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Phylogeny and ontogeny of the CNS. a Phylogenetic relationships among main deuterostome clades, as cited in the text. b Ontogeny of the CNS, including the brain, in vertebrates. The origin of the different elements of the CSF system has been indicated. Similarities between deuterostome clades and CNS development in vertebrates have also been indicated. 1 Adult starfish possess a neural plate-like nervous system similar to one from early vertebrate embryos, before the formation of the neural tube; 2 Adult Hemichordata possess a hollow dorsal nerve chord similar to one from vertebrate embryos before the closure of the anterior neuropore; 3 Urochordata and cephalochordata larvae possess a hollow dorsal nerve chord anteriorly open similar to one from vertebrate embryos before the closure of the anterior neuropore; 4 Urochordata and cephalochordata adults possess a closed dorsal nerve chord similar to one from vertebrate embryos after the closure of the anterior neuropore; 5 In vertebrates, the neural tube becomes a physiologically sealed system from a very early developmental stage and the site of the embryonic transfer system is depicted
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Within the consolidated field of evolutionary development, there is emerging research on evolutionary aspects of central nervous system development and its implications for adult brain structure and function, including behaviour. The central nervous system is one of the most intriguing systems in complex metazoans, as it controls all body and mind...
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Citations
... Article https://doi.org/10.1038/s41467-023-36083-1 movement of CSF represents a key mechanism by which nutrients and growth factors reach the hippocampus and SVZ 30,31,[68][69][70] . This interpretation is consistent with prior studies that show growth factors, neurotransmitters, and other molecules pertinent in various signaling pathways cross the ventricle wall to interact with type A, B2, and C cells in the SVZ 30,69,70 . ...
... movement of CSF represents a key mechanism by which nutrients and growth factors reach the hippocampus and SVZ 30,31,[68][69][70] . This interpretation is consistent with prior studies that show growth factors, neurotransmitters, and other molecules pertinent in various signaling pathways cross the ventricle wall to interact with type A, B2, and C cells in the SVZ 30,69,70 . Changes in CSF composition and circulation dynamics in the setting of IVH-PHH may disrupt the interaction of these cells with transependymally and transventricularly transported molecules critical for development, with implications for ventricular zone disruption, neural stem cell loss, and eventual neurodevelopmental outcomes. ...
Cerebrospinal fluid (CSF) is essential for the development and function of the central nervous system (CNS). However, the brain and its interstitium have largely been thought of as a single entity through which CSF circulates, and it is not known whether specific cell populations within the CNS preferentially interact with the CSF. Here, we develop a technique for CSF tracking, gold nanoparticle-enhanced X-ray microtomography, to achieve micrometer-scale resolution visualization of CSF circulation patterns during development. Using this method and subsequent histological analysis in rodents, we identify previously uncharacterized CSF pathways from the subarachnoid space (particularly the basal cisterns) that mediate CSF-parenchymal interactions involving 24 functional-anatomic cell groupings in the brain and spinal cord. CSF distribution to these areas is largely restricted to early development and is altered in posthemorrhagic hydrocephalus. Our study also presents particle size-dependent CSF circulation patterns through the CNS including interaction between neurons and small CSF tracers, but not large CSF tracers. These findings have implications for understanding the biological basis of normal brain development and the pathogenesis of a broad range of disease states, including hydrocephalus. Cerebrospinal fluid (CSF) is essential for brain development. Here, the authors use gold nanoparticle enhanced X-ray microtomography to map CSF distribution in post-natal rodents and describe particle size-dependent CSF pathways that transport CSF into the brain parenchyma of rodents.
... Unfortunately, only a little is known on the micro-anatomical distribution and spatial organization of the different neuronal populations and their patterns of differentiation that form the encephalic vesicles and different synaptic layers of the developing chick brains. A slightly clear and enlightened picture of developing brain anatomy was put forward in 2016 [37]. ...
Comparative developing brain histo-anatomical pathologies of Fluoride ions and Bifenthrin in-ovo exposures were explored in the golden black variety of domestic chick. Three exposure groups were –the Vehicle control group (Vg); Fluoride (F) group and the Bifenthrin (Bn) group each with forty fertilized eggs and received their respective group treatment at zero day of incubation. Embryos were extracted, dissected from head region and the embryonic whole brains were recovered after 14 days of incubation. The embryonic brains were preserved in bouin fixative for 24 h for further studies. The morphological results show the atrophied and hypertrophied embryonic brain in F and Bn groups respectively as compared to Vg group. The toxicological signs of encephalic anatomy and histology of F and Bn exposure were the enlarged third ventricles, optocoeles and arachnoid mater, encephalic spongiosis and decreased neuroglial density. The morphometric data showed significant decrease (p ≤ 0.05) in mean weight and density of whole brain in F and Bn groups compared Vg. The mean length and width of whole brain in F were significantly lower than that of the Bn and Vg. whereas, the mean breadth of third ventricle in Bn remained significantly lower than F and Vg groups. On the other hand, the mean breadth of optocoele and fourth ventricle in F and Bn groups remained significantly higher than Vg. Conversely the mean optic lobe wall thickness in F remained significantly lower than Bn and Vg. Additionally, the mean neuronal density in diencephalon, optic lobe and cerebellum in F group and Bn group remained significantly (p ≤ 0.05) lower than Vg. Results show that low dose in-ovo fluoride or bifenthrin exposure may cause neuro-developmental abnormalities in the developing chick embryos indicating that the Fluoride-ions and Bifenthrin harbor strong developmental neurotoxic capacity.
... Hydrodynamic fluid properties and the composition of CSF components are thought to contribute to normal 164), and a closed neural tube is essential for normal development (15, 165). The cellular lining of the neural tube is a specialized epithelium, the "neuroepithelium," which comprises the pool of stem cells that will generate the vast majority of CNS cells (166,167). ...
Studies of the choroid plexuses lag behind those of, the more widely known, blood brain barrier in spite of a much longer history. This review has two overall aims. The first is to outline longstanding areas of research where there are unanswered questions, such as control of cerebrospinal fluid (CSF) secretion and blood flow. The second part reviews research over the past ten years where the focus has shifted to the idea that the choroid plexuses make specific contributions to brain development and function through molecules they generate and circulate throughout the CSF; these appear to be particularly important for aspects of normal brain growth. Most research in the 20 th Century dealt with the choroid plexuses as one of the brain barrier interfaces that make an important contribution to the composition and stability of the internal environment of the brain in the adult and during its development. More recent research has shown the importance of choroid plexus generated CSF in neurogenesis, influence of sex and other hormones on plexus function, and their role in circadian rhythms and sleep. Of clinical importance are attempts to develop methods to deliver brain-specific drugs via the CSF and understanding the implications of drug entry into developing brain when administered to pregnant women.
... Many of these developmentally important growth factors, such as FGF2, may derive from the embryonic environment prior to closure of the anterior neuropore. 7 The choroid plexus epithelium also secretes IGF-II, with continued secretion of factors such as EGF, FGF-2 and retinoic acid in adults, which are important for neurogenesis in the subventricular zone. 8 Aside from the role of CSF in normal brain development, it is also speculated to act as a cushioning system and buoyant force which reduces the overall weight of the brain from 1500 to 25À50 g. 9 This theory has been used to partially explain the appearance of an external CSF compartment in terrestrial animals as more cushioning of the brain was required in the transition from a liquid to gaseous environment. ...
Congenital hydrocephalus occurs in one in 500–1000 babies born in the United States and acquired hydrocephalus may occur as the consequence of stroke, intraventricular and subarachnoid hemorrhage, traumatic brain injuries, brain tumors, craniectomy or may be idiopathic, as in the case of normal pressure hydrocephalus. Irrespective of its prevalence and significant impact on quality of life, neurosurgeons still rely on invasive cerebrospinal fluid shunt systems for the treatment of hydrocephalus that are exceptionally prone to failure and/or infection. Further understanding of this process at a molecular level, therefore, may have profound implications for improving treatment and quality of life for millions of individuals worldwide. The purpose of this article is to review the current research landscape on hydrocephalus with a focus on recent advances in our understanding of cerebrospinal fluid pathways from an evolutionary, genetics and molecular perspective.
... The disruption of the BCSFB is another pathology that might contribute to the electrolyte, total protein, and osmolality changes [33,59,87,88]. Of note, CSF osmolality and the concentrations of many electrolytes exceed serum levels in PHH. ...
... Finally, maintaining a normal CSF biochemical profile is essential for normal neurodevelopment and neuronal activity especially at the neonatal age period [90]. CSF contents have been shown to affect neural progenitor cell behavior (proliferation and differentiation), brain patterning, and neurogenesis [87,91,92] and may be related to some of the neurodevelopmental impairments observed in children with PHH. This further emphasizes the importance of this study and future studies should evaluate the interaction of CSF electrolytes, the neurogenic niche, and neurodevelopmental outcomes. ...
Abstract Background Intraventricular hemorrhage (IVH) and post-hemorrhagic hydrocephalus (PHH) have a complex pathophysiology involving inflammatory response, ventricular zone and cell–cell junction disruption, and choroid-plexus (ChP) hypersecretion. Increased cerebrospinal fluid (CSF) cytokines, extracellular matrix proteins, and blood metabolites have been noted in IVH/PHH, but osmolality and electrolyte disturbances have not been evaluated in human infants with these conditions. We hypothesized that CSF total protein, osmolality, electrolytes, and immune cells increase in PHH. Methods CSF samples were obtained from lumbar punctures of control infants and infants with IVH prior to the development of PHH and any neurosurgical intervention. Osmolality, total protein, and electrolytes were measured in 52 infants (18 controls, 10 low grade (LG) IVH, 13 high grade (HG) IVH, and 11 PHH). Serum electrolyte concentrations, and CSF and serum cell counts within 1-day of clinical sampling were obtained from clinical charts. Frontal occipital horn ratio (FOR) was measured for estimating the degree of ventriculomegaly. Dunn or Tukey’s post-test ANOVA analysis were used for pair-wise comparisons. Results CSF osmolality, sodium, potassium, and chloride were elevated in PHH compared to control (p = 0.012
... In development, it is possible that this transependymal movement of CSF represents a key mechanism by which growth factors reach the hippocampus and SVZ. [77][78][79][80][81] This interpretation is consistent with previous studies that implicate growth factors, neurotransmitters, and other molecules pertinent in various signaling pathways diffuse across the ventricle wall to interact with type A, B2, and C cells in the SVZ. [79][80][81] Changes in CSF composition 435 and circulation dynamics in the setting of IVH-PHH may disrupt the interaction of these cells with transependymally transported molecules critical for development, with implications for ventricular zone disruption, neural stem cell loss, and eventual neurodevelopmental outcomes. ...
... [77][78][79][80][81] This interpretation is consistent with previous studies that implicate growth factors, neurotransmitters, and other molecules pertinent in various signaling pathways diffuse across the ventricle wall to interact with type A, B2, and C cells in the SVZ. [79][80][81] Changes in CSF composition 435 and circulation dynamics in the setting of IVH-PHH may disrupt the interaction of these cells with transependymally transported molecules critical for development, with implications for ventricular zone disruption, neural stem cell loss, and eventual neurodevelopmental outcomes. ...
Cerebrospinal fluid (CSF) movement within the brain interstitium is essential for the development and functioning of the brain. However, the interstitium has largely been thought of as a single entity through which CSF circulates, and it is not known whether specific cell populations within the CNS preferentially interact with CSF. Here, we developed a novel technique for CSF tracking, gold nanoparticle enhanced X-ray microtomography, to achieve micrometer-scale resolution visualization of CSF pathways during development. Using this method and subsequent histological analysis, we map global CSF pathways and present novel particle size-dependent circulation patterns through the CNS. We identify an intraparenchymal CSF circulation that targets stem cell-rich and cholinergic neuronal populations. CSF solute distribution to these areas is mediated by CSF flow along projections from the basal cisterns which is altered in posthemorrhagic hydrocephalus. Our study uncovers region-specific patterns in a biologically driven CSF circulation that has implications for normal brain development and the pathophysiology of hydrocephalus and neurodegenerative disorders.
... The disruption of the BCSFB is another pathology that might contribute to the electrolyte and osmolality changes (33,62,89,90). Of note, CSF osmolality and the concentrations of many electrolytes exceed serum levels in PHH. ...
... Finally, maintaining a normal CSF biochemical pro le is essential for normal neurodevelopment and neuronal activity especially at the neonatal age period (92). CSF contents have been shown to affect neural progenitor cell behavior (proliferation and differentiation), brain patterning, and neurogenesis (89,93,94) and may be related to some of the neurodevelopmental impairments observed in children with PHH. This further emphasizes the importance of this study and future studies should evaluate the interaction of CSF electrolytes, the neurogenic niche, and neurodevelopmental outcomes. ...
BACKGROUND
Intraventricular hemorrhage (IVH) and post-hemorrhagic hydrocephalus (PHH) have complex pathophysiology involving inflammatory response, ventricular zone and cell-cell junction disruption, and choroid-plexus (ChP) hypersecretion. Increased cerebrospinal fluid (CSF) cytokines, extracellular matrix proteins, and blood metabolites have been noted in IVH/PHH, but osmolality and electrolyte disturbances have not been evaluated in human infants with these conditions. We hypothesized that CSF total protein, osmolality, electrolytes, and immune cells increase in PHH.
METHODS
CSF samples were obtained from lumbar punctures in control infants and infants with IVH prior to development of PHH and any neurosurgical intervention. Osmolality, total protein, and electrolytes were measured in 52 infants (18 controls, 10 low grade (LG) IVH, 13 high grade (HG) IVH, and 11 PHH). Serum electrolyte concentrations, and CSF and serum cell counts within 1-day of clinical sampling were obtained from clinical charts. Dunn or Tukey’s post-test ANOVA analysis were used for pair-wise comparisons.
RESULTS
CSF osmolality, sodium, potassium, and chloride were elevated in PHH compared to control (p=0.012 - <0.0001), LGIVH (p=0.023 - <0.0001), and HGIVH (p=0.015 - 0.0003), while magnesium and calcium levels were higher compared to control (p=0.031) and LGIVH (p=0.041). CSF total protein was higher in both HGIVH and PHH compared to control (p=0.0009 and 0.0006 respectively) and LGIVH (p=0.034 and 0.028 respectively). These differences were not reflected in serum electrolyte concentrations nor calculated osmolality across the groups. However, quantitatively, CSF sodium and chloride contributed 86% of CSF osmolality change between control and PHH; and CSF osmolality positively correlated with CSF sodium (r,p=0.55,0.0015), potassium (r,p=0.51,0.0041), chloride (r,p=0.60,0.0004), but not total protein across the entire patient cohort. CSF total cells (p=0.012), total nucleated cells (p=0.0005), and percent monocyte (p=0.016) were elevated in PHH compared to control. Serum white blood cell count increased in PHH compared to control (p=0.042) but there were no differences in serum cell differential across groups. CSF total nucleated cells also positively correlated with CSF osmolality, sodium, potassium, and total protein (p=0.025-0.0008) in the whole cohort.
CONCLUSIONS
CSF osmolality increased in PHH, largely driven by electrolyte changes rather than protein levels. However, serum electrolytes levels were unchanged across groups. CSF osmolality and electrolyte changes were correlated with CSF total nucleated cells which were also increased in PHH, further suggesting PHH is a neuro-inflammatory condition.
... The CSF is essential for brain functioning in adult animals, and a number of studies in the past decades have strongly supported the crucial role of CSF in early developmental processes, including those involving the brain and body axis. The earliest form of CSF, known as eCSF, is found in the neural tube during the embryonic and fetal development of vertebrates [34]. Generally, eCSF is a protein-rich fluid and differs from adult CSF mainly in terms of composition [35,36]. ...
Background
Cerebrospinal fluid (CSF) is an ultra-filtrated colorless brain fluid that circulates within brain spaces like the ventricular cavities, subarachnoid space, and the spine. Its continuous flow serves many primary functions, including nourishment, brain protection, and waste removal.
Main body
The abnormal accumulation of CSF in brain cavities triggers severe hydrocephalus. Accumulating evidence had indicated that synchronized beats of motile cilia (cilia from multiciliated cells or the ependymal lining in brain ventricles) provide forceful pressure to generate and restrain CSF flow and maintain overall CSF circulation within brain spaces. In humans, the disorders caused by defective primary and/or motile cilia are generally referred to as ciliopathies. The key role of CSF circulation in brain development and its functioning has not been fully elucidated.
Conclusions
In this review, we briefly discuss the underlying role of motile cilia in CSF circulation and hydrocephalus. We have reviewed cilia and ciliated cells in the brain and the existing evidence for the regulatory role of functional cilia in CSF circulation in the brain. We further discuss the findings obtained for defective cilia and their potential involvement in hydrocephalus. Furthermore, this review will reinforce the idea of motile cilia as master regulators of CSF movements, brain development, and neuronal diseases.
... These segments further subdivide, and by the end of the embryonic period the five secondary brain vesicles are present, thus establishing the primary organization of the central nervous system (CNS) [24]. Throughout this period, embryonic CSF plays a vital role in delivering diffusible signals and nutrients to the developing brain, indicating major contributions to the proliferation, differentiation and survival of NSCs [25]. NSCs have the ability to self-renew and generate into the three major cell types in the CNS: neurons, astrocytes, and oligodendrocytes [26,27]. ...
Epigenetic mechanisms play an important regulatory role in neural processes associated with brain development and phenotypic outcome, and do so from early embryonic development through senescence. Though a complete picture has yet to emerge, it is clear that epigenetic changes promote a range of processes important for brain evolution, development, and function. Herein, we highlight key studies demonstrating a role for epigenetic mechanisms in these phenomena, including changes in phenotypes that are passed on to the next generation, gene imprinting, neural cell differentiation, neurogenesis, neuroimmune crosstalk, cognition, and psychopathology.
... Mass spectrometry analyses of embryonic CSF reveal a complex mixture of proteins that provide growth and survival signals to aRGCs, including extracellular matrix components, osmotic pressure regulators, ion carriers, hormone-binding proteins, lipid metabolism regulators, enzymes and their regulators. This composition seems to be conserved across species (Bueno & Garcia-Fernàndez, 2016;Cavanagh et al., 1983;Gato et al., 2004;Parada, Gato, & Bueno, 2005;Zappaterra et al., 2007). Because of the liquid nature of the CSF, its constituent signaling factors reach distant targets within the telencephalic ventricle throughout the entire rostro-caudal and lateromedial extent of the cortical VZ. ...
The mammalian cerebral cortex is the pinnacle of brain evolution, reaching its maximum complexity in terms of neuron number, diversity and functional circuitry. The emergence of this outstanding complexity begins during embryonic development, when a limited number of neural stem and progenitor cells manage to generate myriads of neurons in the appropriate numbers, types and proportions, in a process called neurogenesis. Here we review the current knowledge on the regulation of cortical neurogenesis, beginning with a description of the types of progenitor cells and their lineage relationships. This is followed by a review of the determinants of neuron fate, the molecular and genetic regulatory mechanisms, and considerations on the evolution of cortical neurogenesis in vertebrates leading to humans. We finish with an overview on how dysregulation of neurogenesis is a leading cause of human brain malformations and functional disabilities.
