Abstract

Introduction

Crying is one of the few means by which human infants can communicate a variety of emotions, including hunger, pain, and frustration. The majority of research investigating infant crying has evaluated acoustic features as a non-invasive index of neurophysiological states during the neonatal period, including pain stress (Stevens et al., 2007) and medical complications (Wasz-Höckert et al., 1985). In line with these findings, the most common acoustic feature of pain-induced cries is that of fundamental frequency (F₀); for example, abnormally high F₀ values are related to a variety of medical conditions including chromosomal, endocrine, metabolic, and neurological disturbances (Wasz-Höckert et al., 1985).

Previous studies investigating preterm infants (gestational age < 37 weeks) have focused on F₀ in neonatal cries. Preterm infants exhibit higher F₀ of pain-induced cries before term-equivalent age compared to term newborns but these differences disappear around term-equivalent age (Michelsson et al., 1983; Johnston et al., 1993; Cacace et al., 1995). In contrast, the present authors found that the spontaneous cries (i.e., cries unaffected by external stress) of preterm infants at term-equivalent age are higher in terms of F₀ min, F₀ mean, and F₀ max (see section “Materials and Methods”) than those of term newborns (Shinya et al., 2014). Our research group also showed that shorter gestational age is significantly associated with higher F₀, regardless of body size at cry recording and intrauterine growth retardation [IUGR]. Thus, rather than being a product of a smaller body size, the increased F₀ of spontaneous cries in preterm infants may be the result of more complicated neurophysiological states, such as low vagal activity (Shinya et al., 2016), due to their different intra- and extrauterine experiences.

On the other hand, melody (i.e., time variation in F₀) is considered to be one of the most crucial acoustic features of infant cries. In term infants, spontaneous cries exhibit rich melodic features even during the neonatal period (Mampe et al., 2009; Wermke et al., 2016) and their cry melodies are reported to become increasingly more variable (Prescott, 1975) and complex (Wermke et al., 2002, 2007) across the first months of life. For example, developmental changes have been observed in the spontaneous cries of term infants such that F₀ variability (i.e., standard deviation [SD]) within a cry utterance increases from 28 Hz at 1–2 weeks of age to 53 Hz at 6–9 months of age (Prescott, 1975). Furthermore, the spontaneous cries of term infants show unidirectional development from mostly simple single-arc melody structures to an increasing number of multiple-arc structures during the first several months (Wermke et al., 2002, 2007; Figures 1A,B). These developmental changes in infant cry melody are assumed to reflect increases in laryngeal vocal coordination due to maturation in the developing central nervous system (CNS).

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FIGURE 1

(A) An example of spectrogram and (B) corresponding melody (i.e., time series of fundamental frequency [F₀]) contour diagrams for a complex cry with multiple-arcs. (C) Two examples of melody contours in a series of spontaneous cries in 60 s, indicating the F₀ transposition range, which means the difference between minimum and maximum values among F₀ max. The upper diagram indicated a smaller F₀ transposition range (98 Hz [478–576], 3.24 semitones), while the bottom one indicated a greater F₀ transposition range (197 Hz [405–602], 6.85 semitones). Not included in the diagrams were cry utterances excluded from the main analysis, respiratory phases, and no-phonatory periods.

Broadening the perspective, there is a potential relationship between the development of an infant’s cry melody and language acquisition (Darwin, 1872; Lieberman, 1985; Wermke and Mende, 2009). The evolutionary viewpoint emphasizes that expressive language may originate from the imitation and modification of humans’ instinctive cries by articulate sounds (Darwin, 1871). According to this view, an increased melodic variation in infant crying is assumed to provide an essential base for linguistic prosody expressive of various emotions (Darwin, 1872; Jespersen, 1922; Wermke and Mende, 2009). This assumption is consistent with observations of the high sensitivity to melodic features of adult speech during the fetal (Kisilevsky et al., 2009; Partanen et al., 2013; Webb et al., 2015) and neonatal (Kujala et al., 2004; Naoi et al., 2013) periods. Additionally, infant cry melody is shaped by ambient language during these periods (Mampe et al., 2009; Wermke et al., 2016).

The continuity between cry melody and language development is supported by phonetic evidence as well. Wermke et al. (2007) reported that a high percentage of term infants who exhibit multiple-arc melody in cries made during the second month have better language outcomes at 2.5 years (Wermke et al., 2007). Previous studies of mammals suggest that the production of infant cries in humans involves cortical regions, such as the anterior cingulate gyrus, as well as brainstem regions (Müller-Preuss and Jürgens, 1976; Jürgens, 2002; Newman, 2007). Considering the rapid maturation of the CNS during the first few months of life, the development of infant cry melody may reflect increasing voluntary vocal control by the cortex, which provides experience that facilitates control over later non-cry vocalizations related to language (Lieberman, 1985; Wermke et al., 2007).

However, the manner in which preterm birth might affect the melodic features of spontaneous cries and how these cries are related to later language acquisition in preterm peers remain unclear. Preterm infants exhibit slower acquisition of receptive and expressive language skills in their second year of life (Foster-Cohen et al., 2007; Sansavini et al., 2011) as well as during childhood (Luu et al., 2009; Barre et al., 2011; van Noort-van der Spek et al., 2012). Furthermore, during the earlier stages of language acquisition, preterm infants exhibit atypical developmental patterns of preverbal communication, such as an earlier onset of canonical babbling (Eilers et al., 1993) and reductions in joint attention (Garner et al., 1991; De Schuymer et al., 2011a; Imafuku et al., 2017). Considering their atypical developmental pattern of language acquisition, the identification of melodic features of spontaneous cries during early developmental periods and the assessment of the relationships of these features with early language acquisition are significant issues (Smith and Ulvund, 2003; Peña et al., 2010; De Schuymer et al., 2011b).

Thus, the present study assessed melodic features of spontaneous cries in preterm infants with no severe complications at a term-equivalent age and compared these features to those of term newborns (Shinya et al., 2014). In particular, the variability (i.e., height of F₀ variation) and complexity (i.e., amount of melody arcs) of the melodic features were a specific focus. Furthermore, based on the assumption of a potential link between cry melody and language development (Darwin, 1872; Lieberman, 1985; Wermke and Mende, 2009), the manner in which the analyzed melodic features of spontaneous cries at term contribute to early communication and language development at 18 months of corrected age were examined in preterm and term infants. Especially, it was expected that infants who exhibit more variable and complex cry melodies at term would show better language outcomes at 18 months. We focused on their language outcomes at 18 months of age because it has been reported that preterm infants (gestational age ≤ 32 weeks) begin to show lower receptive and expressive language development by the age, compared to term infants (Sansavini et al., 2011).

Materials and Methods

Results

Differences of Cry Melodic Features and Developmental Outcomes between Preterm and Term Infants

The acoustic features of spontaneous crying at term-equivalent age are detailed in Table ​Table11 and language developmental scores at 18 months of corrected age are provided in Table ​Table22. For the melodic features of crying, a one-way ANOVA assessing data from the gestational group revealed significant group differences in F₀ range, F₀ sigma, F₀ transposition range, and MCI number (Table ​Table11). Post hoc testing using the Bonferroni method revealed that the MLP group had higher values for F₀ range (p < 0.001), F₀ sigma (p < 0.001), F₀ transposition range (p = 0.011), and MCI number (p = 0.041) than the term group (Figure ​Figure22).

Table 2

Developmental outcomes in preterm and term infants at 18 months old of corrected age.

	Preterm infants						Term infants
	VP			MLP			Term
	M	SD	Range	M	SD	Range	M	SD	Range	F-Value	p-Value	Post hoc (p < 0.05)
MCDI	(n = 29)			(n = 27)			(n = 19)
Gesture	35	11	9–51	40	9	21–53	41	6	26–51	4.06	0.021	VP < Term
Receptive language	127	81	10–297	236	95	43–410	153	81	46–300	11.93	<0.001	VP < MLP, MLP > Term
Expressive language	24	30	0–134	63	61	1–218	38	40	1–170	4.99	0.009	VP < MLP
KSPD	(n = 30)			(n = 32)			(n = 20)
Postural-motor	96	22	28–151	105	20	55–156	101	15	64–129	1.69	0.191
Cognitive-adaptation	96	15	60–121	104	10	81–127	108	10	81–123	7.75	<0.001	VP < MLP, VP < Term
Language-social	92	14	62–116	102	15	54–125	103	11	75–120	5.62	0.005	VP < MLP, VP < Term

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VP, very preterm; MLP, moderate to late preterm; MCDI, MacArthur Communicative Development Inventory; KSPD, Kyoto Scale of Psychological Development.

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FIGURE 2

Box plots for melodic features of spontaneous crying: (A) variability indexes (i.e., F₀ range, F₀ sigma, F₀ Transposition range) and (B) melody complexity indexes (i.e., MCI ratio, MCI number) in very preterm (VP; n = 36, white box), moderate-to-late preterm (MLP; n = 41, gray box), and term infants (Term; n = 30, black box) at term-equivalent age. Boxes represent medians with upper and lower quartiles; whiskers represent maximum and minimum values, excluding outliers indicated by circles, at least 1.5 times the interquartile range (i.e., 1.5 box lengths from the upper or lower edge of the box). p < 0.05; p < 0.01.

For the developmental scores, there were significant group differences in the MCDI scores for gesture, receptive language, and expressive language and KSPD scores for the C-A and L-S (Table ​Table22). Post hoc testing of the MCDI data showed that the VP group had lower gesture scores than the term group (p = 0.046) as well as lower receptive and expressive language scores than the MLP group (p < 0.001). Additionally, the receptive language score of the MLP group was higher than that of the term group (p = 0.023). For the KSPD, the VP group exhibited a lower C-A score than the MLP and term groups (p = 0.035; p = 0.003, respectively) and the L-S score of the VP group was lower than that of the MLP group (p = 0.041).

Relations between Cry Melodic Features and Language Development

We firstly performed Pearson’s correlation to assess relations between cry melodic features at term and developmental outcomes at 18 months for all participants (MCDI: n = 75; KSPD: n = 82). The F₀ transposition range exhibited a significant positive correlation with the receptive language (r = 0.25, p = 0.033) and expressive language (r = 0.38, p < 0.001) scores on the MCDI and with the L-S score (r = 0.29, p = 0.008) on the KSPD; there were no significant correlations with the MCDI gesture score (r = 0.18, p = 0.119) or the KSPD P-M and C-A scores (r = 0.04, p = 0.729; r = 0.18, p = 0.114, respectively). Scatter plots were constructed to illustrate the correlations between F₀ transposition range at term and language development at 18 months (Figure ​Figure33). The other acoustic variables did not significantly relate to any developmental outcomes (Supplementary Table S2).

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FIGURE 3

Scatter plots and regression lines with 95% confidence intervals showing the relationships between F₀ transposition range of spontaneous cries at term-equivalent age and language outcomes at 18 months of corrected age: (A) MCDI’s gesture (n = 75, r = 0.18, p = 0.119); (B) MCDI’s receptive language (n = 75, r = 0.25, p = 0.033); (C) MCDI’s expressive language (n = 75, r = 0.38, p < 0.001); (D) KSPD’s Language-Social (n = 82, r = 0.29, p = 0.008). The groups of infants were VP (white circles), MLP (gray circles), and Term (black circles).

Additionally, hierarchical multiple regression analyses were conducted to analyze further the independent contributions of cry melodic variables to developmental outcomes, especially language development. Gestational age (Aarnoudse-Moens et al., 2009) and IUGR (Bergvall et al., 2006) were entered as independent variables in the first two steps; the next two steps included weight at cry recording and corrected age of developmental assessment, and the final step included each of the melodic variables of crying. In this model, we excluded other demographic variables related to gestational age (i.e., birth weight, Apgar score at 5 min, and postnatal age at cry recording) to avoid any collinearity of the predictors.

In the first four steps, a shorter gestational age significantly predicted lower gesture scores on the MCDI (p < 0.001) and lower P-M (p = 0.033), C-A (p < 0.001), and L-S (p = 0.004) scores on the KSPD. IUGR was significantly related to lower gesture scores on the MCDI (p = 0.018) and C-A (p = 0.005) and L-S (p = 0.018) scores on the KSPD. The next two steps did not result in significant values for any developmental outcomes (Table ​Table33). In the final step, a higher F₀ transposition range predicted higher gesture (p = 0.022), receptive language (p = 0.008), and expressive language (p < 0.001) scores on the MCDI and C-A (p = 0.024) and L-S (p < 0.001) scores on the KSPD (Table ​Table33). The other melodic features of crying and F₀ measures did not significantly predict any developmental outcomes; the partial correlation coefficients are reported in Supplementary Table S2.

Table 3

Hierarchical multiple regression analyses predicting developmental outcomes in all participants.

		MacArthur Communicative Development Inventory (n = 75)
		Gesture			Receptive language			Expressive language
Step	Predictor	β	ΔR2	ΔF	β	ΔR2	ΔF	β	ΔR2	ΔF
1	Gestational age	0.35	0.12	10.31***	0.20	0.04	3.1	0.22	0.05	3.85
2	IUGR	-0.26	0.07	5.91*	-0.08	0.01	0.47	-0.20	0.04	3.16
3	Weight at cry recording	-0.16	0.02	1.79	-0.23	0.04	3.25	-0.03	0.00	0.06
4	Corrected age at developmental assessment	-0.14	0.02	1.82	-0.13	0.02	1.26	0.02	0.00	0.03
5	F0 transposition range	0.24	0.06	5.53*	0.30	0.09	7.49**	0.40	0.16	14.99***
	R2 total =	0.29, F5,69 = 5.56, p < 0.001			19, F5,69 = 3.30, p = 0.010			0.25, F5,69 = 4.68, p < 0.001
		Kyoto Scale of Psychological Development (n = 82)
		Postural-motor			Cognitive-adaptation			Language-social
Step	Predictor	β	ΔR2	ΔF	β	ΔR2	ΔF	β	ΔR2	ΔF
1	Gestational age	0.24	0.06	4.69*	0.49	0.24	25.07***	0.32	0.10	8.95**
2	IUGR	-0.00	0.00	0.00	-0.27	0.07	8.29**	-0.25	0.06	5.87*
3	Weight at cry recording	0.04	0.00	0.09	0.09	0.01	0.66	-0.15	0.02	1.64
4	Corrected age at developmental assessment	-0.16	0.02	1.95	-0.02	0.00	0.05	-0.14	0.02	1.63
5	F0 transposition range	0.08	0.01	0.53	0.22	0.04	5.31*	0.36	0.12	13.55***
	R2 total =	0.09, F576 = 1.51, p = 0.197			0.36, F576 = 8.62, p < 0.001			0.32, F576 = 7.10, p < 0.001

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β, standardized regression coefficient; IUGR, intrauterine growth retardation p < 0.05, p < 0.01, p < 0.001.

Discussion

To the best of our knowledge, the present study is the first to investigate the effects of preterm birth on melodic features (i.e., time variation of F₀) of spontaneous cries at term-equivalent age. Additionally, the relationships of the analyzed melodic features of crying with language outcomes at 18 months of corrected age were examined in a sample including preterm and term infants, based on the assumption of cry melody as an ontogenetic origin of language (Darwin, 1872; Lieberman, 1985; Wermke and Mende, 2009). The present results revealed that the spontaneous cries of the MLP group had significantly higher F₀ variation and melody complexity compared to term infants, and that increased F₀ variation within cry series (i.e., F₀ transposition range) at term was significantly associated with better language and cognitive outcomes at 18 months. Even after confounding factors such as gestational age and IUGR were controlled for, the F₀ transposition range of spontaneous crying significantly predicted language and cognitive outcomes, particularly expressive language skill.

We demonstrated that the spontaneous cries of MLP infants at term showed higher F₀ variation (i.e., F₀ range, F₀ sigma, and F₀ transposition range) and melody complexity (i.e., MCI number) than those of term infants. In contrast, there were no significant differences in melodic features between VP and term infants. Previous studies of term infants have reported that the melody of spontaneous cries gradually exhibits increased variability (Prescott, 1975) and complexity (Wermke et al., 2002, 2007) across the first several months. These developmental changes are assumed to reflect the maturation of vocal control over melodic contours in spontaneous crying (Wermke and Mende, 2009). Additionally, because preterm infants begin vocalizing as early as 8 weeks before their projected due date (Caskey et al., 2011), the postnatal experiences of spontaneous crying at term in preterm infants may be greater than that of term infants. Therefore, the additional vocal experience of the MLP group in the extrauterine environment may facilitate vocal control over melodic contours during spontaneous crying. Actually, this observation may be in line with previous research reporting that healthy preterm infants, with age corrected for gestational age, began canonical babbling earlier than term infants (Eilers et al., 1993). On the other hand, it is possible that this additional experience might not contribute to the increased variability and complexity of cry melodies in the VP group due to their more complicated neurophysiological states (Peterson et al., 2000; Aarnoudse-Moens et al., 2009; Naoi et al., 2013; Shinya et al., 2016).

Moreover, the present study showed that a larger F₀ variation within cry series (i.e., F₀ transposition range) of spontaneous crying at term was significantly related to better language skills at 18 months. This finding is consistent with the notion of a potential continuity between the development of cry melody and language acquisition (Darwin, 1872; Lieberman, 1985; Wermke and Mende, 2009). Notably, the larger range was primarily associated with higher levels of expressive language skills at 18 months among developmental outcomes. F₀ transposition range in infant crying reflects the ability to transpose melody across different frequency levels. Although the range is reported to increase gradually with postnatal age, there are large individual differences in F₀ transposition range even during the neonatal period (Wermke and Mende, 2009). Thus, individual differences in F₀ transposition range may reflect voluntary control over cry melody, which, in turn, contributes to later non-cry vocalizations such as babbling and expressive language (Lieberman, 1985). In practice, during language acquisition, the ability to transpose a melody across different frequency levels is assumed to be necessary for imitating simple melodies and speech sounds in one’s ambient language beginning in the neonatal period (Kuhl and Meltzoff, 1996; Mampe et al., 2009; Wermke and Mende, 2009; Gratier and Devouche, 2011; Wermke et al., 2016). Importantly, the effects of F₀ transposition range at term on language development at 18 months are independent of confounding factors such as gestational age and IUGR (Hille et al., 2007; Aarnoudse-Moens et al., 2009). Considering that preterm infants, especially VP infants, have higher risks of later language-related problems (Foster-Cohen et al., 2007; Luu et al., 2009; Barre et al., 2011; Sansavini et al., 2011; van Noort-van der Spek et al., 2012), the F₀ transposition range of spontaneous cries will be an additional measure that can predict the risks in preterm peers. Nevertheless, further studies are needed to replicate this preliminary observation of a relationship between the F₀ transposition range of spontaneous cries and later language acquisition.

The present study did not reveal any significant associations between melody complexity at term and language outcomes at 18 months, which is inconsistent with previous reports showing that MCI rate during the second month is positively related to language outcomes at 2.5 years in term children (Wermke et al., 2007). The discrepancy might be due to the difference in the definitions of MCI. Wermke et al. (2007) used for a single melody arc definition an amplitude of at least three semitones, while the present study used only two semitones (Wermke et al., 2014). This different approach may increase the number of identifiable arcs and affect the results of the associations between MCI and language outcomes at 18 months. On the other hand, melody in spontaneous cries becomes increasingly more complex during the first several months of life (Wermke et al., 2002, 2007). Therefore, the melody complexity of spontaneous cries is assumed to be much lower at term age than at the second month. In fact, the mean MCI ratio at term was 0.29 in the present study while Wermke et al. (2007) found this ratio to be 0.52 during the second month. Thus, it is possible that melody complexity at term age has not sufficiently developed to reflect individual differences in voluntary vocal control that later contribute to language acquisition at 18 months of age. Future studies should follow-up the development of melody complexity of spontaneous cries in preterm peers after the term period and relate these findings to language development.

Another important finding is that the F₀ transposition range of spontaneous crying at term was positively associated with cognitive development at 18 months, as indexed by the C-A score on the KSPD. One possibility is that individual differences in F₀ transposition range at term may reflect the integrity of the developing CNS in a manner similar to that of spontaneous physical movements, such as general movements (GMs; Prechtl, 2001). Particularly in preterm infants, abnormal GMs at an early developmental stage (i.e., less variability and complexity) are a major predictor of cerebral palsy (Prechtl, 2001) and has been recently reported to relate to delayed cognitive development from infancy to school age (Butcher et al., 2009; Beccaria et al., 2012; Kanemaru et al., 2013). Less variable and frequent spontaneous movements are assumed to be due to reductions in the modulation of the generation of spontaneous movements from central pattern generators in the brainstem by the developing cerebral cortex; this can result in domain general developmental delays (Einspieler et al., 2016). Spontaneous crying is also generated from the reflexive central pattern generators in the periaqueductal gray and nucleus retroambiguus. These brainstem regions may be modulated by forebrain regions such as the amygdala and anterior cingulate cortex and lead to more variable patterns of melody in infant crying (Newman, 2007; Holstege and Subramanian, 2015). Thus, the limited F₀ transposition range in spontaneous crying at term might reflect the reduced integrity of the developing CNS, which may be a partial risk factor of cognitive delay (Butcher et al., 2009; Einspieler et al., 2016).

The present study has several limitations that should be noted. First, the selection of participants for the present study might reflect a sample bias because the sample size was relatively small, especially for the term group. Future research is needed to replicate these findings using a larger sample that controls for confounding factors, such as socioeconomic status (Eilers et al., 1993; Fernald et al., 2012) and exposure to another language (Hoff et al., 2011), which may potentially affect developmental outcomes, including language development. Second, the present study did not investigate the melodic features of spontaneous cries in preterm infants from birth onward through development. To examine further the possibility that additional vocal experience may facilitate the development of cry melodies in healthy preterm peers, a longitudinal assessment of the developmental process from birth to term age will be required. Third, language development was evaluated only at 18 months of corrected age. In the present study, the difference in language development between the preterm and term groups at that timepoint was smaller than that observed in previous studies (Foster-Cohen et al., 2007; Sansavini et al., 2011). This may be because the present study included only preterm peers without severe complications and because the relationships between low birth weight and cognitive outcomes have been mitigated by recent medical advances (Goisis et al., 2017). However, researchers also need to follow-up with language outcomes after 18 months, considering that several recent studies have reported preterm children exhibit higher risks of language-related problems after infancy (Luu et al., 2009; Barre et al., 2011; van Noort-van der Spek et al., 2012).

Conclusion

The present study revealed that MLP infants exhibited greater F₀ variation and complexity in neonatal spontaneous crying at term age compared to term infants, although the differences were not found between VP and term infants. Furthermore, F₀ variation within cry series (i.e., F₀ transposition range) was positively related to language development, particularly expressive language skills, at 18 months, which is consistent with previous observations of the potential link between cry melody and language (Darwin, 1872; Lieberman, 1985; Wermke and Mende, 2009). The present findings suggest that the additional postnatal vocal experience of MLP infants increased F₀ variation and complexity of spontaneous cries at term. Additionally, the increased F₀ variation within cry series may partially reflect developing voluntary vocal control, which contributes to expressive language in infancy. Future studies should examine whether assessments of the melodic features of crying represent a valuable addition to existing early indices and improve the ability to predict language outcomes in preterm peers.

Author Contributions

YS, MK, FN, MI, and MM contributed to the conception and design of the work; contributed in revising the work for important intellectual content. YS, FN, and MI contributed in the data acquisition. YS, MK, and MM contributed in the analysis and interpretation of data for the work. YS and MI contributed in drafting the work. All authors approved the final version to be published, and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

Footnotes

References