Structural basis of the developmental plasticity in the human cerebral cortex: The role of the transient subplate zone

Kostović, Ivica; Lukinović, Nikola; Judaš, Miloš; Bogdanović, Nenad; Mrzljak, Ladislav; Zečević, Nada; Kubat, Milovan

doi:10.1007/bf00999489

Cited by 82 publications

(45 citation statements)

References 16 publications

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“…Similar disruption of axonal outgrowth of the pyramidal neurons has been observed in Golgi-stained neuropathological samples from infants who have survived the preterm period (30). A significant complication of WM damage is the localized disruption of axon fibers resulting in the loss of inputs and outputs to and from the overlying areas of gray mater (31). The clinical correlate of even a minimal amount of such WM injury could be cerebral palsy, dyslexia, epilepsy, audiovisual deficits, and learning deficits.…”

Section: Discussionmentioning

confidence: 73%

Selective Cortical Alteration after Hypoxic-Ischemic Injury in the Very Immature Rat Brain

et al. 2003

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Distinctive cerebral lesions with disruptions to the developing white matter are found in very low birth weight (VLBW) infants. Although hypoxia-ischemia (HI) is a causal pathway, the pathogenesis of cerebral white matter injury in the VLBW infant is not fully understood. Pertinent murine models would facilitate the investigation of the processes leading to these cerebral lesions and enable the evaluation of therapeutic strategies. Postnatal d 3 (P3) rats are at a stage of cortical oligodendroglial maturation and axonal outgrowth similar to very preterm infants. Our aim was to characterize the effects of a focal hypoxic-ischemic injury at P3 on subsequent cerebral development. Three groups of P3 Wistar rats were investigated: group I underwent right carotid ligation followed by 6% hypoxia for 30 min (HI), group 2 had carotid ligation only, and group 3 had no intervention. At P21, in the HI group, the right cortical area was reduced compared with controls (p Ͻ 0.01). There were no significant alterations in the size of the dorsal hippocampus, striatum, and thalamus. The cortical myelinated area was reduced in the HI animals compared with controls (p Ͻ 0.01). There was a corresponding loss of myelinated axons extending up into the cortex, with deep cortical neuronal and axonal architecture markedly disrupted. Glial fibrillary acidic protein immunohistology showed a reactive gliosis in the deep parietal cortex (p Ͻ 0.01). Moderate HI injury in the immature rat brain compromised cortical growth and led to a selective alteration of cortical myelinated axons with persistent gliosis. These alterations induced at P3 by unilateral HI share neuropathological similarities with the diffuse white matter lesions found in VLBW infants. Of those infants born weighing Ͻ1500 g, 25-50% will later exhibit developmental disabilities and up to 5-15% will display a more major cerebral palsy (1, 2). The pattern of brain damage associated with prematurity is unique, with a specific loss of the developing cerebral WM (3), and differs markedly from the predominantly gray matter injuries that occur in the more mature CNS. The distinct cystic WM lesions termed PVL and a more subtle and diffuse lesion with loss of WM volume and ventriculomegaly (3, 4) feature with subsequent abnormal development of cortical gray matter and alterations in the central and distal WM microstructure (5-7). The etiology of these injuries in the premature infant is not fully understood (8), although HI injury, inflammation associated with cytotoxic cytokines, and an increased vulnerability of oligodendrocytes precursors to HI appear to be important (9, 10). Prevention of these adverse outcomes requires an understanding of the pathogenesis of the lesion and the subsequent alterations in brain development.It is difficult to precisely compare neural maturation between species. However, the cortex of the 12-to 14-d-old rat corresponds approximately to that of a term human newborn with myelination of the fiber tracts beginning on approximately d 11 in the rat. The 7-d-o...

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Section: Discussionmentioning

confidence: 73%

Selective Cortical Alteration after Hypoxic-Ischemic Injury in the Very Immature Rat Brain

et al. 2003

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“…5 In animal experiments, it has been shown that this transient fetal circuitry of the subplate zone is functional, 23,24 characterized by endogeneous spontaneous activity and involved in several activity-dependent events such as the formation of ocular dominance columns in the fetal visual cortex. 25,26 As the transient subplate zone is best developed in humans and at the peak of its development is four times thicker than the cortical plate 5 and contains well-differentiated neurons, 4,10,27 it probably has a substantial role in development of cortical circuitry and generation of cortical activity in brains of preterm infants. In addition, experimental data suggest that thalamocortical activity can modulate the early spontaneous activity of transient subplate circuitry.…”

Section: Comparison Of Mri and Histological Findingsmentioning

confidence: 99%

Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants

Kostović

Judaš

2006

Develop Med Child Neuro

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136

117

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The aim of this paper is to evaluate correlative magnetic resonance imaging (MRI) and histological parameters of development of cortical afferents during pathfinding and target selection in transient fetal cerebral laminas in human fetuses and preterm infants. The transient fetal subplate zone, situated between the fetal white matter (i.e. intermediate zone) and the cortical plate, is the crucial laminar compartment for development of thalamocortical and corticocortical afferents. The prolonged coexistence of transient (endogenously active) and permanent (sensorydriven) circuitry within the transient fetal zones is a salient feature of the fetal and preterm cortex; this transient circuitry is the substrate of cerebral functions in preterm infants. Another transient aspect of organization of developing fibre pathways is the abundance of extracellular matrix and guidance molecules in periventricular crossroads of projection and corticocortical pathways. Both the subplate zone and periventricular crossroads are visible on MRI in vivo and in vitro. Hypoxic-ischaemic lesions of periventricular crossroads are the substrate for motor, sensory, and cognitive deficits after focal periventricular leukomalacia (PVL). Lesions of distal portions of the white matter and the subplate zone are the substrate for diffuse PVL. The neuronal elements in transient fetal zones form a developmental potential for plasticity after perinatal cerebral lesions.Our understanding and interpretation of structural and functional consequences of cerebral lesions in human fetuses and preterm infants largely depends on knowledge of neurogenetic cellular events that can be demonstrated by in vivo neuroimaging. A necessary step in this approach is the correlation between magnetic resonance imaging (MRI) and histological organization during different phases of histogenesis. Namely, in the fetal cerebrum, early neurogenetic cellular events (i.e. proliferation, migration, aggregation, cell death, growth of axons, and the establishment of neuronal connections) proceed according to the specific timetable within transient, histologically recognizable fetal zones which do not have an equivalent in the adult brain. 1 During the last third of gestation, neuronal proliferation and migration are mostly completed 1 whereas the development of axonal pathways 2,3 and the differentiation of cortical neurons 4 become the most prominent neurogenetic events. Synaptogenesis continues as the dominant neurogenetic event during postnatal life. In addition to precise timing, these neurogenetic events also display a characteristic spatial occurrence: neuronal proliferation occurs in the ventricular and subventricular zones, whereas neuronal migration and growth of axons occur predominantly in the intermediate zone (the fetal white matter) and the subplate zone, which is situated between the intermediate zone and the cortical plate. 1 Neuronal differentiation and synaptogenesis begin in the transient subplate zone 5 and continue in the cortical plate. 1,5 Recent research in...

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“…Studies on the subplate neurons of the developing human cerebral cortex [63,64,71] have also provided information on the possible relationship between the subplate neurons and different kinds of periventricular lesions. The thickness of the subplate in the frontal lobe reaches a peak at around 22-34 weeks of gestation.…”

Section: The Subplate As a Waiting Compartmentmentioning

confidence: 99%

“…After a variable time period, these fibers enter the cortical plate and the subplate disappears, leaving cells scattered throughout the subcortical white matter [64,71], or the subplate neurons just die. The subplate neurons, which are present throughout the neocortex, reach a high degree of functional and morphological maturity early in life, making them uniquely susceptible to the effects of trophic factor deprivation or excitotoxicity.…”

Section: The Subplate As a Waiting Compartmentmentioning

confidence: 99%

Normal and Abnormal Development of the Human Cerebral Cortex

et al. 2002

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The functional organization of the developing human brain does not only differ substantially from that of the mature brain, but it also undergoes continuous changes. During fetal brain development, transient neuronal circuitries are formed which are essential for the subsequent development of mature projections. Transitory connections are linked to transient structures which are particularly prominent in the human fetal brain and are susceptible to damage under pathological circumstances. The First International Symposium on Normal and Abnormal Development of the Human Fetal Brain aimed to gather basic information on these transitory organizations and the major developmental events that occur in the fetal brain. This paper summarizes a roundtable discussion at the symposium on transient characteristics and injuries in the developing human cerebral cortex. An overview of cortical development is first presented and then the development of several fetal structures, including the subventricular zone, ganglionic eminence, marginal zone, subplate and cortical plate, is discussed with regard to their important contribution to the formation of the correct fiber projections in the adult. The last section focuses on the anomalies that are commonly found in the premature fetal brain on the one hand and on the other hand are related to the transitory characteristics of the developing brain.

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Structural basis of the developmental plasticity in the human cerebral cortex: The role of the transient subplate zone

Cited by 82 publications

References 16 publications

Selective Cortical Alteration after Hypoxic-Ischemic Injury in the Very Immature Rat Brain

Selective Cortical Alteration after Hypoxic-Ischemic Injury in the Very Immature Rat Brain

Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants

Normal and Abnormal Development of the Human Cerebral Cortex

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