Cortical Processing of Multimodal Sensory Learning in Human Neonates

Abstract

Following birth, infants must immediately process and rapidly adapt to the array of unknown sensory experiences associated with their new ex-utero environment. However, although it is known that unimodal stimuli induce activity in the corresponding primary sensory cortices of the newborn brain, it is unclear how multimodal stimuli are processed and integrated across modalities. The latter is essential for learning and understanding environmental contingencies through encoding relationships between sensory experiences; and ultimately likely subserves development of life-long skills such as speech and language. Here, for the first time, we map the intracerebral processing which underlies auditory-sensorimotor classical conditioning in a group of 13 neonates (median gestational age at birth: 38 weeks + 4 days, range: 32 weeks + 2 days to 41 weeks + 6 days; median postmenstrual age at scan: 40 weeks + 5 days, range: 38 weeks + 3 days to 42 weeks + 1 days) with blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (MRI) and magnetic resonance (MR) compatible robotics. We demonstrate that classical conditioning can induce crossmodal changes within putative unimodal sensory cortex even in the absence of its archetypal substrate. Our results also suggest that multimodal learning is associated with network wide activity within the conditioned neural system. These findings suggest that in early life, external multimodal sensory stimulation and integration shapes activity in the developing cortex and may influence its associated functional network architecture.

Typical and disrupted brain circuitry for conscious awareness in full-term and preterm infants

“…This is consistent with a recent study that shows processing of cross-modal stimuli and learning of multimodal contingencies in neonates. 92 We also show that this system is yet to undergo substantial change before it resembles that of the adults. Therefore, while these findings suggest that the capacity for conscious experiences is present at birth, coupled with previous evidence, they suggest that such experiences may be limited.…”

Developmental switch in prediction and adaptation to pain in human neonates

“…A top-down driver to the habituating responses observed could be explained within an associative learning (Dall'Orso et al, 2021) and/or a predictive coding framework (Friston & Kiebel, 2009;Rao & Ballard, 1999) thus requiring information preceding the noxious event to guide subsequent stimulus processing. Predictive-coding models represent the brain as a learning and modelling engine that updates world-related predictions through the encoding of unexpected or novel inputs (i.e., the prediction error) rather than processing all aspects (e.g., saliency, intensity, position, timing) of the input at each occasion (Friston & Kiebel, 2009).…”

“…In particular, the earliest evoked potential components are modulated by the prediction of the incoming stimulus (Bendixen et al, 2012; Rauss et al, 2011), while later responses are more closely coupled with the prediction error (Stefanics et al, 2018). Expectations about a stimuli are normally manipulated before stimulus delivery with instructions to the participants, but they can also develop through basic associative learning processes such as classical conditioning, which is already possible in term neonates (Dall’Orso et al, 2021). The conditioning stimulus in our case (i.e.…”

An ode to fetal, infant, and toddler neuroimaging: Chronicling early clinical to research applications with MRI, and an introduction to an academic society connecting the field

“…Renewed interest in task-based fMRI, both in sleeping ( Adam-Darque et al, 2018 , Allievi et al, 2016 , Dall’Orso et al, 2018 , Dall’Orso et al, 2021 , Graham et al, 2013 , Sylvester et al, 2021 , Wild et al, 2017 ) and awake infants and toddlers ( Baxter et al, 2019 , Baxter et al, 2021 , Biagi et al, 2015 , Deen et al, 2017 , Ellis et al, 2021 ), has expanded the early work of Dehaene-Lambertz and others ( Anderson et al, 2001 , Arichi et al, 2012 , Dehaene-Lambertz, 2002 , Dehaene-Lambertz et al, 2006 ). This area of research has been one of the slowest to progress, with many investigators paving the way by spending years refining protocols to optimize infant comfort during MRI scans ( Raschle et al, 2012 ).…”