Differential microstructural development within sensorimotor cortical regions: A diffusion MRI study in preterm and full-term infants

The sensorimotor system develops early in utero and supports the emergence of body representations critical for perception, action, and interaction with environment. While somatotopic protomaps are already developed in the primary somatosensory and motor cortices in late pregnancy, little is known about the anatomical substrates of this functional specialization. In this study, we aimed to decipher the microstructural properties of these regions in the developing brain. Using advanced diffusion MRI and post-processing tools, we parcellated the pre- and post-central gyri into microstructurally distinct clusters along the lateral-to-medial axis in 25 full-term neonates, confirming the early differentiation within sensorimotor regions. These clusters were further analyzed in 59 preterm infants scanned at term-equivalent age (TEA, PT<sub>TEA</sub>), of which 45 were also scanned near birth (PT<sub>Birth</sub>), and compared with another group of 59 full-term neonates. Applying a multivariate Mahalanobis distance approach, we quantified deviations in preterm cortical microstructure relative to the full-term reference. Preterm infants showed significant region- and position-specific deviations at both ages, though these were smaller at TEA (repeated-measures ANCOVA: PT<sub>Birth</sub>: region effect F=25.48, position effect F=16.06; PT<sub>TEA</sub>: region effect F=14.87, all p < 0.001), consistently with ongoing maturation during the pre-term period. Differences between the pre- and post-central gyri, and along the somatotopic axis, suggested differential vulnerability to prematurity. In particular, compared with somatosensory regions, the motor regions appeared to be at a more advanced stage of maturation close to birth (paired t-test, T = -4.388, p < 0.001) and less vulnerable at TEA (paired t-test, T = -4.169, p < 0.001), suggesting lesser impact of prematurity. An opposite pattern was observed, particularly close to birth, for lateral positions related to mouth representation compared with intermediary (paired t-test: T = 5.933, p < 0.001) and medial (paired t-test: T = 4.712, p < 0.001) positions. These findings support the notion that early sensorimotor cortical specialization is microstructurally emergent during gestation and sensitive to atypical developmental context of preterm birth.

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Journal
Developmental Cognitive Neuroscience
Published
2025-08-30
DOI
https://doi.org/10.1016/j.dcn.2025.101610
Primary Topic
Advanced Neuroimaging Techniques and Applications
Type
article
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article

Differential microstructural development within sensorimotor cortical regions: A diffusion MRI study in preterm and full-term infants

Yann Leprince, Andrea Gondová, Guillaume Auzias, Denis Rivière et al.
Developmental Cognitive Neuroscience
Advanced Neuroimaging Techniques and Applications
article

Differential microstructural development within sensorimotor cortical regions: A diffusion MRI study in preterm and full-term infants

Yann Leprince, Andrea Gondová, Guillaume Auzias, Denis Rivière, Jessica Dubois, Laurie Devisscher, Alexandra Brandstaetter
article en

Abstract

The sensorimotor system develops early in utero and supports the emergence of body representations critical for perception, action, and interaction with environment. While somatotopic protomaps are already developed in the primary somatosensory and motor cortices in late pregnancy, little is known about the anatomical substrates of this functional specialization. In this study, we aimed to decipher the microstructural properties of these regions in the developing brain. Using advanced diffusion MRI and post-processing tools, we parcellated the pre- and post-central gyri into microstructurally distinct clusters along the lateral-to-medial axis in 25 full-term neonates, confirming the early differentiation within sensorimotor regions. These clusters were further analyzed in 59 preterm infants scanned at term-equivalent age (TEA, PT<sub>TEA</sub>), of which 45 were also scanned near birth (PT<sub>Birth</sub>), and compared with another group of 59 full-term neonates. Applying a multivariate Mahalanobis distance approach, we quantified deviations in preterm cortical microstructure relative to the full-term reference. Preterm infants showed significant region- and position-specific deviations at both ages, though these were smaller at TEA (repeated-measures ANCOVA: PT<sub>Birth</sub>: region effect F=25.48, position effect F=16.06; PT<sub>TEA</sub>: region effect F=14.87, all p < 0.001), consistently with ongoing maturation during the pre-term period. Differences between the pre- and post-central gyri, and along the somatotopic axis, suggested differential vulnerability to prematurity. In particular, compared with somatosensory regions, the motor regions appeared to be at a more advanced stage of maturation close to birth (paired t-test, T = -4.388, p < 0.001) and less vulnerable at TEA (paired t-test, T = -4.169, p < 0.001), suggesting lesser impact of prematurity. An opposite pattern was observed, particularly close to birth, for lateral positions related to mouth representation compared with intermediary (paired t-test: T = 5.933, p < 0.001) and medial (paired t-test: T = 4.712, p < 0.001) positions. These findings support the notion that early sensorimotor cortical specialization is microstructurally emergent during gestation and sensitive to atypical developmental context of preterm birth.

Developmental Cognitive NeuroscienceVol. 75
Boston Children's Hospital (US), Centre National de la Recherche Scientifique (FR), Inserm (FR), Université Paris Cité (FR), Aix-Marseille Université (FR), Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR), Université Paris-Saclay (FR), University of Massachusetts Boston (US), Hôpital Robert-Debré (FR), CEA Paris-Saclay (FR), Institut de Neurosciences de la Timone (FR), Cognitive Neuroimaging Lab (FR), NeuroDiderot (FR)
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Advanced Neuroimaging Techniques and Applications
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