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:Multiple strategies have evolved to compensate for masking noise, leading to changes in call features. One call adjustment is the Lombard effect, an increase in call amplitude in response to noise. Another strategy involves call production in periods where noise is absent. While mechanisms underlying vocal adjustments have been well studied, mechanisms underlying noise avoidance strategies remain largely unclear. We systematically perturbed ongoing phee calls of marmosets to investigate noise avoidance strategies. Marmosets canceled their calls after noise onset and produced longer calls after noise-phases ended. Additionally, the number of uttered syllables decreased during noise perturbation. This behavior persisted beyond the noise-phase. Using machine learning techniques, we found that a fraction of single phees were initially planned as double phees and became interrupted after the first syllable. Our findings indicate that marmosets use different noise avoidance strategies and suggest vocal flexibility at different complexity levels in the marmoset brain.
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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:ObjectiveIn adult female rodents, ovarian estradiol (E2) regulates body weight, adiposity, energy balance, physical activity, glucose-insulin homeodynamics, and lipid metabolism, while protecting against diet-induced obesity. The same E2 actions are presumed to occur in primates, but confirmatory studies have been lacking.MethodsWe investigated the consequences of ovariectomy (OVX) and E2 replacement in female marmoset monkeys on major metabolic and morphometric endpoints. Sexual behavior and uterine diameters were assessed as positive controls for E2 treatment efficacy. Metabolic parameters were measured 1 mo prior to OVX, and 3 and 6 mo thereafter. During OVX, animals received empty or E2-containing silastic s.c. implants. To test the interaction between E2 and diet, both treatment groups were assigned to either a higher fat diet (HFD) or a low-fat diet (LFD).ResultsAs anticipated, OVX animals exhibited diminished frequency (p = 0.04) of sexually receptive behavior and increased rejection behavior (p = 0.04) toward their male partners compared with E2-treated OVX females. OVX also decreased (p = 0.01) uterine diameter. There were no treatment effects on total caloric intake. There were no significant effects of OVX, E2 treatment, or diet on body weight, body composition, energy expenditure, physical activity, fasting glucose, or glucose tolerance. Regardless of E2 treatment, serum triglycerides were higher (p = 0.05) in HFD than LFD females. Postmortem qPCR analysis of hypothalamic tissues revealed higher mRNA expression (p < 0.001) for PGR in E2-treated monkeys versus OVX controls regardless of diet, but no differences between groups in other selected metabolic genes. In contrast, regardless of E2 treatment, there was a decreased mRNA expression of PGC1α (PPARGC1A), HTR1A, and HTR5A in HFD compared with LFD females.ConclusionsOur findings, overall, document a greatly diminished role for ovarian E2 in the metabolic physiology of a female primate, and encourage consideration that primates, including humans, evolved metabolic control systems regulated by extra-ovarian E2 or are generally less subject to E2 regulation.
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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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Project description:Vocal communication in animals often involves taking turns vocalizing. In humans, turn-taking is a fundamental rule in conversation. Among non-human primates, the common marmoset is known to engage in antiphonal calling using phee calls and trill calls. Calls of the trill type are the most common, yet difficult to study, because they are not very loud and uttered in conditions when animals are in close proximity to one another. Here we recorded trill calls in captive pair-housed marmosets using wearable microphones, while the animals were together with their partner or separated, but within trill call range. Trills were exchanged mainly with the partner and not with other animals in the room. Animals placed outside the home cage increased their trill call rate and uttered more trills in response to their partner compared to strangers. The fundamental frequency, F0, of trills increased when animals were placed outside the cage. Our results indicate that trill calls can be monitored using wearable audio equipment and that minor changes in social context affect trill call interactions and spectral properties of trill calls.
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