Cortical Auditory-Evoked Responses in Preterm Neonates: Revisited by Spectral and Temporal Analyses

Abstract

Characteristic preterm EEG patterns of "Delta-brushes" (DBs) have been reported in the temporal cortex following auditory stimuli, but their spatio-temporal dynamics remains elusive. Using 32-electrode EEG recordings and co-registration of electrodes' position to 3D-MRI of age-matched neonates, we explored the cortical auditory-evoked responses (AERs) after 'click' stimuli in 30 healthy neonates aged 30-38 post-menstrual weeks (PMW). (1) We visually identified auditory-evoked DBs within AERs in all the babies between 30 and 33 PMW and a decreasing response rate afterwards. (2) The AERs showed an increase in EEG power from delta to gamma frequency bands over the middle and posterior temporal regions with higher values in quiet sleep and on the right. (3) Time-frequency and averaging analyses showed that the delta component of DBs, which negatively peaked around 550 and 750 ms over the middle and posterior temporal regions, respectively, was superimposed with fast (alpha-gamma) oscillations and corresponded to the late part of the cortical auditory-evoked potential (CAEP), a feature missed when using classical CAEP processing. As evoked DBs rate and AERs delta to alpha frequency power decreased until full term, auditory-evoked DBs are thus associated with the prenatal development of auditory processing and may suggest an early emerging hemispheric specialization.

The intimate relationship between coalescent generators in very premature human newborn brains: Quantifying the coupling of nested endogenous oscillations

“…In line with our previous results (Routier et al, 2017), click stimuli similar to those used to evoke delta-brush activities in preterm newborns before 35 wGA (Chipaux et al, 2013;Kaminska et al, 2017) did not evoke TTA-SW events between 24-27 wGA. TTA-SW events for both bursts and IBI were considered in this analysis.…”

“…This observation holds in adults (Chacko et al, 2018;Helfrich, Mander, Jagust, Knight, & Walker, 2018;Mak-McCully et al, 2017;Mölle, Bergmann, Marshall, & Born, 2011;Voytek et al, 2010), where intrinsic CFC constitutes a key feature of ongoing neural activity (Engel, Gerloff, Hilgetag, & Nolte, 2013;Hyafil, Giraud, Fontolan, & Gutkin, 2015), which in turn supposedly enhances combinatorial opportunities for encoding (Fell & Axmacher, 2011;Rasch & Born, 2013) and facilitates synaptic plasticity (Bergmann & Born, 2018;Buzsáki & Draguhn, 2004;Salimpour & Anderson, 2019). In the present work, we show that this generic mechanism is already in place early in the course of development, that is, before the onset of better-known development-related oscillatory activities such as spindle bursts (M. T. Colonnese & Phillips, 2018;Khazipov & Milh, 2018), delta brush (Kaminska et al, 2017) and neonatal prefrontal oscillations (Brockmann, Pöschel, Cichon, & Hanganu-Opatz, 2011).…”

“…A prudent analogy with the visual system may suggest that TTA-SW is correlated with spontaneous cochlear activity before the onset of hearing, and independent of the auditory exogenous stimuli. These spontaneous activities thus differ from the delta-spindles described in animals (Chipaux et al, 2013;Kaminska et al, 2017;Khazipov & Milh, 2018;Luhmann & Khazipov, 2018;Milh et al, 2006;Minlebaev et al, 2007) and the delta-brushes observed in human newborns after 28 wGA (André et al, 2010), which are at least partly driven by exogenous sensory stimuli (Chipaux et al, 2013;Kaminska et al, 2017). It has been suggested that these delta oscillations (within which higher frequencies in the alpha and beta range are nested) are involved in amplifying and controlling sensory inputs via complex mechanisms involving the thalamus, the subplate, and the cortical plate (Murata & Colonnese, 2016).…”

Cortical responses to tactile stimuli in preterm infants

“…Recent experimental findings have demonstrated distinct developmental changes in the cortical processing of afferent information (Bernhard, Kolmodin, & Meyerson, ; Luhmann & Khazipov, ), while prior human work has suggested significant developmental changes in the early responses of multiple sensory modalities (Ellingson, , ; Hrbek et al, ; Hrbek & Mareš, ; Kaminska et al, ; Whitehead, Papadelis, Laudiano‐Dray, Meek, & Fabrizi, ). In our study, we observed an expected decline in cSER amplitudes; however, we also found a perhaps unexpected lack of comparable change in the iSERs.…”

“…These findings together are compatible with the idea that the prominent ipsilateral responses in the preterm primary sensory cortices are a developmentally transient phenomenon during the period when organization of the sensorimotor cortical networks is guided by sensory input (Inacio et al, ). The immature, bursting‐type sensory responses akin to SERs are known to arise from a complex network involving subplate‐cortex structures, they disappear after the age comparable to human neonatal period (Chipaux et al, ; Kaminska et al, ; Luhmann & Khazipov, ) and they will be replaced by the adult‐like intracortical responses (for a schematic drawing, see Vanhatalo and Lauronen ()). Hence, though we cannot pinpoint the exact cortical area generating the prominent iSERs observed in our study, we suggest that they represent organization of the bilateral sensorimotor cortical networks, a phenomenon specific for the preterm period.…”