Saturday, September 07, 2024

Active sampling as an information seeking strategy in primate vocal interactions

Thiago T. Varella,
Daniel Y. Takahashi &
Asif A. Ghazanfar

Communications Biology volume 7, 
Article number: 1098 (2024) Cite this article
Article

Open access
Published: 07 September 2024
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Abstract

Active sensing is a behavioral strategy for exploring the environment. In this study, we show that contact vocal behaviors can be an active sensing mechanism that uses sampling to gain information about the social environment, in particular, the vocal behavior of others. With a focus on the real-time vocal interactions of marmoset monkeys, we contrast active sampling to a vocal accommodation framework in which vocalizations are adjusted simply to maximize responses. We conduct simulations of a vocal accommodation and an active sampling policy and compare them with actual vocal interaction data. Our findings support active sampling as the best model for real-time marmoset monkey vocal exchanges. In some cases, the active sampling model was even able to partially predict the distribution of vocal durations for individuals to approximate the optimal call duration. These results suggest a non-traditional function for primate vocal interactions in which they are used by animals to seek information about their social environments.


Introduction


Contact calls are produced by a variety of animals, particularly when they are out of sight of one another. The functions of contact calls seem to be context-dependent. Among primate species, the same vocalizations are variously used during territorial encounters, mate attraction and isolation1. In all contexts, contact calls produced by one individual typically elicit a similar vocalization by another. There are two common assumptions as to the immediate purpose of these vocal exchanges. The first is that the goal of each individual is to maximize the probability of a response from the other (e.g., frogs2,3 and monkeys4,5). The second assumption is that, in some cases, vocal plasticity is used to either adjust these vocalizations acoustically to signal social closeness or to optimize signal transmission in noisy environments. This, again, has the purpose of increasing the probability of a vocal response (a phenomenon known as “vocal accommodation”6). Here, we consider another possibility: vocal exchanges are a form of active sensing used to gain information about conspecifics (that is, they are active sampling)7, information that can be used to estimate the probability of response. By active sensing, we mean the purposive use of motor control to emit a self-generated energetic signal to collect sensory information8. Active sampling, on the other hand, is defined as defined as gathering information that is important for a specific task7.

Marmoset monkeys are one species where there has been much focus on the use of their contact calls in vocal exchanges (Fig. 1). When by themselves, adult marmosets will produce contact calls and will do so approximately every 10 s as a function of an autonomic nervous system rhythm9,10. When auditory contact is made, two marmosets will communicate with multiple back-and-forth exchanges of contact calls10. When the distance between them changes or if they become visible to each other, then marmosets adjust the latency, loudness, and/or duration of their contact calls and/or switch to producing different affiliative call types11,12. These and other data demonstrate that marmoset vocal production remains flexible (or plastic) throughout adulthood13,14,15. Here, we test whether the real-time contact calling behavior of marmoset monkeys is consistent with active sampling. Are they interrogating their social environment using a “question-and-answer” strategy?

One proposal for active sampling suggests that animals in complex environments with incomplete information use a belief-based policy16, where “belief” here means the state of an animal’s knowledge at that moment. In a belief-based system, information has value, and this value can motivate exploration under conditions in which they must consider many alternatives and where the potential rewards are not known beforehand. In the context of contact calling by marmoset monkeys who, under natural conditions, live in dense, tropical rainforests where they cannot easily see conspecifics, we hypothesize that vocalizing is a way of seeking information about conspecifics.

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https://www.nature.com/articles/s42003-024-06764-8

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