Vocal Learning via Social Reinforcement by Infant Marmoset Monkeys

Abstract

For over half a century now, primate vocalizations have been thought to undergo little or no experience-dependent acoustic changes during development [1]. If any changes are apparent, then they are routinely (and quite reasonably) attributed to the passive consequences of growth. Indeed, previous experiments on squirrel monkeys and macaque monkeys showed that social isolation [2, 3], deafness [2], cross-fostering [4] and parental absence [5] have little or no effect on vocal development. Here, we explicitly test in marmoset monkeys-a very vocal and cooperatively breeding species [6]-whether the transformation of immature into mature contact calls by infants is influenced by contingent parental vocal feedback. Using a closed-loop design, we experimentally provided more versus less contingent vocal feedback to twin infant marmoset monkeys over their first 2 months of life, the interval during which their contact calls transform from noisy, immature calls to tonal adult-like "phee" calls [7, 8]. Infants who received more contingent feedback had a faster rate of vocal development, producing mature-sounding contact calls earlier than the other twin. The differential rate of vocal development was not linked to genetics, perinatal experience, or body growth; nor did the amount of contingency influence the overall rate of spontaneous vocal production. Thus, we provide the first experimental evidence for production-related vocal learning during the development of a nonhuman primate.

Female Social Feedback Reveals Non-imitative Mechanisms of Vocal Learning in Zebra Finches

“…In contrast to these findings in humans, the immature song of songbirds is generally considered a non-communicative epiphenomenon of motor practice [10][11][12]. Little attention has been paid to the social ecology of vocal learners, and few studies have addressed the potentially significant function of immature vocalizations in eliciting social feedback [7,8,13]. Early vocal behavior may provide learning opportunities by exploiting information available in the immediate social environment.…”

“…In contrast to songbirds, the presence of socially guided vocal learning is better characterized in infant marmoset monkeys and humans, which both have the capacity for socially guided vocal learning. Young marmosets that receive more vocal feedback from parents contingent on their immature calls develop mature calls more quickly [13]. Lack of parental interaction during development results in long-term disruptions to the acoustic structure of marmoset vocalizations, suggesting that parental feedback is necessary for proper vocal learning [27].…”

The social functions of babbling: acoustic and contextual characteristics that facilitate maternal responsiveness

“…Infants also show facilitated learning of word‐object associations when, after babbling at an object (object‐directed vocalizations: ODVs), adults immediately label that object (Goldstein, Schwade, Briesch, & Syal, ). Further, recent work using computational modeling has revealed evidence of neural mechanisms (e.g., spike‐timing dependent plasticity) that could underlie changes in vocalizations as a result of contingent feedback (e.g., Takahashi et al., ; Takahaski, Liao, & Ghanzafar, ; Warlaumont & Finnegan, ). Not all forms of caregiver responsiveness, however, have a positive effect on infant learning.…”

Vocalization development in common marmosets for neurodegenerative translational modeling

“…The range of vocalizations is well-conserved in monkeys raised in captive colonies bred for research purposes and can be evaluated without complex elicitation protocols [e.g., 28, 29, 30, 31, 32]. Vocalizations develop in common marmosets with modeling from parental feedback [33, 34], and call acoustic parameters develop differently based on call type [31]. Most published evaluations of marmoset vocalization development are performed using specialized audio recording equipment, and call analysis requires specific training.…”