Monkey drumming reveals common networks for perceiving vocal and nonvocal communication sounds.
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.
Remedios
Ryan
R
Max-Planck Institute for Biological Cybernetics, Spemannstrasse 38, 72076 Tübingen, Germany.
Logothetis
Nikos K
NK
Kayser
Christoph
C
D000161:Acoustic Stimulation; D000162:Acoustics; D000819:Animal Communication; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D005075:Biological Evolution; D005868:Gestures; D006801:Humans; D008253:Macaca mulatta / Q000033:anatomy & histology / Q000502:physiology* / Q000523:psychology*; D008279:Magnetic Resonance Imaging; D008297:Male; D008959:Models, Neurological; D009146:Music; D009415:Nerve Net / Q000502:physiology; D012919:Social Behavior; D013060:Speech; D013702:Temporal Lobe / Q000033:anatomy & histology / Q000502:physiology; D014828:Vocalization, Animal / Q000502:physiology*