In recent years, a variety of segmentation methods have been proposed for automatic delineation of the fetal and neonatal brain MRI. These methods aim to define regions of interest of different ...granularity: brain, tissue types or more localised structures. Different methodologies have been applied for this segmentation task and can be classified into unsupervised, parametric, classification, atlas fusion and deformable models. Brain atlases are commonly utilised as training data in the segmentation process. Challenges relating to the image acquisition, the rapid brain development as well as the limited availability of imaging data however hinder this segmentation task. In this paper, we review methods adopted for the perinatal brain and categorise them according to the target population, structures segmented and methodology. We outline different methods proposed in the literature and discuss their major contributions. Different approaches for the evaluation of the segmentation accuracy and benchmarks used for the segmentation quality are presented. We conclude this review with a discussion on shortcomings in the perinatal domain and possible future directions.
•We present a comprehensive review of perinatal brain MRI segmentation methods.•A detailed classification of techniques is proposed based on methodology.•We outline existing atlases for the fetal and neonatal brain.•We discuss future directions and open challenges for research.
In recent years, exploration of the developing brain has become a major focus for researchers and clinicians in an attempt to understand what allows children to acquire amazing and unique abilities, ...as well as the impact of early disruptions (eg, prematurity, neonatal insults) that can lead to a wide range of neurodevelopmental disorders. Noninvasive neuroimaging methods such as MRI are essential to establish links between the brain and behavioral changes in newborns and infants. In this review article, we aim to highlight recent and representative studies using the various techniques available: anatomical MRI, quantitative MRI (relaxometry, diffusion MRI), multiparametric approaches, and functional MRI. Today, protocols use 1.5 or 3T MRI scanners, and specialized methodologies have been put in place for data acquisition and processing to address the methodological challenges specific to this population, such as sensitivity to motion. MR sequences must be adapted to the brains of newborns and infants to obtain relevant good soft‐tissue contrast, given the small size of the cerebral structures and the incomplete maturation of tissues. The use of age‐specific image postprocessing tools is also essential, as signal and contrast differ from the adult brain. Appropriate methodologies then make it possible to explore multiple neurodevelopmental mechanisms in a precise way, and assess changes with age or differences between groups of subjects, particularly through large‐scale projects. Although MRI measurements only indirectly reflect the complex series of dynamic processes observed throughout development at the molecular and cellular levels, this technique can provide information on brain morphology, structural connectivity, microstructural properties of gray and white matter, and on the functional architecture. Finally, MRI measures related to clinical, behavioral, and electrophysiological markers have a key role to play from a diagnostic and prognostic perspective in the implementation of early interventions to avoid long‐term disabilities in children.
Evidence Level
2
Technical Efficacy Stage
1
Rich-club organization of the newborn human brain Ball, Gareth; Aljabar, Paul; Zebari, Sally ...
Proceedings of the National Academy of Sciences - PNAS,
05/2014, Letnik:
111, Številka:
20
Journal Article
Recenzirano
Odprti dostop
Combining diffusion magnetic resonance imaging and network analysis in the adult human brain has identified a set of highly connected cortical hubs that form a “rich club”—a high-cost, high-capacity ...backbone thought to enable efficient network communication. Rich-club architecture appears to be a persistent feature of the mature mammalian brain, but it is not known when this structure emerges during human development. In this longitudinal study we chart the emergence of structural organization in mid to late gestation. We demonstrate that a rich club of interconnected cortical hubs is already present by 30 wk gestation. Subsequently, until the time of normal birth, the principal development is a proliferation of connections between core hubs and the rest of the brain. We also consider the impact of environmental factors on early network development, and compare term-born neonates to preterm infants at term-equivalent age. Though rich-club organization remains intact following premature birth, we reveal significant disruptions in both in cortical–subcortical connectivity and short-distance corticocortical connections. Rich club organization is present well before the normal time of birth and may provide the fundamental structural architecture for the subsequent emergence of complex neurological functions. Premature exposure to the extrauterine environment is associated with altered network architecture and reduced network capacity, which may in part account for the high prevalence of cognitive problems in preterm infants.
Medical imaging has shown that, during early development, the brain undergoes more changes in size, shape and appearance than at any other time in life. A better understanding of brain development ...requires a spatio-temporal atlas that characterizes the dynamic changes during this period. In this paper we present an approach for constructing a 4D atlas of the developing brain, between 28 and 44weeks post-menstrual age at time of scan, using T1 and T2 weighted MR images from 204 premature neonates. The method used for the creation of the average 4D atlas utilizes non-rigid registration between all pairs of images to eliminate bias in the atlas toward any of the original images. In addition, kernel regression is used to produce age-dependent anatomical templates. A novelty in our approach is the use of a time-varying kernel width, to overcome the variations in the distribution of subjects at different ages. This leads to an atlas that retains a consistent level of detail at every time-point. Comparisons between the resulting atlas and atlases constructed using affine and non-rigid registration are presented. The resulting 4D atlas has greater anatomic definition than currently available 4D atlases created using various affine and non-rigid registration approaches, an important factor in improving registrations between the atlas and individual subjects. Also, the resulting 4D atlas can serve as a good representative of the population of interest as it reflects both global and local changes. The atlas is publicly available at www.brain-development.org.
► A new approach for constructing high-definition 4D atlases is presented. ► Multi-modal MR images from 204 preterm neonates (age-range 26–44weeks PMA) are used. ► The resulting atlas retains a consistent level of detail at every time-point. ► The atlas has greater anatomic definition than currently available 4D atlases. ► Such a sharp atlas enables improved registration between the atlas and individuals.
Detailed morphometric analysis of the neonatal brain is required to characterise brain development and define neuroimaging biomarkers related to impaired brain growth. Accurate automatic segmentation ...of neonatal brain MRI is a prerequisite to analyse large datasets. We have previously presented an accurate and robust automatic segmentation technique for parcellating the neonatal brain into multiple cortical and subcortical regions. In this study, we further extend our segmentation method to detect cortical sulci and provide a detailed delineation of the cortical ribbon. These detailed segmentations are used to build a 4-dimensional spatio-temporal structural atlas of the brain for 82 cortical and subcortical structures throughout this developmental period. We employ the algorithm to segment an extensive database of 420 MR images of the developing brain, from 27 to 45weeks post-menstrual age at imaging. Regional volumetric and cortical surface measurements are derived and used to investigate brain growth and development during this critical period and to assess the impact of immaturity at birth. Whole brain volume, the absolute volume of all structures studied, cortical curvature and cortical surface area increased with increasing age at scan. Relative volumes of cortical grey matter, cerebellum and cerebrospinal fluid increased with age at scan, while relative volumes of white matter, ventricles, brainstem and basal ganglia and thalami decreased. Preterm infants at term had smaller whole brain volumes, reduced regional white matter and cortical and subcortical grey matter volumes, and reduced cortical surface area compared with term born controls, while ventricular volume was greater in the preterm group. Increasing prematurity at birth was associated with a reduction in total and regional white matter, cortical and subcortical grey matter volume, an increase in ventricular volume, and reduced cortical surface area.
•A novel methodology is proposed for delineating the cortical ribbon.•Regional brain growth is assessed in the developing preterm brain.•We investigate the effect of prematurity on brain growth and cortical development.•A spatio-temporal neonatal atlas is constructed with 82 brain structures.
Thalamocortical connections are: essential for brain function, established early in development, and significantly impaired following preterm birth. Impaired cognitive abilities in preterm infants ...may be related to disruptions in thalamocortical connectivity. The aim of this study was to test the hypothesis: thalamocortical connectivity in the preterm brain at term-equivalent is correlated with cognitive performance in early childhood. We examined 57 infants who were born <35 weeks gestational age (GA) and had no evidence of focal abnormality on magnetic resonance imaging (MRI). Infants underwent diffusion MRI at term and cognitive performance at 2 years was assessed using the Bayley III scales of Infant and Toddler development. Cognitive scores at 2 years were correlated with structural connectivity between the thalamus and extensive cortical regions at term. Mean thalamocortical connectivity across the whole cortex explained 11% of the variance in cognitive scores at 2 years. The inclusion of GA at birth and parental socioeconomic group in the model explained 30% of the variance in subsequent cognitive performance. Identifying impairments in thalamocortical connectivity as early as term equivalent can help identify those infants at risk of subsequent cognitive delay and may be useful to assess efficacy of potential treatments at an early age.
Cortical maturation was studied in 65 infants between 27 and 46 wk postconception using structural and diffusion magnetic resonance imaging. Alterations in neural structure and complexity were ...inferred from changes in mean diffusivity and fractional anisotropy, analyzed by sampling regions of interest and also by a unique whole-cortex mapping approach. Mean diffusivity was higher in gyri than sulci and in frontal compared with occipital lobes, decreasing consistently throughout the study period. Fractional anisotropy declined until 38 wk, with initial values and rates of change higher in gyri, frontal and temporal poles, and parietal cortex; and lower in sulcal, perirolandic, and medial occipital cortex. Neuroanatomical studies and experimental diffusion–anatomic correlations strongly suggested the interpretation that cellular and synaptic complexity and density increased steadily throughout the period, whereas elongation and branching of dendrites orthogonal to cortical columns was later and faster in higher-order association cortex, proceeding rapidly before becoming undetectable after 38 wk. The rate of microstructural maturation correlated locally with cortical growth, and predicted higher neurodevelopmental test scores at 2 y of age. Cortical microstructural development was reduced in a dose-dependent fashion by longer premature exposure to the extrauterine environment, and preterm infants at term-corrected age possessed less mature cortex than term-born infants. The results are compatible with predictions of the tension theory of cortical growth and show that rapidly developing cortical microstructure is vulnerable to the effects of premature birth, suggesting a mechanism for the adverse effects of preterm delivery on cognitive function.
Early human brain development constitutes a sequence of intricate processes resulting in the ontogeny of functionally operative neural circuits. Developmental trajectories of early brain network ...formation are genetically programmed and can be modified by epigenetic and environmental influences. Such alterations may exert profound effects on neurodevelopment, potentially persisting throughout the lifespan. This review focuses on the critical period of fetal and early postnatal brain development. Here we collate findings from neuroimaging studies, with a particular focus on functional MRI research that interrogated early brain network development in both health and high-risk or disease states. First, we will provide an overview of the developmental processes that take place from the embryonic period through early infancy in order to contextualize brain network formation. Second, functional brain network development in the typically developing brain will be discussed. Third, we will touch on prenatal and perinatal risk factors that may interfere with the trajectories of functional brain wiring, including prenatal substance exposure, maternal mental illness and preterm birth. Collectively, studies have revealed the blueprint of adult human brain organization to be present in the neonatal brain. Distinct attributes of human brain architecture have even been detected in the developing fetal brain from as early as 24 postconceptional weeks. During postnatal brain development, the brain's wiring pattern is further sculpted and modulated to become the full facsimile of the adult human brain, with functional brain network refinement being more rigorous than structural brain network maturation. Advances in neuroimaging techniques have paved the way towards a comprehensive understanding of the maturational pathways of brain network development and of how early developmental adversity may affect these trajectories. Such insights are fundamental for our understanding of human brain functioning, for early identification of infants at risk, as well as for future neuroprotective strategies.
•Interhemispheric functional coupling has been noted in the fetal brain from 24 PCW.•The overall framework of mature brain wiring is established by the time of birth.•Development of functional architecture follows a primary-to-higher order sequence.•Prematurity disrupts long-range connectivity of primarily thalamocortical pathways.•Prenatal substance exposure affects receptor regions and amygdala-frontal circuits.
Traumatic brain injury often results in cognitive impairments that limit recovery. The underlying pathophysiology of these impairments is uncertain, which restricts clinical assessment and ...management. Here, we use magnetic resonance imaging to test the hypotheses that: (i) traumatic brain injury results in abnormalities of functional connectivity within key cognitive networks; (ii) these changes are correlated with cognitive performance; and (iii) functional connectivity within these networks is influenced by underlying changes in structural connectivity produced by diffuse axonal injury. We studied 20 patients in the chronic phase after traumatic brain injury compared with age-matched controls. Network function was investigated in detail using functional magnetic resonance imaging to analyse both regional brain activation, and the interaction of brain regions within a network (functional connectivity). We studied patients during performance of a simple choice-reaction task and at 'rest'. Since functional connectivity reflects underlying structural connectivity, diffusion tensor imaging was used to quantify axonal injury, and test whether structural damage correlated with functional change. The patient group showed typical impairments in information processing and attention, when compared with age-matched controls. Patients were able to perform the task accurately, but showed slow and variable responses. Brain regions activated by the task were similar between the groups, but patients showed greater deactivation within the default mode network, in keeping with an increased cognitive load. A multivariate analysis of 'resting' state functional magnetic resonance imaging was then used to investigate whether changes in network function were present in the absence of explicit task performance. Overall, default mode network functional connectivity was increased in the patient group. Patients with the highest functional connectivity had the least cognitive impairment. In addition, functional connectivity at rest also predicted patterns of brain activation during later performance of the task. As expected, patients showed widespread white matter damage compared with controls. Lower default mode network functional connectivity was seen in those patients with more evidence of diffuse axonal injury within the adjacent corpus callosum. Taken together, our results demonstrate altered patterns of functional connectivity in cognitive networks following injury. The results support a direct relationship between white matter organization within the brain's structural core, functional connectivity within the default mode network and cognitive function following brain injury. They can be explained by two related changes: a compensatory increase in functional connectivity within the default mode network; and a variable degree of structural disconnection that modulates this change in network function.
Human cortical development during the third trimester is characterised by macro- and microstructural changes which are reflected in alterations in diffusion MRI (dMRI) measures, with significant ...decreases in cortical mean diffusivity (MD) and fractional anisotropy (FA). This has been interpreted as reflecting increased cellular density and dendritic arborisation. However, the fall in FA stops abruptly at 38 weeks post-menstrual age (PMA), and then tends to plateau, while MD continues to fall, suggesting a more complex picture and raising the hypothesis that after this age development is dominated by continuing increase in neural and organelle density rather than alterations in the geometry of dendritic trees. To test this, we used neurite orientation dispersion and density imaging (NODDI), acquiring multi-shell, high angular resolution dMRI and measures of cortical volume and mean curvature in 99 preterm infants scanned between 25 and 47 weeks PMA. We predicted that increased neurite and organelle density would be reflected in increases in neurite density index (NDI), while a relatively unchanging geometrical structure would be associated with constant orientation dispersion index (ODI). As dendritic arborisation is likely to be one of the drivers of gyrification, we also predicted that measures of cortical volume and curvature would correlate with ODI and show slower growth after 38 weeks.
We observed a decrease of MD throughout the period, while cortical FA decreased from 25 to 38 weeks PMA and then increased. ODI increased up to 38 weeks and then plateaued, while NDI rose after 38 weeks. The evolution of ODI correlated with cortical volume and curvature. Regional analysis of cortical microstructure revealed a heterogenous pattern with increases in FA and NDI after 38 weeks confined to primary motor and sensory regions. These results support the interpretation that cortical development between 25 and 38 weeks PMA shows a predominant increase in dendritic arborisation and neurite growth, while between 38 and 47 weeks PMA it is dominated by increasing cellular and organelle density.
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•DTI and NODDI cortical measures between 25 and 47 weeks GA•Early cortical changes consistent with dendritic arborisation and neurite growth•After 38 weeks cortical changes consistent with increasing cellular density•Cortical curvature evolves in parallel with dendritic arborisation
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