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The regulation of brain states by neuroactive substances distributed via the cerebrospinal fluid; a review.

Veening JG, Barendregt HP - Cerebrospinal Fluid Res (2010)

Bottom Line: Thus, many brain areas are exposed to and can be influenced by substances contained in the CSF.In addition, the available evidence for the release of neuropeptides and other neuroactive substances into the CSF is reviewed, with particular attention to the selective effects of these on distant downstream receptive brain areas.As a conclusion we suggest that (1) the flowing CSF is involved in more than just nutrient and waste control, but is also used as a broadcasting system consisting of coordinated messages to a variety of nearby and distant brain areas; (2) this special form of volume transmission underlies changes in behavioral states.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, (109) UMC St Radboud, Nijmegen, the Netherlands. j.g.veening@ru.nl

ABSTRACT
The cerebrospinal fluid (CSF) system provides nutrients to and removes waste products from the brain. Recent findings suggest, however, that in addition, the CSF contains message molecules in the form of actively released neuroactive substances. The concentrations of these vary between locations, suggesting they are important for the changes in brain activity that underlie different brain states, and induce different sensory input and behavioral output relationships.The cranial CSF displays a rapid caudally-directed ventricular flow followed by a slower rostrally-directed subarachnoid flow (mainly towards the cribriform plate and from there into the nasal lymphatics). Thus, many brain areas are exposed to and can be influenced by substances contained in the CSF. In this review we discuss the production and flow of the CSF, including the mechanisms involved in the regulation of its composition. In addition, the available evidence for the release of neuropeptides and other neuroactive substances into the CSF is reviewed, with particular attention to the selective effects of these on distant downstream receptive brain areas. As a conclusion we suggest that (1) the flowing CSF is involved in more than just nutrient and waste control, but is also used as a broadcasting system consisting of coordinated messages to a variety of nearby and distant brain areas; (2) this special form of volume transmission underlies changes in behavioral states.

No MeSH data available.


Related in: MedlinePlus

A schematic diagram showing the direction of the CSF bulk flow in the mammalian brain based on a midsagittal section of the rat brain, kindly provided by Prof. L.W. Swanson. The following regions are indicated: telencephalon (pink shades); diencephalon (interbrain) and brainstem areas (yellow shades); cerebellum dorsal to the brainstem (light blue); sectioned fiber tracts (black). CSF (blue arrows) flows from the lateral ventricles to the third ventricle via the interventricular foramen (IVF), and flows caudally along the dorsal and ventral side of thalamic adhesion, to the cerebral aqueduct (AQ) and fourth ventricle (V4). Some CSF may continue flowing caudally through the central canal of the spinal cord (CC), but most leaves the ventricular system via the lateral apertures and flows through the subarachnoid space, surrounding the brain. This external flow is indicated here along the dorsal and ventral side of the brain but occurs also along all other external brain surfaces. The destination of the subarachnoid flow is the cribriform plate of the ethmoidal bone, containing the penetrating olfactory fibers, where CSF is released in small lymphatic vessels. Additional abbreviations: V3(p, h, m, t, pi): regions and recesses of the third ventricle; Circumventricular organs: 1: subfornical organ; 2: organum vasculosum of the lamina terminalis; 3: median eminence; 4: subcommissural organ; 5: pineal organ; 6: area postrema; AL, IL and NL: different lobes of pituitary; Fiber bundles crossing the midline, coloured black, are not relevant for the present review.
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Figure 2: A schematic diagram showing the direction of the CSF bulk flow in the mammalian brain based on a midsagittal section of the rat brain, kindly provided by Prof. L.W. Swanson. The following regions are indicated: telencephalon (pink shades); diencephalon (interbrain) and brainstem areas (yellow shades); cerebellum dorsal to the brainstem (light blue); sectioned fiber tracts (black). CSF (blue arrows) flows from the lateral ventricles to the third ventricle via the interventricular foramen (IVF), and flows caudally along the dorsal and ventral side of thalamic adhesion, to the cerebral aqueduct (AQ) and fourth ventricle (V4). Some CSF may continue flowing caudally through the central canal of the spinal cord (CC), but most leaves the ventricular system via the lateral apertures and flows through the subarachnoid space, surrounding the brain. This external flow is indicated here along the dorsal and ventral side of the brain but occurs also along all other external brain surfaces. The destination of the subarachnoid flow is the cribriform plate of the ethmoidal bone, containing the penetrating olfactory fibers, where CSF is released in small lymphatic vessels. Additional abbreviations: V3(p, h, m, t, pi): regions and recesses of the third ventricle; Circumventricular organs: 1: subfornical organ; 2: organum vasculosum of the lamina terminalis; 3: median eminence; 4: subcommissural organ; 5: pineal organ; 6: area postrema; AL, IL and NL: different lobes of pituitary; Fiber bundles crossing the midline, coloured black, are not relevant for the present review.

Mentions: Concerning the cranial CSF surrounding the brain, most textbooks tell us that arachnoid granulations, penetrating the dura and extending into the superior sagittal sinus, compose the main outlet system for CSF absorption in the human. Recent animal investigations, however, have shown that at least 50% and perhaps up to 80% or more of the CSF leaves the cranial cavity through the cribriform plate, via the perineuronal spaces surrounding the olfactory nerves, to drain into the nasal and cervical lymphatics (Fig 2) [64-70]. This rostral outflow of CSF contains considerable amounts of interstitial fluid, especially from midbrain areas [71,72], and plays an important role in CNS immune system interactions [68,73].


The regulation of brain states by neuroactive substances distributed via the cerebrospinal fluid; a review.

Veening JG, Barendregt HP - Cerebrospinal Fluid Res (2010)

A schematic diagram showing the direction of the CSF bulk flow in the mammalian brain based on a midsagittal section of the rat brain, kindly provided by Prof. L.W. Swanson. The following regions are indicated: telencephalon (pink shades); diencephalon (interbrain) and brainstem areas (yellow shades); cerebellum dorsal to the brainstem (light blue); sectioned fiber tracts (black). CSF (blue arrows) flows from the lateral ventricles to the third ventricle via the interventricular foramen (IVF), and flows caudally along the dorsal and ventral side of thalamic adhesion, to the cerebral aqueduct (AQ) and fourth ventricle (V4). Some CSF may continue flowing caudally through the central canal of the spinal cord (CC), but most leaves the ventricular system via the lateral apertures and flows through the subarachnoid space, surrounding the brain. This external flow is indicated here along the dorsal and ventral side of the brain but occurs also along all other external brain surfaces. The destination of the subarachnoid flow is the cribriform plate of the ethmoidal bone, containing the penetrating olfactory fibers, where CSF is released in small lymphatic vessels. Additional abbreviations: V3(p, h, m, t, pi): regions and recesses of the third ventricle; Circumventricular organs: 1: subfornical organ; 2: organum vasculosum of the lamina terminalis; 3: median eminence; 4: subcommissural organ; 5: pineal organ; 6: area postrema; AL, IL and NL: different lobes of pituitary; Fiber bundles crossing the midline, coloured black, are not relevant for the present review.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2821375&req=5

Figure 2: A schematic diagram showing the direction of the CSF bulk flow in the mammalian brain based on a midsagittal section of the rat brain, kindly provided by Prof. L.W. Swanson. The following regions are indicated: telencephalon (pink shades); diencephalon (interbrain) and brainstem areas (yellow shades); cerebellum dorsal to the brainstem (light blue); sectioned fiber tracts (black). CSF (blue arrows) flows from the lateral ventricles to the third ventricle via the interventricular foramen (IVF), and flows caudally along the dorsal and ventral side of thalamic adhesion, to the cerebral aqueduct (AQ) and fourth ventricle (V4). Some CSF may continue flowing caudally through the central canal of the spinal cord (CC), but most leaves the ventricular system via the lateral apertures and flows through the subarachnoid space, surrounding the brain. This external flow is indicated here along the dorsal and ventral side of the brain but occurs also along all other external brain surfaces. The destination of the subarachnoid flow is the cribriform plate of the ethmoidal bone, containing the penetrating olfactory fibers, where CSF is released in small lymphatic vessels. Additional abbreviations: V3(p, h, m, t, pi): regions and recesses of the third ventricle; Circumventricular organs: 1: subfornical organ; 2: organum vasculosum of the lamina terminalis; 3: median eminence; 4: subcommissural organ; 5: pineal organ; 6: area postrema; AL, IL and NL: different lobes of pituitary; Fiber bundles crossing the midline, coloured black, are not relevant for the present review.
Mentions: Concerning the cranial CSF surrounding the brain, most textbooks tell us that arachnoid granulations, penetrating the dura and extending into the superior sagittal sinus, compose the main outlet system for CSF absorption in the human. Recent animal investigations, however, have shown that at least 50% and perhaps up to 80% or more of the CSF leaves the cranial cavity through the cribriform plate, via the perineuronal spaces surrounding the olfactory nerves, to drain into the nasal and cervical lymphatics (Fig 2) [64-70]. This rostral outflow of CSF contains considerable amounts of interstitial fluid, especially from midbrain areas [71,72], and plays an important role in CNS immune system interactions [68,73].

Bottom Line: Thus, many brain areas are exposed to and can be influenced by substances contained in the CSF.In addition, the available evidence for the release of neuropeptides and other neuroactive substances into the CSF is reviewed, with particular attention to the selective effects of these on distant downstream receptive brain areas.As a conclusion we suggest that (1) the flowing CSF is involved in more than just nutrient and waste control, but is also used as a broadcasting system consisting of coordinated messages to a variety of nearby and distant brain areas; (2) this special form of volume transmission underlies changes in behavioral states.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, (109) UMC St Radboud, Nijmegen, the Netherlands. j.g.veening@ru.nl

ABSTRACT
The cerebrospinal fluid (CSF) system provides nutrients to and removes waste products from the brain. Recent findings suggest, however, that in addition, the CSF contains message molecules in the form of actively released neuroactive substances. The concentrations of these vary between locations, suggesting they are important for the changes in brain activity that underlie different brain states, and induce different sensory input and behavioral output relationships.The cranial CSF displays a rapid caudally-directed ventricular flow followed by a slower rostrally-directed subarachnoid flow (mainly towards the cribriform plate and from there into the nasal lymphatics). Thus, many brain areas are exposed to and can be influenced by substances contained in the CSF. In this review we discuss the production and flow of the CSF, including the mechanisms involved in the regulation of its composition. In addition, the available evidence for the release of neuropeptides and other neuroactive substances into the CSF is reviewed, with particular attention to the selective effects of these on distant downstream receptive brain areas. As a conclusion we suggest that (1) the flowing CSF is involved in more than just nutrient and waste control, but is also used as a broadcasting system consisting of coordinated messages to a variety of nearby and distant brain areas; (2) this special form of volume transmission underlies changes in behavioral states.

No MeSH data available.


Related in: MedlinePlus