sequence from a video clip showing an avatar face producing a lip-smacking gesture. Lip-smacking is characterized by regular cycles of vertical jaw movement, often involving a parting of the lips.

Fig. 2.

Preferential viewing times are longer for biological lip-smacking rates (6 Hz) than for slower or faster manipulations (3 or 10 Hz). (A) Total viewing times in seconds for individual subjects (lines) and the grand total (mean ± SE). All but one subject showed a preference for the avatar with biological lip smack rate. (B) Preferential-looking time for each avatar (i.e., frequency), expressed in percentage of the total time viewing either avatar. Bars indicate the mean ± SE across subjects for all comparisons (6 vs. 3 or 10 Hz) and individually for subject groups tested on 6 vs. 3 Hz and 6 vs. 10 Hz, respectively. Subjects consistently preferred the 6-Hz lip-smacking versus other frequencies.

Fig. 3.

Monkey subjects respond to lip-smacking avatars with their own lip-smacking facial expressions. Three exemplars of lip-smacking movement trajectories from subjects produced when they viewed lip-smacking avatars. The y axis represents normalized units for mouth opening, with peak interlip distance during the sequence set at 100; the x axis is time in seconds.