Monkey drumming reveals common networks for perceiving vocal and nonvocal communication sounds

Abstract

Salient sounds such as those created by drumming can serve as means of nonvocal acoustic communication in addition to vocal sounds. Despite the ubiquity of drumming across human cultures, its origins and the brain regions specialized in processing such signals remain unexplored. Here, we report that an important animal model for vocal communication, the macaque monkey, also displays drumming behavior, and we exploit this finding to show that vocal and nonvocal communication sounds are represented by overlapping networks in the brain's temporal lobe. Observing social macaque groups, we found that these animals use artificial objects to produce salient periodic sounds, similar to acoustic gestures. Behavioral tests confirmed that these drumming sounds attract the attention of listening monkeys similarly as conspecific vocalizations. Furthermore, in a preferential looking experiment, drumming sounds influenced the way monkeys viewed their conspecifics, suggesting that drumming serves as a multimodal signal of social dominance. Finally, by using high-resolution functional imaging we identified those brain regions preferentially activated by drumming sounds or by vocalizations and found that the representations of both these communication sounds overlap in caudal auditory cortex and the amygdala. The similar behavioral responses to drumming and vocal sounds, and their shared neural representation, suggest a common origin of primate vocal and nonvocal communication systems and support the notion of a gestural origin of speech and music.gestures ͉ speech ͉ temporal lobe S ocial living requires effective means of expression and many species communicate by using sounds. Communication sounds can be as diverse as the methods used to produce them, covering a range of temporal rates and spectral frequencies, ranging from rattlesnake rattling and stork clapping to complex human speech. Interestingly, some species communicate not only by using a variety of sounds produced by the same means, but also by using sounds produced by different means. Humans, for example, produce vocal sounds including speech and nonspeech utterances, as well as nonvocal sounds-also called acoustic gestures (1-4). Acoustic gestures encompass a range of sounds such as the discrete knocking on a door, rhythmic hand clapping, and even thumping a table in anger. Animals, too, create sounds akin to acoustic gestures in addition to their vocalizations; for example, some nonhuman primates create sounds by chest beating or hand clapping (5-7), and rodents create sounds by drumming their paws on the ground (8). The use of nonvocal acoustic signals for communication raises two fundamental questions: first whether the same brain regions are specialized for the processing of vocal and nonvocal communication sounds; and second, whether vocal and nonvocal communication systems share a common evolutionary origin (2,3,(9)(10)(11)(12).Insights into the evolution of human communication systems can be revealed by comparative studies on closely related primate models, wh...

Supramodal Representation of Emotions

“…Studies in nonhuman primates revealed an ability to integrate socially relevant multimodal cues from conspecifics (Ghazanfar and Logothetis, 2003), which is characterized by responsiveness of amygdala and auditory cortex (Ghazanfar et al, 2005;Remedios et al, 2009), superior temporal sulcus (STS) (Ghazanfar et al, 2008), and ventrolateral prefrontal cortex (Sugihara et al, 2006). However, it remained ambiguous whether this pattern was driven by emotional integration or low-level stimulus features.…”

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

“…Macaque monkeys frequently produce such rhythmic gestures by shaking the branches of a tree or by hitting the ground, resulting in periodic sounds. Captive macaques exhibit a similar behavior by shaking environmental objects (53). Intriguingly, the rhythmic structure of this nonfacial acoustic gesture falls into the theta range as well, with typical frequencies around 5 Hz.…”

“…Using preferential-orienting tests, the behavioral relevance of such drumming sounds was demonstrated. Moreover, these acoustic gestures preferentially activate those auditory cortical regions known to be sensitive to vocal communication sounds (53), which may generate the prominent low-frequency rhythms observed in the auditory cortex (17). Thus, communicative audiovisual displays, whether produced using hands or orofacial structures, exhibit similar temporal organization, suggesting that the link between the rhythmic organization of cortical activity and the rhythmic structure of communication signals is general and effector-independent.…”

Primate social structure as a predictor of modes of communication and the ability to learn a human language

“…Tactile communication is intimate, involving skin-to-skin contact such as allogrooming and embracing (Weber 1973) and is used to maintain social structure, strengthen bonds between individuals, relieve stress and social agitation and maintain mother-infant attachments (Hertenstein et al 2006). Auditory communication can occur through vocalisations, as well as acoustic gestures such as tree buttress drumming (Arcadi et al 1998), branch shaking (Zhao 1997), chest-beating or hand-clapping (Kalan and Rainey 2009), and is used to express social status (Remedios et al 2009), defend territory, assist in agonistic confrontations and advertise alliances and group strength (Hagen and Hammerstein 2009). Finally, visual communication can involve the use of brachiomanual gestures such as arm-raising (Pollick and de Waal 2007) and beckoning (Hobaiter and Byrne 2011), facial expressions (Micheletta et al 2015) and body language/posture (Smith and Delgado 2015) to convey messages about an individual's internal state such as emotions and desires (Pika et al 2003;Parr et al 2005).…”