Intrinsic and extrinsic factors driving vocal interactions in marmoset monkeys

Abstract

A key question for understanding speech evolution is whether or not the vocalizations of our closest living relatives — nonhuman primates — represent the precursors to speech. Some believe that primate vocalizations are not volitional, but are instead inextricably linked to internal states like arousal with different vocalizations produced simply as a result of the animal’s changing state. However, testing the integrity of this claim has been difficult given that it is difficult to get a quantitative measure of arousal in the wild but also difficult to elicit different call-types in the lab because of the scarcity of contextual cues driving complex vocal behaviors. To address this quandary, we present a behavioral paradigm that reliably elicits different types of affiliative vocalizations from marmosets while measuring their heart rate via non-invasive electromyography (EMG). By modulating both the physical distance between marmosets and the sensory information available to them, we find that arousal levels are linked, but not inextricably, to vocal production. External factors like the calls of the partner also drive the temporal and spectral dynamics of the vocal interaction.

To further examine the interplay between arousal and the processing of sensory stimuli, we examined a node in the vocal production network, the anterior cingulate cortex (ACC), that is known to modulate and be modulated by arousal. However, the ACC exhibits extensive structural and functional heterogeneity and so we first utilize functional ultrasound imaging, with its excellent temporal and spatial resolution, to localize vocal perception-correlated subregions of the ACC. We then performed targeted recordings of those ACC neurons during playback of different call types while simultaneously collecting EMG data. We found a significant proportion of neurons in the ACC exhibited significant but heterogeneous responses to call playback. In addition to representing different call-types, neural responses also reflect differences in the acoustic structure within a call type. When taking the marmoset’s current arousal state before call playback onset, we also show modulation of the neurons responsiveness to call type presentation and sensitivity to call features. This coupling of internal states and sensory processing may be a mechanism underlying the ability to respond adaptively and flexibly to dynamic events in the environment.