Facial Expressions and the Evolution of the Speech Rhythm

Abstract

In primates, different vocalizations are produced, at least in part, by making different facial expressions. Not surprisingly, humans, apes, and monkeys all recognize the correspondence between vocalizations and the facial postures associated with them. However, one major dissimilarity between monkey vocalizations and human speech is that, in the latter, the acoustic output and associated movements of the mouth are both rhythmic (in the 3- to 8-Hz range) and tightly correlated, whereas monkey vocalizations have a similar acoustic rhythmicity but lack the concommitant rhythmic facial motion. This raises the question of how we evolved from a presumptive ancestral acoustic-only vocal rhythm to the one that is audiovisual with improved perceptual sensitivity. According to one hypothesis, this bisensory speech rhythm evolved through the rhythmic facial expressions of ancestral primates. If this hypothesis has any validity, we expect that the extant nonhuman primates produce at least some facial expressions with a speech-like rhythm in the 3- to 8-Hz frequency range. Lip smacking, an affiliative signal observed in many genera of primates, satisfies this criterion. We review a series of studies using developmental, x-ray cineradiographic, EMG, and perceptual approaches with macaque monkeys producing lip smacks to further investigate this hypothesis. We then explore its putative neural basis and remark on important differences between lip smacking and speech production. Overall, the data support the hypothesis that lip smacking may have been an ancestral expression that was linked to vocal output to produce the original rhythmic audiovisual speech-like utterances in the human lineage.

The neurobiology of primate vocal communication

“…Interestingly, breaking down the evoked responses into band-passed local field potentials (LFPs) revealed that the theta frequency band in this rostral region carried the most information about vocalizations. This is consistent with the idea that the structure of monkey vocalizations (like the structure of speech) may exploit neural activity in the theta band [15,16]. …”

The evolution of speech: vision, rhythm, cooperation

“…It is thought that the speech rhythm parses the signal into basic units from which information on a finer (faster) temporal scale can be extracted [46]. Given the importance of this rhythm in speech and its underlying neurophysiology [53, 54], understanding how speech evolved requires investigating the origins of its bi-sensory rhythmic structure.…”

“…We do know that macaque monkey vocalizations have a similar acoustic rhythmicity as human speech but without the concomitant and temporally-correlated rhythmic facial motion [55]. Modulation-spectra analyses of the acoustic rhythmicity of macaque monkey vocalizations reveal that their rhythmicity is strikingly similar to that of the acoustic envelope for speech [55] (Figure 2A). Both signals fall within the 3 – 8 Hz range (see also [56] for shared low-frequency components of macaque monkey calls and speech).…”

Convergent Evolution of Vocal Cooperation without Convergent Evolution of Brain Size

“…Thus, marmoset vocal communication, like human speech communication, can be modeled as loosely coupled oscillators. As a mechanistic description of vocal turn taking, coupled oscillators are advantageous since they are consistent with the data from speech processing that brain oscillations are critical to temporal structure [Giraud and Poeppel, 2012;Hasson et al, 2012] and its evolution [Ghazanfar and Takahashi, 2014]. Further, such oscillations do not necessarily require any higher-order cognitive capacities to operate [Takahashi et al, 2013].…”