Daniel Takahashi

Barbara Shinn-Cunningham

eLife assessment
This is an important study on changes in newborns' neural abilities to distinguish auditory signals at 37 weeks of gestation. The evidence of change in neural discrimination as a function of gestational age is convincing, but further analysis of the acoustic signals and description of the infants' language environment would strengthen the interpretation of the results. The work contributes to the field of neurodevelopment and suggests potential clinical applications in neurodevelopmental disorders.

anonymous

Reviewer #1 (Public Review):
Summary:
This manuscript aimed to investigate the emergence of emotional sensitivity and its relationship with gestational age. Using an oddball paradigm and event-related potentials, the authors conducted an experiment in 120 healthy neonates with a gestational age range of 35 to 40 weeks. A significant developmental milestone was identified at 37 weeks gestational age, marking a crucial juncture in neonatal emotional responsiveness.
Strengths:
This study has several strengths, by providing profound insights into the early development of social-emotional functioning and unveiling the role of gestational age in shaping neonatal perceptual abilities. The methodology of this study demonstrates rigor and well-controlled experimental design, particularly involving matched control sounds, which enhances the reliability of the research. Their findings not only contribute to the field of neurodevelopment, but also showcase potential clinical applications, especially in the context of autism screening and early intervention for neurodevelopmental disorders.
Weaknesses:
More details should be provided in terms of inclusion and exclusion criteria for the participants, as well as missing data due to the non-cooperation of newborns during the experimental process. Potential differences between preterm and full-term infants are worth exploring. Several aspects of EEG data analyses and data interpretation should be better clarified.

Reviewer #2 (Public Review):
Summary:
This is an important and very interesting report on a change in newborns' neural abilities to distinguish auditory signals as a function of the gestational age (GA) of the infant at birth (from 35 weeks GA to 40 weeks GA). The authors tested neural discrimination of sounds that were labeled 'happy' vs 'neutral' by listeners that represent two categories of sound, either human voices or auditory signals that mimic only certain properties of the human vocal signals. The finding is that a change occurs in neural discrimination of the happy and neutral auditory signals for infants born at or after 37 weeks of gestation, and not prior (at 35 or 36 weeks of gestation), and only for discrimination of the human vocal signals; no change occurs in discrimination of the nonhuman signals over the 35- to 40-week gestational ages tested. The neural evidence of discrimination of the vocal happy-neutral distinction and the absence of the discrimination of the control signals is convincing. The authors interpret this as a 'landmark' in infants' ability to detect changes in emotional vocal signals, and remark on the potential value of the test as a marker of the infants' interest in emotional signals, underscoring the fact that children at risk for autism spectrum disorder may not show the discrimination. Although the finding is novel and interesting, additional discussion is essential so that readers understand two potential caveats affecting this interpretation.
Strengths:
The event-related potential (ERP) method and results are clear, well-described, and convincing.
Weaknesses/ Information needed:
First, readers need to see spectrograms that show the 0-4000 Hz in more detail, rather than what is now shown (0-10,000 Hz). The vocal signals in clearer spectrograms will show I believe the initial consonant burst and formant frequencies that are unique to human speech and give rise to the perception of the consonant sounds in the vocal signals like 'dada' and 'tutu' that were tested. The control signals will presumably not show these abrupt acoustic changes at their onset, even though they appear (from the oscillograms) to approximate the amplitude envelope. The primary cue distinguishing the happy and neutral signals in both the vocal and control signals is the pitch of the signals (high vs low), but the burst of energy representing the consonants is only contained in the vocal signals; it has no comparable match in the control signals. It is possible that the presence of a sharp acoustic onset (a unique characteristic of consonants in human speech) is especially alerting to the infants, and that this acoustic cue, in the context of the pitch change, enhances discrimination in the vocal case. One way to test this would be to use only vowel sounds to represent the vocal signals, without consonants. Another critical detail that the authors need to include about the signals is an explanation of how the control signals were generated. The text states that the Fo and amplitude envelope of the vocal signals were mimicked in the control signals, but what was the signal used for the controls? Was a pure tone complex modulated, or was pink noise used to generate the control signals? Or were the original vocal signals simply filtered in some way to create the controls, which would preserve the Fo and amplitude envelope? If merely filtered, the control signals still may be perceived as 'vocal' signals, rather than as nonspeech (the Supplement contains the sounds, and some of the control sounds can be perceived, to my ear, as 'vocal' signals).
Second, there is no information in the manuscript or supplement about the auditory environment of the participants, nor discussion of the fetus' ability to hear in the womb. In the womb, infants are listening to the mothers' bone-conducted speech (which is full of consonant sounds), and we know from published studies that infants can discern differences not only in the prosody of the speech they hear in the womb, but the phonetic characteristics of the mother's speech. The ability at 37 weeks GA or beyond to discriminate the pitch changes in the vocal, but not control signals, could thus be due to additional experience in utero to speech. Another experiential explanation is that the infants born at 37 weeks GA and beyond may be exposed to greater amounts of speech after birth, when compared to those born at 35 and 36 weeks GA, from the attending nurses and from their caregivers, and this speech is also full of consonant sounds. What these infants hear is likely to be 'infant-directed speech,' which is significantly higher in pitch, mirroring the signals tested here. At 37 weeks GA, infants are likely more robust, may sleep less, and are likely more alert. If infants' exposure to speech, either after birth, or their auditory ability to discern differences in speech in utero, is enhanced at 37 weeks GA and beyond, then an 'experience-related' explanation is a viable alternative to a maturational explanation, and should be discussed. Perhaps both are playing a role. As the authors state, many more signals need to be tested to discern how the effect should be interpreted, and other viable interpretations of the current results discussed.

Neonatal sensitivity to vocal emotions: A milestone at 37 weeks of gestational age

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