Skip to main content
Top
Published in: Brain Structure and Function 7/2020

01-09-2020 | Original Article

Functional and structural correlates of the preterm infant’s brain: relating developmental changes of auditory evoked responses to structural maturation

Authors: Farveh Daneshvarfard, Hamid Abrishami Moghaddam, Guy Kongolo, Fabrice Wallois, Mahdi Mahmoudzadeh

Published in: Brain Structure and Function | Issue 7/2020

Login to get access

Abstract

Functional responses recorded during the last trimester of gestation reveal that human sensory activity begins before birth, allowing the brain to process the external environment. Along with the maturation of the brain, new cognitive skills emerge in the human infant’s brain. The development of non-invasive techniques provides the opportunity to study the relationship between brain structural maturation and cognitive development in vivo. Here, we aimed to relate developmental changes of the latency of cortical auditory evoked potentials (CAEPs) to a structural maturation index, presumed to be representative of myelination. CAEPs to syllables were recorded in 17 preterm neonates with a mean recording age of 30.5 weeks gestational age (28.4–32.2 wGA). The latency of the first peak of the global field power (GFP) was considered the functional feature of interest to be examined for correlation with age and the structural maturation index extracted from brain atlases of the corresponding term age. GFP latency significantly decreased with age (R2 = 0.311, p = 0.02). Structural maturation indices, calculated as the mean values of T1w/T2w image intensities, were extracted for various brain regions. We observed significant correlations between the maturation indices of the auditory-involved areas and the latency of the GFP first-peak, as well as age. In hierarchical models, neither the structural maturation index nor age contributed to significant additional variance in the GFP first-peak latency after accounting for the variance associated with the other parameter.
Literature
go back to reference Adibpour P et al (2019) Anatomo-functional correlates of auditory development in infancy. bioRxiv. Adibpour P et al (2019) Anatomo-functional correlates of auditory development in infancy. bioRxiv.
go back to reference Alho K et al (1990) Event-related brain potential of human newborns to pitch change of an acoustic stimulus. Electroencephalogr Clin Neurophysiol 77:151–155CrossRef Alho K et al (1990) Event-related brain potential of human newborns to pitch change of an acoustic stimulus. Electroencephalogr Clin Neurophysiol 77:151–155CrossRef
go back to reference Baumann N, Pham-dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871–927CrossRef Baumann N, Pham-dinh D (2001) Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81:871–927CrossRef
go back to reference Bisiacchi PS, Mento G, Suppiej A (2009) Cortical auditory processing in preterm newborns: an ERP study. Biol Psychol 82:176–185CrossRef Bisiacchi PS, Mento G, Suppiej A (2009) Cortical auditory processing in preterm newborns: an ERP study. Biol Psychol 82:176–185CrossRef
go back to reference Brody B, Kinney H, Kloman A, Gilles F (1987) Sequence of central nervous system myelination in human infancy. I. an autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301CrossRef Brody B, Kinney H, Kloman A, Gilles F (1987) Sequence of central nervous system myelination in human infancy. I. an autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301CrossRef
go back to reference Cheour M et al (2002) Electric brain responses obtained from newborn infants to changes in duration in complex harmonic tones. Dev Neuropsychol 22:471–479CrossRef Cheour M et al (2002) Electric brain responses obtained from newborn infants to changes in duration in complex harmonic tones. Dev Neuropsychol 22:471–479CrossRef
go back to reference Cheour-Luhtanen M et al (1996) The ontogenetically earliest discriminative response of the human brain. Psychophysiology 33:478–481CrossRef Cheour-Luhtanen M et al (1996) The ontogenetically earliest discriminative response of the human brain. Psychophysiology 33:478–481CrossRef
go back to reference Copriviza KL, Lima CG (1984) Auditory arousal in preterm infants. NSSLHA 11:3–9CrossRef Copriviza KL, Lima CG (1984) Auditory arousal in preterm infants. NSSLHA 11:3–9CrossRef
go back to reference Daneshvarfard F et al (2019) Neurodevelopment and asymmetry of auditory-related responses to repetitive syllabic stimuli in preterm neonates based on frequency-domain analysis. Sci Rep 9:10654CrossRef Daneshvarfard F et al (2019) Neurodevelopment and asymmetry of auditory-related responses to repetitive syllabic stimuli in preterm neonates based on frequency-domain analysis. Sci Rep 9:10654CrossRef
go back to reference Dockstader C, Gaetz W, Rockel C, Mabbott DJ (2012) White matter maturation in visual and motor areas predicts the latency of visual activation in children. Hum Brain Mapp 33:179–191CrossRef Dockstader C, Gaetz W, Rockel C, Mabbott DJ (2012) White matter maturation in visual and motor areas predicts the latency of visual activation in children. Hum Brain Mapp 33:179–191CrossRef
go back to reference Draganova R et al (2007) Serial magnetoencephalographic study of fetal and newborn auditory discriminative evoked responses. Early Hum Dev 83:199–207CrossRef Draganova R et al (2007) Serial magnetoencephalographic study of fetal and newborn auditory discriminative evoked responses. Early Hum Dev 83:199–207CrossRef
go back to reference Dubois J et al (2016) MRI and M/EEG studies of the white matter development in human fetuses and infants : review and opinion. Brain Plast 2:49–69CrossRef Dubois J et al (2016) MRI and M/EEG studies of the white matter development in human fetuses and infants : review and opinion. Brain Plast 2:49–69CrossRef
go back to reference Dubois J et al (2008) Microstructural correlates of infant functional development: example of the visual pathways. J Neuros 28:1943–1948CrossRef Dubois J et al (2008) Microstructural correlates of infant functional development: example of the visual pathways. J Neuros 28:1943–1948CrossRef
go back to reference Glasser MF, Van Essen DC (2011) Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI. J Neurosci 31:11597–11616CrossRef Glasser MF, Van Essen DC (2011) Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI. J Neurosci 31:11597–11616CrossRef
go back to reference Graziani LJ, Katz L, Weitzman ED (1974) The Maturation and interrelationship of EEG patterns and auditory evoked responses in premature infants. Electroencephalogr Clin Neurophysiol 36:367–375CrossRef Graziani LJ, Katz L, Weitzman ED (1974) The Maturation and interrelationship of EEG patterns and auditory evoked responses in premature infants. Electroencephalogr Clin Neurophysiol 36:367–375CrossRef
go back to reference Grydeland H et al (2013) Intracortical myelin links with performance variability across the human lifespan: results from T1- and T2- weighted MRI myelin mapping and diffusion tensor imaging. J Neurosci 33:18618–18630CrossRef Grydeland H et al (2013) Intracortical myelin links with performance variability across the human lifespan: results from T1- and T2- weighted MRI myelin mapping and diffusion tensor imaging. J Neurosci 33:18618–18630CrossRef
go back to reference Holst M (2005) Development of auditory evoked fields in human fetuses and newborns: a longitudinal MEG study. Clin Neurophysiol 116:1949–1955CrossRef Holst M (2005) Development of auditory evoked fields in human fetuses and newborns: a longitudinal MEG study. Clin Neurophysiol 116:1949–1955CrossRef
go back to reference Iwatani J et al (2015) Use of T1-weighted / T2-weighted magnetic resonance ratio images to elucidate changes in the schizophrenic brain. Brain Behav 5:1–14CrossRef Iwatani J et al (2015) Use of T1-weighted / T2-weighted magnetic resonance ratio images to elucidate changes in the schizophrenic brain. Brain Behav 5:1–14CrossRef
go back to reference Kinney HC, Brody BA, Kloman AS, Gilles FH (1988) Sequence of central nervous system myelination in human infancy II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47:217–234CrossRef Kinney HC, Brody BA, Kloman AS, Gilles FH (1988) Sequence of central nervous system myelination in human infancy II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47:217–234CrossRef
go back to reference Van der Knaap MS, Valk J (1995a) Myelin and white matter. In: Valk J (ed) Magnetic resonance of myelin, myelination and myelin disorders. Springer- Verlag, BerlinCrossRef Van der Knaap MS, Valk J (1995a) Myelin and white matter. In: Valk J (ed) Magnetic resonance of myelin, myelination and myelin disorders. Springer- Verlag, BerlinCrossRef
go back to reference Van der Knaap MS, Valk J (1995b) Myelination and retarded myelination. In: Valk J (ed) Magnetic resonance of myelin, myelination and myelin disorders. Springer- Verlag, BerlinCrossRef Van der Knaap MS, Valk J (1995b) Myelination and retarded myelination. In: Valk J (ed) Magnetic resonance of myelin, myelination and myelin disorders. Springer- Verlag, BerlinCrossRef
go back to reference Kushnerenko E et al (2001) Central auditory processing of durational changes in complex speech patterns by newborns: an eventrelated brain potential study. Dev Neuropsychol 19:83–97CrossRef Kushnerenko E et al (2001) Central auditory processing of durational changes in complex speech patterns by newborns: an eventrelated brain potential study. Dev Neuropsychol 19:83–97CrossRef
go back to reference Lee K et al (2015) Early postnatal myelin content estimate of white matter via T1w/T2w ratio. Proc SPIE Int Soc Opt Eng 9417:1–7 Lee K et al (2015) Early postnatal myelin content estimate of white matter via T1w/T2w ratio. Proc SPIE Int Soc Opt Eng 9417:1–7
go back to reference Long P, Wan G, Roberts MT, Corfas G (2018) Myelin development, plasticity, and pathology in the auditory system. Dev Neurobiol 78:80–92CrossRef Long P, Wan G, Roberts MT, Corfas G (2018) Myelin development, plasticity, and pathology in the auditory system. Dev Neurobiol 78:80–92CrossRef
go back to reference Mahmoudzadeh M et al (2013) Syllabic discrimination in premature human infants prior to complete formation of cortical layers. PNAS 110:4846–4851CrossRef Mahmoudzadeh M et al (2013) Syllabic discrimination in premature human infants prior to complete formation of cortical layers. PNAS 110:4846–4851CrossRef
go back to reference Mahmoudzadeh M et al (2017) Functional maps at the onset of auditory inputs in very early preterm human neonates. Cereb Cortex 27:2500–2512PubMed Mahmoudzadeh M et al (2017) Functional maps at the onset of auditory inputs in very early preterm human neonates. Cereb Cortex 27:2500–2512PubMed
go back to reference Makropoulos A et al (2014) Automatic whole brain MRI segmentation of the developing neonatal brain. IEEE T Med Imag 33:1818–1831CrossRef Makropoulos A et al (2014) Automatic whole brain MRI segmentation of the developing neonatal brain. IEEE T Med Imag 33:1818–1831CrossRef
go back to reference Novitski N et al (2007) Neonatal frequency discrimination in 250–4000 Hz range: electrophysiological evidence. Clin Neurophysiol 118:412–419CrossRef Novitski N et al (2007) Neonatal frequency discrimination in 250–4000 Hz range: electrophysiological evidence. Clin Neurophysiol 118:412–419CrossRef
go back to reference Price D et al (2017) Age-related delay in visual and auditory evoked responses is mediated by white- and grey-matter differences. Nat Commun 8:15671CrossRef Price D et al (2017) Age-related delay in visual and auditory evoked responses is mediated by white- and grey-matter differences. Nat Commun 8:15671CrossRef
go back to reference Roberts TP et al (2009) Developmental correlation of diffusion anisotropy with auditory-evoked response. NeuroReport 20:1586–1591CrossRef Roberts TP et al (2009) Developmental correlation of diffusion anisotropy with auditory-evoked response. NeuroReport 20:1586–1591CrossRef
go back to reference Rotteveel JJ et al (1987) The maturation of the central auditory conduction in preterm infants until 3 months post term. V. The auditory cortical response (ACR). Hear Res 27:95–110CrossRef Rotteveel JJ et al (1987) The maturation of the central auditory conduction in preterm infants until 3 months post term. V. The auditory cortical response (ACR). Hear Res 27:95–110CrossRef
go back to reference Salvan P et al (2017) Language ability in preterm children is associated with arcuate fasciculi microstructure at term. Hum Brain Mapp 38:3836–3847CrossRef Salvan P et al (2017) Language ability in preterm children is associated with arcuate fasciculi microstructure at term. Hum Brain Mapp 38:3836–3847CrossRef
go back to reference Skrandies W (1990) Global field power and topographic similarity. Brain Topogr 3:137–141CrossRef Skrandies W (1990) Global field power and topographic similarity. Brain Topogr 3:137–141CrossRef
go back to reference Stufflebeam SM et al (2008) A non-invasive method to relate the timing of neural activity to white matter microstructural integrity. Neuroimage 42:710–716CrossRef Stufflebeam SM et al (2008) A non-invasive method to relate the timing of neural activity to white matter microstructural integrity. Neuroimage 42:710–716CrossRef
go back to reference Weitzman WD, Graziani LJ (1968) Maturation and topography of the auditory evoked response of the prematurely born infant. Psychobiol 1:79–89CrossRef Weitzman WD, Graziani LJ (1968) Maturation and topography of the auditory evoked response of the prematurely born infant. Psychobiol 1:79–89CrossRef
go back to reference Yakovlev PI, Lecours AR (1967) The myelogenetic cycles of regional maturation in the brain. In: Minowski A (ed) Regional development of the brain in early life. Blackwell, Oxford, pp 3–69 Yakovlev PI, Lecours AR (1967) The myelogenetic cycles of regional maturation in the brain. In: Minowski A (ed) Regional development of the brain in early life. Blackwell, Oxford, pp 3–69
Metadata
Title
Functional and structural correlates of the preterm infant’s brain: relating developmental changes of auditory evoked responses to structural maturation
Authors
Farveh Daneshvarfard
Hamid Abrishami Moghaddam
Guy Kongolo
Fabrice Wallois
Mahdi Mahmoudzadeh
Publication date
01-09-2020
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 7/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02117-3

Other articles of this Issue 7/2020

Brain Structure and Function 7/2020 Go to the issue