The power of rhythms: how steady-state evoked responses reveal early neurocognitive development.

Electroencephalography (EEG) is a non-invasive and painless recording of cerebral activity, particularly well-suited for studying young infants, allowing the inspection of cerebral responses in a constellation of different ways. Of particular interest for developmental cognitive neuroscientists is the use of rhythmic stimulation, and the analysis of steady-state evoked potentials (SS-EPs) - an approach also known as frequency tagging. In this paper we rely on the existing SS-EP early developmental literature to illustrate the important advantages of SS-EPs for studying the developing brain. We argue that (1) the technique is both objective and predictive: the response is expected at the stimulation frequency (and/or higher harmonics), (2) its high spectral specificity makes the computed responses particularly robust to artifacts, and (3) the technique allows for short and efficient recordings, compatible with infants' limited attentional spans. We additionally provide an overview of some recent inspiring use of the SS-EP technique in adult research, in order to argue that (4) the SS-EP approach can be implemented creatively to target a wide range of cognitive and neural processes. For all these reasons, we expect SS-EPs to play an increasing role in the understanding of early cognitive processes. Finally, we provide practical guidelines for implementing and analyzing SS-EP studies.

Explicit access to phonetic representations in 3-month-old infants.

Preverbal infants are particularly good at discriminating syllables that differ by a single phoneme but do they perceive syllables as a whole unit or can they become aware of the underlying phonemes if their attention is attracted to the relevant level of analysis? We trained 3-month-old infants to pair two consonants, co-articulated with different vowels, with two visual shapes. Using event-related potentials, we showed that infants generalize the learned associations to new syllables with respect to the training phase. The systematic pairing of a visual label with a phonetic category is rapidly learned in a few trials, suggesting that phonemes are natural categories for infants but also that phonetic representations are accessible to internal operations outside the linguistic system. Hence, the possibility of an explicit access to the phonetic level, which is the main process underlying alphabetic reading system, is grounded in the early faculties of the human infant.

Anatomo-functional correlates of auditory development in infancy.

Infant brain development incorporates several intermingled mechanisms leading to intense and asynchronous maturation across cerebral networks and functional modalities. Combining electroencephalography (EEG) and diffusion magnetic resonance imaging (MRI), previous studies in the visual modality showed that the functional maturation of the event-related potentials (ERP) during the first postnatal semester relates to structural changes in the corresponding white matter pathways. Here investigated similar issues in the auditory modality. We measured ERPs to syllables in 1- to 6-month-old infants and related them to the maturational properties of underlying neural substrates measured with diffusion tensor imaging (DTI). We first observed a decrease in the latency of the auditory P2, and in the diffusivities in the auditory tracts and perisylvian regions with age. Secondly, we highlighted some of the early functional and structural substrates of lateralization. Contralateral responses to monoaural syllables were stronger and faster than ipsilateral responses, particularly in the left hemisphere. Besides, the acoustic radiations, arcuate fasciculus, middle temporal and angular gyri showed DTI asymmetries with a more complex and advanced microstructure in the left hemisphere, whereas the reverse was observed for the inferior frontal and superior temporal gyri. Finally, after accounting for the age-related variance, we correlated the inter-individual variability in P2 responses and in the microstructural properties of callosal fibers and inferior frontal regions. This study combining dedicated EEG and MRI approaches in infants highlights the complex relation between the functional responses to auditory stimuli and the maturational properties of the corresponding neural network.

Symbolic labeling in 5-month-old human infants.

Humans' ability to create and manipulate symbolic structures far exceeds that of other animals. We hypothesized that this ability rests on an early capacity to use arbitrary signs to represent any mental representation, even as abstract as an algebraic rule. In three experiments, we collected high-density EEG recordings while 150 5-month-old infants were presented with speech triplets characterized by their abstract syllabic structure-the location of syllable repetition-which predicted a following arbitrary label (e.g., ABA words were followed by a fish picture, AAB words by a lion). After a brief learning phase, EEG responses to novel words revealed that infants built expectations about the upcoming label based on the triplet structure and were surprised when it happened to be incongruent. Preverbal infants were thus able to recode the incoming triplets into abstract mental variables to which arbitrary labels were flexibly assigned. Importantly, infants also generalized to novel trials in which the pairing order was reversed (with the label preceding the auditory structure). Beyond conditioned associations, infants instantly inferred a bidirectional mapping between the abstract structures and the following label, a foundational operation for any symbolic system.

Classifying the mental representation of word meaning in children with Multivariate Pattern Analysis of fNIRS.

This study presents the implementation of a within-subject neural decoder, based on Support Vector Machines, and its application for the classification of distributed patterns of hemodynamic activation, measured with Functional Near Infrared Spectroscopy (fNIRS) on children, in response to meaningful and meaningless auditory stimuli. Classification accuracy nominally exceeds chance level for the majority of the participants, but fails to reach statistical significance. Future work should investigate whether individual differences in classification accuracy may relate to other characteristics of the children, such as their cognitive, speech or reading abilities.

Speech encoding by coupled cortical theta and gamma oscillations.

Many environmental stimuli present a quasi-rhythmic structure at different timescales that the brain needs to decompose and integrate. Cortical oscillations have been proposed as instruments of sensory de-multiplexing, i.e., the parallel processing of different frequency streams in sensory signals. Yet their causal role in such a process has never been demonstrated. Here, we used a neural microcircuit model to address whether coupled theta-gamma oscillations, as observed in human auditory cortex, could underpin the multiscale sensory analysis of speech. We show that, in continuous speech, theta oscillations can flexibly track the syllabic rhythm and temporally organize the phoneme-level response of gamma neurons into a code that enables syllable identification. The tracking of slow speech fluctuations by theta oscillations, and its coupling to gamma-spiking activity both appeared as critical features for accurate speech encoding. These results demonstrate that cortical oscillations can be a key instrument of speech de-multiplexing, parsing, and encoding.