Domestication Phenotype Linked to Vocal Behavior in Marmoset Monkeys.
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ABSTRACT:
SUBMITTER: Ghazanfar AA
PROVIDER: S-EPMC8204797 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Humans exhibit a high level of vocal plasticity in speech production, which allows us to acquire both native and foreign languages and dialects, and adapt to local accents in social communication. In comparison, non-human primates exhibit limited vocal plasticity, especially in adulthood, which would limit their ability to adapt to different social and environmental contexts in vocal communication. Here, we quantitatively examined the ability of adult common marmosets ( Callithrix jacchus), a highly vocal New World primate species, to modulate their vocal production in social contexts. While recent studies have demonstrated vocal learning in developing marmosets, we know much less about the extent of vocal learning and plasticity in adult marmosets. We found, in the present study, that marmosets were able to adaptively modify the spectrotemporal structure of their vocalizations when they encountered interfering sounds. Our experiments showed that marmosets shifted the spectrum of their vocalizations away from the spectrum of the interfering sounds in order to avoid the overlap. More interestingly, we found that marmosets made predictive and long-lasting spectral shifts in their vocalizations after they had experienced a particular type of interfering sound. These observations provided evidence for directional control of the vocalization spectrum and long-term vocal plasticity by adult marmosets. The findings reported here have important implications for the ability of this New World primate species in voluntarily and adaptively controlling their vocal production in social communication.
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Project description:Marmosets have attracted significant interest in the life sciences. Similarities with human brain anatomy and physiology, such as the granular frontal cortex, as well as the development of transgenic lines and potential for transferring rodent neuroscientific techniques to small primates make them a promising neurodegenerative and neuropsychiatric model system. However, whether marmosets can exhibit complex motor tasks in highly controlled experimental designs-one of the prerequisites for investigating higher-order control mechanisms underlying cognitive motor behavior-has not been demonstrated. We show that marmosets can be trained to perform vocal behavior in response to arbitrary visual cues in controlled operant conditioning tasks. Our results emphasize the marmoset as a suitable model to study complex motor behavior and the evolution of cognitive control underlying speech.
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Project description:Human vocal development is dependent on learning by imitation through social feedback between infants and caregivers. Recent studies have revealed that vocal development is also influenced by parental feedback in marmoset monkeys, suggesting vocal learning mechanisms in nonhuman primates. Marmoset infants that experience more contingent vocal feedback than their littermates develop vocalizations more rapidly, and infant marmosets with limited parental interaction exhibit immature vocal behavior beyond infancy. However, it is yet unclear whether direct parental interaction is an obligate requirement for proper vocal development because all monkeys in the aforementioned studies were able to produce the adult call repertoire after infancy. Using quantitative measures to compare distinct call parameters and vocal sequence structure, we show that social interaction has a direct impact not only on the maturation of the vocal behavior but also on acoustic call structures during vocal development. Monkeys with limited parental interaction during development show systematic differences in call entropy, a measure for maturity, compared with their normally raised siblings. In addition, different call types were occasionally uttered in motif-like sequences similar to those exhibited by vocal learners, such as birds and humans, in early vocal development. These results indicate that a lack of parental interaction leads to long-term disturbances in the acoustic structure of marmoset vocalizations, suggesting an imperative role for social interaction in proper primate vocal development.
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Project description:Communication is a keystone of animal behavior. However, the physiological states underlying natural vocal signaling are still largely unknown. In this study, we investigated the correlation of affective vocal utterances with concomitant cardiorespiratory mechanisms. We telemetrically recorded electrocardiography, blood pressure, and physical activity in six freely moving and interacting cynomolgus monkeys (Macaca fascicularis). Our results demonstrate that vocal onsets are strengthened during states of sympathetic activation, and are phase locked to a slower Mayer wave and a faster heart rate signal at ∼2.5 Hz. Vocalizations are coupled with a distinct peri-vocal physiological signature based on which we were able to predict the onset of vocal output using three machine learning classification models. These findings emphasize the role of cardiorespiratory mechanisms correlated with vocal onsets to optimize arousal levels and minimize energy expenditure during natural vocal production.
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Project description:The relationships that offspring develop with caregivers can exert a powerful influence on behavior and physiology, including the hypothalamic-pituitary-adrenal (HPA) axis. In many mammalian species, offspring-caregiver relationships are largely limited to interactions with mother. Marmoset monkeys receive care in early life from multiple classes of caregivers in addition to the mother, including fathers and siblings. We evaluated whether affiliative social interactions with family members in marmosets were associated with differences in cortisol reactivity to a short-term social separation stressor, and whether these variations in affiliative interactions upon reunion predicted how well marmosets subsequently regulated HPA axis function after cessation of the stressor. Marmosets were separated from the family for 8h at three developmental time points (6-, 12-, and 18-months of age), and interactions of the separated marmoset with the family group were recorded during reunion. Urinary cortisol was measured prior to social separation, every 2h during the separation, and on the morning after separation. Heightened cortisol reactivity during social separation did not predict affiliative social behavior upon reunion but higher rates of grooming and play behavior predicted enhanced HPA regulation. Marmosets with higher rates of grooming and play with family members upon reunion had post-stress cortisol levels closer to preseparation baseline than marmosets with lower rates of affiliative reunion behavior. Combined with previous research showing the early programming effects of social interactions with caregivers, as well as the buffering effect of a close social partner during stress, the current study highlights the high degree of behavioral and HPA adaptability to social stressors across development in marmoset monkeys.
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Project description:The ability to extract the direction of the other's gaze allows us to shift our attention to an object of interest to the other and to establish joint attention. By mapping one's own intentions on the object of joint attention, humans develop a Theory of (the other's) Mind (TOM), a functional sequence possibly disrupted in autism. Gaze following of both humans and old world monkeys is orchestrated by very similar cortical architectures, strongly suggesting homology. Also new world monkeys, a primate suborder that split from the old world monkey line about 35 million years ago, have complex social structures and one member of this group, the common marmosets (Callithrix jacchus) are known to follow human head-gaze. However, the question is if they use gaze following to establish joint attention with conspecifics. Here we show that this is indeed the case. In a free choice task, head-restrained marmosets prefer objects gazed at by a conspecific and, moreover, they exhibit considerably shorter choice reaction times for the same objects. These findings support the assumption of an evolutionarily old domain specific faculty shared within the primate order and they underline the potential value of marmosets in studies of normal and disturbed joint attention.
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Project description:Gaze shifts, the directing of the eyes to an approaching predator, preferred food source, or potential mate, have universal biological significance for the survival of a species. Our knowledge of gaze behavior is based primarily on visually triggered responses, whereas head orientation triggered by auditory stimuli remains poorly characterized. Common marmoset (Callithrix jacchus) is a diurnal, small-bodied (∼350 g), New World monkey species, known for its rich behavioral repertoires during social interactions. We used a lightweight head tracking system to measure marmosets' reflexive head orientations toward a natural stimulus presented from behind. We found that marmoset could rotate its head at angular velocities above 1,000°/s and maintained target accuracy for a wide range of rotation amplitudes (up to 250°). This unusual, saccadic head orienting behavior offers opportunities for understanding the many biological factors that have shaped the evolution of sensorimotor controls of gaze orientation by the primate brain.
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