INMED/TINS special issue
Nature and nurture in language acquisition: anatomical and functional brain-imaging studies in infants

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Speech processing in adults relies on precise and specialized networks, located primarily in the left hemisphere. Behavioral studies in infants indicate that a considerable amount of language learning already takes place in the first year of life in the domains of phonology, prosody and word segmentation. Thanks to neuroimaging, we can move beyond behavioral methods and examine how the infant brain processes verbal stimuli before learning. These studies reveal a structural and functional organization close to what is described in adults and suggest a strong bias for speech processing in these regions that might guide infants as they discover the properties of their native language, although no evidence can be provided as yet for speech specificity of such networks. This review is part of the INMED/TINS special issue Nature and nurture in brain development and neurological disorders, based on presentations at the annual INMED/TINS symposium (http://inmednet.com/).

Introduction

Human language achieves efficient communication based on precise mapping between sounds and meaning that is shared by all members of a group. The power of this communication tool is based on elementary bricks that can be combined in multiple ways to convey new meanings. These elementary bricks (phonemes, syllables and words) are realized as a continuous speech signal that should be correctly segmented by the listeners to decipher the information. Most human brains easily perform these complex operations in their left perisylvian regions. Why does language processing rely on these precise brain regions? Do they possess special properties that can explain language emergence in humans? Study of the cerebral bases of language processing in adults points to structural and functional differences between hemispheres, but the long-term training of adults with such stimuli makes it unclear whether these asymmetries are the cause of language development in our species or only consequences of heavy exposure to the particular acoustic properties of speech. Comparative studies aim to differentiate between the linguistic capacities specific to humans and those shared with other animals. However, similar performances do not necessarily imply both the same strategies and neural correlates. We propose that infant studies, and particularly brain-imaging studies of infants' linguistic competences, might contribute to a reappraisal of the issue of language development in our species. Such studies should reveal what human brains before intense exposure to speech have in common with the brains of animals and with those of mature and linguistically competent human adults.

Section snippets

Structural asymmetries in the human adult brain: a basis for speech processing?

Since Broca's seminal publication [1], numerous studies in neuropsychology and neuroimaging have associated speech processing with the left perisylvian regions in most humans, and have questioned whether a particular organization of this part of the brain might explain the language faculty in our species. Indeed, structural asymmetries are observed at the macroscopic and cytoarchitectonic levels, such as a longer left sylvian fissure and a larger left planum temporale [2], and less frequently a

Brain asymmetries in animals

Another reason to doubt a strict causal relationship between brain temporal asymmetries in humans and the development of language is that the asymmetries are not restricted to human brains. Great apes also exhibit a larger left planum temporale 15, 16, although cytoarchitectonic differences between both hemispheres are less salient than in humans. For example, the lateralization of the organization of minicolumns observed in human temporal cortex has not been found in chimpanzees and rhesus

Speech processing in animals

If brain asymmetries are not unique to humans, what about processing of the speech input? One main characteristic of phoneme perception in humans is to be categorical and normalized across different acoustic realizations. Similar properties have been observed in animals. Monkeys [26], chinchillas [27] and even birds such as quails [28] can be trained to perceive speech syllables categorically as humans do, and are able to generalize this behavior to exemplars to which they have not been

Infants' early capacities to process speech

Although human speech production does not become significant before the end of the first year of life, infants display early sophisticated perceptive capacities that are rapidly modified by their linguistic environment. Neonates can discriminate between languages belonging to different rhythmic families 37, 38, as rats and tamarins do, but they clearly prefer to listen to their native language even when speakers are unknown 37, 39. Two-month-old infants orient faster to the speaker playing

A role for prenatal exposure to speech?

It is sometimes argued that the fast learning of native-language features during the first weeks of life can be explained by exposure to speech in utero, because hearing function develops during the third trimester of pregnancy. This exposure would have the advantage of centering the auditory environment on the mother's voice, which is largely audible above endogenous noises (e.g. those created by arterial blood flow or heart beats) thanks to the direct transmission to the fetal ear of the

Structural and functional asymmetries of the infant brain

In humans, early structural brain asymmetries first favor the right side. During the third trimester of gestation, the superior frontal gyrus, superior temporal gyrus and Heschl's gyrus are detectable on the right one or two weeks earlier than on the left [55]. However, the sylvian fissure is longer on the left and is associated with a larger left planum temporale already during fetal life 55, 56. Twin studies reveal a strong genetic influence in these areas [57], with little influence of

Functional continuity from infanthood to adulthood

The lateralization observed in infants is not as strong as in adults and it consolidates during development and acquisition of more sophisticated language skills [65], but the brain regions involved when infants listen to speech are nevertheless close to those observed in adults. ERPs have been used to decipher the processing of brief sounds. By subtracting the response evoked by a stimulus preceded either by itself or by another close stimulus (e.g. da da da da versus ba ba ba da), it is

Concluding remarks

From the first weeks of life onwards, the human brain displays normalization and phonetic categorization capacities, and rhythmic and prosodic sensitivity, which make it particularly adapted for processing speech. These capacities rely mostly on brain circuits similar to those observed in adults. It seems unlikely that the influence of the prenatal and postnatal auditory environment is sufficient to generate this complex organization in only a few weeks of exposure. On the contrary, the

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