Les substrats anatomo-fonctionnels du développement auditif et visuel : perspectives sur l'ontogénie de la latéralisation du traitement de la parole et de la reconnaissance des visages

Several cognitive functions such as face and speech processing are lateralized in the adult human brain. The ontogeny of these functional asymmetries is yet poorly understood. We aimed to evaluate the neural substrates of face and speech processing, nested in the visual and auditory networks using non-invasive neuroimaging techniques in infants. First, we studied how the functional and structural characteristics of these two brain systems change over the first postnatal semester. With EEG, we showed age-related decreases in the latency of brain responses and demonstrated that the speed of early visual responses is related to the maturation of underlying white matter tracts conducting them, as assessed with diffusion MRI. For the auditory system, our results suggested that the speed of responses may rely on maturation of more pathways and cortical regions. In parallel, we studied face processing lateralization using a discrimination paradigm of faces presented in each hemifield and observed that only the right hemisphere was able to discriminate between faces. Further evidence also suggested a transfer of face-relevant information across hemispheres. To study speech processing lateralization, we used a paradigm with monaural presentation of speech stimuli. A comparison between typical infants and infants with callosal agenesis, suggested an asymmetric transfer of auditory information across hemispheres, facilitated toward the left hemisphere, that might contribute to the lateralization of language early on. This thesis highlights the potential of neuroimaging techniques for the study of brain’s structural and functional development and of hemispheric asymmetries early on.Plusieurs fonctions cognitives sont latéralisées dans le cerveau humain adulte. Nous avons étudié l’origine des asymétries fonctionnelles chez les nourrissons, en évaluant les substrats neuronaux de reconnaissance des visages et des traitements du langage imbriqués dans les réseaux visuels et auditifs, grâce à la neuroimagerie non invasive (EEG et l’IRM de diffusion). Pour cela, nous avons étudié le développement fonctionnel et structurel de ces deux systèmes cérébraux au cours des six premiers mois postnataux. Nous avons observé que la vitesse des réponses visuelles était liée à la maturation des faisceaux de fibres de la matière blanche conduisant ces réponses, plus que l’âge des bébés, alors que la vitesse des réponses auditives doit dépendre d’un réseau de faisceaux de fibres et de régions corticales plus vaste. Parallèlement, nous avons étudié la latéralisation de la reconnaissance des visages grâce à un paradigme de discrimination des visages présentés dans chaque hémichamp. Nous avons observé que seul l'hémisphère droit pouvait discriminer les visages et que les informations pertinentes étaient transférées entre les deux hémisphères. Pour cibler la latéralisation du traitement du langage, nous avons étudié les réponses à des stimuli de la parole présentés de manière monaurale. Une comparaison entre un groupe de nourrissons avec une agénésie du corps calleux et un groupe contrôle a montré que les réponses à ces stimuli étaient transférées de façon asymétrique via le corps calleux. Cette asymétrie, facilitée vers l’hémisphère gauche, intervient probablement dans la latéralisation précoce du réseau du langage. L’ensemble de ces études mettent bien en évidence le potentiel de la neuroimagerie pour étudier le développement du cerveau et ces asymétries précoces

Infants' understanding of the causal power of agents and tools

Tools are objects that can be manipulated by agents with the intention to cause an effect in the world. We show that the cognitive capacity to understand tools is present in young infants, even if these produce arbitrary, causally opaque effects. In Experiments 1-2, we used pupillometry to show that 8-month-old infants infer an invisible causal contact to account for the –otherwise unexplained– motion of a ball. In Experiments 3, we probed 8-month-old infants’ account of a state change event (flickering of a box) that lies outside of the explanatory power of intuitive physics. Infants repeatedly watched an intentional agent launch a ball behind an occluder. After a short delay, a cube, positioned at the other end of the occluder began flickering. Rare unoccluded events served to probe infants’ representation of what happened behind the occluder. Infants exhibited larger pupil dilation, signaling more surprise when the ball stopped before touching the cube, than when it contacted the cube, suggesting that infants inferred that the cause of the state change was contact between the ball and the cube. This effect was canceled in Experiment 4, when an inanimate sphere replaced the intentional agent. Altogether, results suggest that, in the infants’ eyes, the power of the ball to cause an arbitrary state change must be inherited from an intentional agent. Eight-month-olds are thus capable of representing complex event structures, involving an intentional agent causing a change with a tool

Comment les nourrissons comprennent le pouvoir des agents et des outils

International audienceTools are objects that are manipulated by agents with the intention to cause an effect in the world. We show that the cognitive capacity to understand tools is present in young infants, even if these tools produce arbitrary, causally opaque effects. In experiments 1–2, we used pupillometry to show that 8-mo-old infants infer an invisible causal contact to account for the—otherwise unexplained—motion of a ball. In experiments 3, we probed 8-mo-old infants’ account of a state change event (flickering of a cube) that lies outside of the explanatory power of intuitive physics. Infants repeatedly watched an intentional agent launch a ball behind an occluder. After a short delay, a cube, positioned at the other end of the occluder began flickering. Rare unoccluded events served to probe infants’ representation of what happened behind the occluder. Infants exhibited larger pupil dilation, signaling more surprise, when the ball stopped before touching the cube, than when it contacted the cube, suggesting that infants inferred that the cause of the state change was contact between the ball and the cube. This effect was canceled in experiment 4, when an inanimate sphere replaced the intentional agent. Altogether, results suggest that, in the infants’ eyes, a ball (an inanimate object) has the power to cause an arbitrary state change, but only if it inherits this power from an intentional agent. Eight-month-olds are thus capable of representing complex event structures, involving an intentional agent causing a change with a tool

Right but not left hemispheric discrimination of faces in infancy

International audienceThe ontogeny of the human brain functional asymmetries is poorly understood. Are they a consequence of differential development based on competition mechanisms, or are they constitutive of the human brain architecture from the start? Using structural MRI and a face discrimination EEG paradigm with lateralized presentation of faces, we studied face perception in infants over the first postnatal semester. We showed that the corpus callosum is sufficiently mature to transfer visual information across hemispheres, but the inter-hemispheric transfer time of early visual responses is modulated by callosal fibers myelination. We also revealed that only the right hemisphere shows evidence for face discrimination when presented in the left visual-hemifield. This capability improved throughout the first semester with no evidence of discrimination in the left hemisphere. Face processing lateralization is thus a characteristic of the infant's extra-striate visual cortex, highlighting the differential left-right organization of the human brain already established in infanthood

Spatial relations trigger visual binding of people

To navigate the social world, humans must represent social entities, and the relationships between those entities, starting with the spatial relationships. Recent research suggests that two bodies are processed with particularly high efficiency in visual perception, when they are in a spatial positioning that cues interaction, i.e. close and face-to-face. Socially relevant spatial relations such as facingness may facilitate visual perception by triggering grouping of bodies into a new integrated percept, which would make the stimuli more visible and easier to process. We used electroencephalography and a frequency-tagging paradigm to measure a neural correlate of grouping (or visual binding), while female and male participants saw images of two bodies face-to-face or back-to-back. The two bodies in a dyad flickered at the frequencies F1 and F2, respectively, and appeared together at a third frequency Fd (dyad frequency). This stimulation should elicit a periodic neural response for each single body at F1 and F2, and a third response at Fd, which would be larger for face-to-face ( vs . back-to-back) bodies, if those stimuli yield additional integrative processing. Results showed that responses at F1 and F2 were higher for upright than for inverted bodies, demonstrating that our paradigm could capture body-specific activity. Crucially, the response to dyads at Fd was larger for face-to-face ( vs . back-to-back) dyads, suggesting integration mediated by grouping. Thus, spatial relations that recur in social interaction (i.e., facingness) may promote binding of multiple bodies into a new representation. This mechanism can explain how the visual system contributes to integrating and transforming the representation of disconnected individual body-shapes into structured representations of social events

Early asymmetric inter-hemispheric transfer in the auditory network: insights from infants with corpus callosum agenesis

International audienceThe left hemisphere specialization for language is a well-established asymmetry in the human brain. Structural and functional asymmetries are observed as early as the prenatal period suggesting genetically determined differences between both hemispheres. The corpus callosum is a large tract connecting mostly homologous areas; some have proposed that it might participate in an enhancement of the left-hemispheric advantage to process speech. To investigate its role in early development, we compared 13 3-4-month-old infants with an agenesis of the corpus callosum ("AgCC") with 18 typical infants using high-density electroencephalography (EEG) in an auditory task. We recorded event-related potentials (ERP) for speech stimuli (syllables and babbling noise), presented binaurally (same syllable in both ears), monaurally (babbling noise in one ear) and dichotically (syllable in one ear and babbling noise in the other ear). In response to these stimuli, both groups developed an anterior positivity synchronous with a posterior negativity, yet the topography significantly differed between groups likely due to the atypical gyration of the medial surface in AgCC. In particular, the anterior positivity was lateral in AgCC infants while it covered the midline in typical infants. We then measured the latencies of the main auditory response (P2 at this age) for the different conditions on the symmetrical left and right clusters. The main difference between groups was a ~60 ms delay in typical infants relative to AgCC, for the ipsilateral response (i.e. left hemisphere) to babbling noise presented in the left ear, whereas no difference was observed in the case of right-ear stimulation. We suggest that our results highlight an asymmetrical callosal connectivity favoring the right-to-left hemisphere direction in typical infants. This asymmetry, similar to recent descriptions in adults, might contribute to an enhancement of left lateralization for language processing beyond the initial cortical left-hemisphere advantage

Anatomo-functional correlates of auditory development in infancy

International audienceInfant 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

MRI and M/EEG studies of the white matter development in human fetuses and infants: review and opinion

International audienceAlready during the last trimester of gestation, functional responses are recorded in foetuses and preterm newborns, attesting an already complex cerebral architecture. Then throughout childhood, anatomical connections are further refined but at different rates and over asynchronous periods across functional networks. Concurrently, infants gradually achieve new psychomotor and cognitive skills. Only the recent use of non-invasive techniques such as magnetic resonance imaging (MRI) and magneto-and electroencephalography (M/EEG) has opened the possibility to understand the relationships between brain maturation and skills development in vivo. In this review, we describe how these techniques have been applied to study the white matter maturation. At the structural level, the early architecture and myelination of bundles have been assessed with diffusion and relaxometry MRI, recently integrated in multi-compartment models and multi-parametric approaches. Nevertheless, technical limitations prevent us to map major developmental mechanisms such as fibers growth and pruning, and the progressive maturation at the bundle scale in case of mixing trajectories. At the functional level, M/EEG have been used to record different visual, somatosensory and auditory evoked responses. Because the conduction velocity of neural impulses increases with the myelination of connections, major changes in the components latency are observed throughout development. But so far, only a few studies have related structural and functional markers of white matter myelination. Such multi-modal approaches will be a major challenge in future research, not only to understand normal development, but also to characterize early mechanisms of pathologies and the influence of fetal and perinatal interventions on later outcome

Event-related variability is modulated by task and development

In carefully designed experiments, cognitive scientists interpret the mean event-related potentials (ERP) in terms of cognitive operations. However, the huge signal variability from one trial to the next, questions the representability of such mean events. We explored here whether this variability is an unwanted noise, or an informative part of the neural response. We took advantage of the rapid changes in the visual system during human infancy and analyzed the variability of visual responses to central and lateralized faces in 2-to 6-month-old infants and adults using high-density electroencephalography (EEG). We observed that neural trajectories of individual trials always remain very far from ERP components, only moderately bending their direction with a substantial temporal jitter across trials. However, single trial trajectories displayed characteristic patterns of acceleration and deceleration when approaching ERP components, as if they were under the active influence of steering forces causing transient attraction and stabilization. These dynamic events could only partly be accounted for by induced microstate transitions or phase reset phenomena. Furthermore, these structured modulations of response variability, both between and within trials, had a rich sequential organization, which, in infants, was modulated by the task difficulty. Our approaches to characterize Event Related Variability (ERV) expand and reinterpret classic ERP analyses, making them compliant with pervasive neural variability and providing a more faithful description of neural events following stimulus presentation