Functional Maps at the Onset of Auditory Inputs in Very Early Preterm Human Neonates

Abstract

During the last trimester of human gestation, neurons reach their final destination and establish long- and short-distance connections. Due to the difficulties obtaining functional data at this age, the characteristics of the functional architecture at the onset of sensory thalamocortical connectivity in humans remain largely unknown. In particular, it is unknown to what extent responses evoked by an external stimulus are general or already sensitive to certain stimuli. In the present study, we recorded high-density event-related potentials (ERPs) in 19 neonates, tested ten weeks before term (28-32 weeks gestational age (wGA), that is, at an average age of 30 wGA) by means of a syllable discrimination task (i.e., a phonetic change: ba vs. ga; and a voice change: male vs. female voice). We first observed that the syllables elicited 4 peaks with distinct topographies implying a progression of the sensory input along a processing hierarchy; second, repetition induced a decrease in the amplitude (repetition suppression) of these peaks, but their latencies and topographies remained stable; and third, a change of stimulus generated mismatch responses, which were more precisely time-locked to event onset in the case of a phonetic change than in the case of a voice change. A hierarchical and parallel functional architecture is therefore able to process environmental sounds in a timely precise fashion, well before term birth. This elaborate functional architecture at the onset of extrinsic neural activity suggests that specialized areas weakly dependent on the environment are present in the perisylvian region as part of the genetic endowment of the human species.

A lateral-to-mesial organization of human ventral visual cortex at birth

“…This early organization of the visual areas at birth, beyond primary areas, dismisses the old but persisting idea of a blank slate newborn (Elman et al, 1996;Johnson, 2011). Although the human infant appears immature at birth due to his poor motor repertoire, early learning is thus supported by a pre-existing cortical architecture now extensively documented by a decade of functional brain imaging studies in infants (Arichi et al, 2010;Bartocci, Bergqvist, Lagercrantz, & Anand, 2006;Mahmoudzadeh et al, 2013;Mahmoudzadeh, Wallois, Kongolo, Goudjil, & Dehaene-Lambertz, 2016).…”

Plasticity of neonatal neuronal networks in very premature infants: Source localization of temporal theta activity, the first endogenous neural biomarker, in temporoparietal areas

“…Only limited human data are available to assess the temporal and spatial organization of these endogenous sensory-independent mechanisms, described in animals during neurodevelopment. Most studies were performed on premature infants aged over 28 wGA [Chipaux et al, 2013;Colonnese et al, 2010;Milh et al, 2007], that is, at a time when thalamic afferents already connect with cortical plate neurons [Kostovic and Judas, 2010], providing sensory inputs for auditory discrimination, for example Mahmoudzadeh et al [2013Mahmoudzadeh et al [ , 2016.…”

Magnetoencephalographic Signatures of Hierarchical Rule Learning in Newborns

“…Early responses reflect a local computation: Given the experimental paradigm, a local effect is defined by a violation of tone repetition, so the sssd and sssD sequences should differ from the two ssss and sssS sequences. Mismatch responses following a sound change in a series of repeated stimuli have been robustly found in newborns, and even before term in preterm neonates (Mahmoudzadeh, Wallois, Kongolo, Goudjil, & Dehaene-Lambertz, 2017) and in fetuses (Draganova et al, 2005;Draganova et al, 2007). Responses to sssd, although in the same direction, were weaker than for sssD.…”

“…We know that brain responses towards local changes can be observed even in very immature brains such as in preterms (Mahmoudzadeh et al, 2017) and fetuses (Draganova et al, 2005;Draganova et al, 2007). In infants, the so called Mismatch Response (MMR) occurs usually between 200-400ms after stimulus onset and is comparable to the adult Mismatch Negativity (Dehaene-Lambertz and Dehaene, 1994;Háden et al, 2016).…”