The prenatal brain readiness for speech processing: A review on foetal development of auditory and primordial language networks
Introduction
Language development relies on perceptual and cognitive abilities, whose developmental path is paved before birth by prenatal experience with auditory and speech input. Given the obvious technical challenges posed by inferring language cognition from experimental observations in the foetus, most studies only indirectly addressed the question of whether the foetus is sensitive to the human voice and speech features, by waiting until the child is actually born and observing her response to stimuli she heard prenatally in the mother's womb. These studies have so far produced striking evidence that newborn babies (0- to 6-day-old) already show sophisticated speech processing abilities, as reviewed in seminal works (Dehaene-Lambertz et al., 2006; Gervain, 2015; Skeide and Friederici, 2016). Behavioural and electroencephalographic evidence has indeed shown that newborns have the ability to recognize speech sounds over equally complex non-speech sounds (Vouloumanos and Werker, 2007), to distinguish between several spoken tongues that differ in intonation and rhythmic vowel-consonant proportions (Nazzi et al., 1998; Ramus et al., 1999, 2000), to discriminate phonemic changes in syllables (Bertoncini et al., 1988; Cheour-Luhtanen et al., 1995; Dehaene-Lambertz and Peña, 2001), and to discern syntactically regular phoneme sequences (e.g., 'mubaba', 'penana', following an ABB rule) from irregular sequences (e.g., 'mubage', 'penaku', following an ABC rule) (Gervain et al., 2008, 2012).
In addition to the ability of processing perceptual speech features, newborn babies display early learning abilities likely driven by prenatal exposure to linguistic stimuli. They show preference for hearing their mother’s voice versus a female stranger’s voice (DeCasper and Fifer, 1980; DeCasper and Spence, 1986; Spence and DeCasper, 1987; Fifer and Moon, 1989; Moon and Fifer, 2000), and for the mother’s native versus a non-native language (Moon et al., 1993). If their mother is bilingual, newborns show an equal preference for both languages and are able to discriminate between them (Byers-Heinlein et al., 2010). Newborns can also distinguish between native and non-native vowels (Moon et al., 2013). When exposed during pregnancy to non-native alterations of vowel phonemes, newborns showed a higher postnatal sensitivity to these alterations compared to a non-exposed control group, as reported in an electroencephalographic study by Partanen et al. (2013). Prenatal exposure to a story read aloud over gestation by either their mother or a female stranger, led newborns to display a preferential response for listening to the familiar versus a novel story, irrespective of the narrating voice (DeCasper and Spence, 1986).
This body of literature suggests that the amount and kinds of capacities that newborns possess at birth, which is referred to as “the initial state” of language acquisition (Gervain, 2015), is the result of a shared labour between learning skills set by a finely-tuned ontogenetic programme, and auditory and linguistic cues available in the foetal environment. Studies in newborn babies, however, cannot entirely exclude the possibility of language exposure biases intervening in the time interval from birth to postnatal testing. These reservations do not apply to studies on foetuses, which permit to directly elucidate the neurobiological mechanisms of the prenatal brain readiness for speech processing. Although these studies have so far suffered from more limited technical advancements, recent refinements of in-vivo multimodal Magnetic Resonance Imaging (MRI) and magnetoencephalography (MEG) engendered a great deal of new data on prenatal brain development. In the last 30 years, foetal neuroimaging has been proved to be feasible and effective in studying the developing brain, both in clinical care and research centers, enabling the acquisition of high-quality, structural and functional brain images. The accumulation of evidence has been paralleled by technological advancements, including an increase of static magnetic field strength, which provides higher signal-to-noise ratios, and the optimization of research protocols. At present, the combination of MRI and MEG methods allows to directly map the brain structure and function with extremely high spatial and temporal resolution. However, it is worth emphasizing the methodological and technical limitations affecting this body of literature, which include artifacts caused by foetal movements during scanning, reduced sample size, and lack of common foetal brain atlases. Although recent progresses have been made to address these issues, such limitations should be carefully considered when interpreting the data.
In this review we will systematically address available evidence about the prenatal neural developmental trajectories of the auditory and primordial language networks. In adult human subjects, brain regions involved in language processing, as broadly defined, have been mapped in widely distributed cortical and subcortical territories across both cerebral hemispheres. However, a highly-specialized brain network supporting core language processing functions can be identified within a more restricted neuroanatomical territory centred around the Sylvian fissure in the left hemisphere, and comprising mainly frontal and temporal brain regions, as well as the white matter fascicles that connect these regions (Friederici, 2012; Price, 2012; Fedorenko and Thompson-Schill, 2014). As we will illustrate, this language network already starts to develop and become operational in the prenatal foetal developmental stages, even though at gestational term it has not yet reached full anatomical maturation. Furthermore, even though we will present evidence that the foetal brain is already responsive at the very least to some phonological speech characteristics, it has not yet acquired the computational capacity to encode language features of greater complexity, such as those that mark the postnatal developmental transition from bottom-up to top-down language processes (Skeide & Friederici, 2016). It is in this perspective that we speak here of a “primordial” language network, as the initial structural and functional circuitry that will later develop to support full-fledged language abilities.
In what follows, we firstly outline available evidence for the prenatal development of the auditory circuitry and of language-related brain structures, as well as their structural connectivity. Secondly, we review how foetal resting-state functional MRI (rs-fMRI) brought initial evidence for the emergence of functional connectivity, and hence for the emergence of auditory and primordial language networks in the foetal brain. In the third part of the review, we will first describe which kind of sound components reach the foetuses in the womb, and to what degree. Then, we will focus on data from studies that applied fMRI and MEG to test prenatal readiness for sound processing, which is a crucial prerequisite for the foetus to gain experience with the maternal voice and with spoken language. We also discuss how multimodal foetal brain imaging has the potential to expand investigations on the prenatal readiness for language.
Section snippets
The emergence of structural networks in the foetal brain
The human cerebral cortex shows the greatest complexity among mammals. Its irregular and fascinating architecture is considered the hallmark of the human brain, supporting high-level cognitive functions such as language (Welker, 1990; Friederici, 2012; Striedter et al., 2015). Its distinctive structure is characterized by a convolutional pattern with inward and outward foldings called, respectively, sulci and gyri. Despite inter-foetuses variability, the maturation of cortical sulci and gyri
The emergence of functional networks in the foetal brain
The evidence reviewed so far suggests that, at least in primordial form, the main brain structures of the auditory and language networks are already present and inter-connected during the third trimester of gestation, although they continue to intensively develop in the subsequent months of postnatal life. Notably, also functional connectivity seems to already develop prenatally (Keunen et al., 2017). The use of rs-fMRI has proven to be extremely advantageous for understanding how functional
Prenatal readiness for experiential information processing
The studies reviewed so far suggest that the structural and functional cerebral scaffolding of the auditory and language networks is already built in foetuses at term, although further extensive maturational changes will take place in the first years of postnatal life.
On the one hand, this developmental achievement is the overall result of intermingled and complex molecular mechanisms occurring under genetic control (Vasung et al., 2019). Multiple lines of evidence claim that structural (e.g.,
Conclusions
Collectively, the reviewed studies outline current knowledge on the prenatal developmental trajectories of the auditory and primordial language brain networks. The emerging picture suggests that the neural roots of language gradually develop throughout the gestational stage and likely underlie the complex speech processing abilities that newborns possess at birth. Equipped with this body of abilities in the initial state, the newly born child is optimally prepared for the stunning unfolding of
Author contributions
M.G., C.C., and M.T. conceptualized and wrote the review paper.
Declaration of Competing Interest
The authors report no declarations of interest.
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