Prenatal development of neonatal vocalizations
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Evaluation Summary:
This paper will be of great interest to the field of developmental neuroscience and social communication. The authors identified prenatal sensorimotor vocal precursors by detecting rhythmic orofacial movements related to vocalizations. These findings will provide new insights into the development of vocal behavior in primates. The data acquired by a highly quantitative approach support the major claims of the paper.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)
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Abstract
Human and non-human primates produce rhythmical sounds as soon as they are born. These early vocalizations are important for soliciting the attention of caregivers. How they develop remains a mystery. The orofacial movements necessary for producing these vocalizations have distinct spatiotemporal signatures. Therefore, their development could potentially be tracked over the course of prenatal life. We densely and longitudinally sampled fetal head and orofacial movements in marmoset monkeys using ultrasound imaging. We show that orofacial movements necessary for producing rhythmical vocalizations differentiate from a larger movement pattern that includes the entire head. We also show that signature features of marmoset infant contact calls emerge prenatally as a distinct pattern of orofacial movements. Our results establish that aspects of the sensorimotor development necessary for vocalizing occur prenatally, even before the production of sound.
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Evaluation Summary:
This paper will be of great interest to the field of developmental neuroscience and social communication. The authors identified prenatal sensorimotor vocal precursors by detecting rhythmic orofacial movements related to vocalizations. These findings will provide new insights into the development of vocal behavior in primates. The data acquired by a highly quantitative approach support the major claims of the paper.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)
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Reviewer #1 (Public Review):
In this manuscript, the authors measured orofacial and head movements of marmoset fetuses at multiple gestation stages. They show that these two types of movements become more independent over the course of development. They then compared the structure of the orofacial movements to the one of contact vocalization of the neonate and found that only orofacial movements matching contact calls are increasingly more prominent during gestation, compared to orofacial movements of the fetuses matching twitters or licks.
I think these are two interesting results per se, that were somehow expected based on previous literature suggesting that human fetuses exhibit movements consistent with postnatal crying. They indicate that motor movements become more structured through gestation and that some preparatory programs …
Reviewer #1 (Public Review):
In this manuscript, the authors measured orofacial and head movements of marmoset fetuses at multiple gestation stages. They show that these two types of movements become more independent over the course of development. They then compared the structure of the orofacial movements to the one of contact vocalization of the neonate and found that only orofacial movements matching contact calls are increasingly more prominent during gestation, compared to orofacial movements of the fetuses matching twitters or licks.
I think these are two interesting results per se, that were somehow expected based on previous literature suggesting that human fetuses exhibit movements consistent with postnatal crying. They indicate that motor movements become more structured through gestation and that some preparatory programs may set the stage for some post-birth vocalizations (contact calls and not twitters). Some analysis could be refined to demonstrate fully the result.
Major concerns:
- Frame-by-frame analyses were performed by experts who are aware of the study goals. Such experts are also likely to recognize the gestation stages based on the images themselves. I am concerned that the manual image processing could be influenced by the lack of blind labeling.
- How do the Shannon entropy and the KL divergence behave when a state probability is null (say stages 3 to 5 in the latest stages of gestation)? I think it is undefined.
- Stage 5 is defined with an extremely stringent criterion (both head and orofacial movements starting at less than 30ms interval). I think this is way too stringent, and the impact of making this criterion more compliant should be quantified. -
Reviewer #2 (Public Review):
Babies cry immediately after birth, but how the ability to produce sounds develops before birth remains a mystery. Marmoset monkeys have attracted much attention as a useful model for studying vocal communication, especially in the early vocal development. Infant marmosets experience a remarkable process of vocal development during the first 2 months after birth. To be sure, the vocal ability also develops during the prenatal period, but it is difficult to observe. The authors try to address this issue in marmoset monkeys by investigating their fetal orofacial movements in a densely-sampled, longitudinal ultrasound imaging study. They analyze fetal head and orofacial movements in marmoset monkeys by a highly quantitative approach and find that orofacial movements necessary for producing rhythmical …
Reviewer #2 (Public Review):
Babies cry immediately after birth, but how the ability to produce sounds develops before birth remains a mystery. Marmoset monkeys have attracted much attention as a useful model for studying vocal communication, especially in the early vocal development. Infant marmosets experience a remarkable process of vocal development during the first 2 months after birth. To be sure, the vocal ability also develops during the prenatal period, but it is difficult to observe. The authors try to address this issue in marmoset monkeys by investigating their fetal orofacial movements in a densely-sampled, longitudinal ultrasound imaging study. They analyze fetal head and orofacial movements in marmoset monkeys by a highly quantitative approach and find that orofacial movements necessary for producing rhythmical vocalizations may differentiate from a larger movement pattern that includes the entire head. More importantly, they find that signature features of marmoset infant contact calls emerge prenatally as a distinct pattern of orofacial movements. Thus, the marmoset monkey is a non-human primate model mimicking not only the vocal maturation after birth but also the sensorimotor development necessary for vocalizing occurs prenatally.
This work is interesting and meaningful. The evidence of prenatal development of orofacial movements required for vocal production is clear. The non-invasive longitudinal ultrasound imaging method is reasonable and the data analyses are highly quantitative and rigorous. The conclusions of this paper are mostly well supported by data, but some aspects of data interpretation need further discussion.
- In this study, the authors want to emphasize the difference between orofacial movements necessary for vocalizations and more global bodily movements. In fact, the development of orofacial movements is a part of the overall development of bodily movements. It is difficult to specifically correlate orofacial movements to vocal production. For example, orofacial movements may be also important for sucking or breathing. They are not in conflict.
- In the study, a distinct pattern of orofacial movements is related to the production of infant contact calls. In previous studies, marmoset monkeys have been shown to produce contact calls around every 10 s (~0.1 Hz), which is correlated with heart rate and "Mayer wave", an oscillation of the autonomic nervous system. Thus, the link between orofacial movements and the production of contact calls could be explained by the autonomic nervous system, such as breathing.
- Contact phee calls and twitter calls are mature calls in marmoset monkeys. Infant marmosets have a specific "cry" call which is similar to that of human babies. It will be of particular interest whether there is any developmental clue for the production of "cry" calls during the prenatal stage.
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Reviewer #3 (Public Review):
In their manuscript, Narayanan and colleagues use ultrasound imaging to investigate the development of prenatal orofacial movements as a precursor to neonatal vocalizations in common marmosets. Using their experimental approach, the authors identify prenatal sensorimotor precursors to vocalization by 1) distinguishing rhythmic orofacial movements associated with vocalizations from general movement patterns and 2) identifying neonatal vocalization-specific features prenatally. Studying the prenatal development of neonatal vocalizations is of great interest, and common marmosets are a good model for investigating this topic. Simultaneous spatiotemporal tracking of fetal mouth and head movements in four pregnancies makes the methodological approach comprehensive. Overall, this is important work.
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