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Developmental switch in neurovascular coupling in the immature rodent barrel cortex.

Zehendner CM, Tsohataridis S, Luhmann HJ, Yang JW - PLoS ONE (2013)

Bottom Line: In the mature CNS it is well accepted that cortical sensory processing results in a rise in regional cerebral blood flow (rCBF).In contrast at P30, MUA remains stable during repetitive stimulation and is associated with an increase in rCBF.Further we characterize in both age groups the responses in NVC to single sensory stimuli.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physiology, University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.

ABSTRACT
Neurovascular coupling (NVC) in the adult central nervous system (CNS) is a mechanism that provides regions of the brain with more oxygen and glucose upon increased levels of neural activation. Hemodynamic changes that go along with neural activation evoke a blood oxygen level-dependent (BOLD) signal in functional magnetic resonance imaging (fMRI) that can be used to study brain activity non-invasively. A correct correlation of the BOLD signal to neural activity is pivotal to understand this signal in neuronal development, health and disease. However, the function of NVC during development is largely unknown. The rodent whisker-to-barrel cortex is an experimentally well established model to study neurovascular interdependences. Using extracellular multi-electrode recordings and laser-Doppler-flowmetry (LDF) we show in the murine barrel cortex of postnatal day 7 (P7) and P30 mice in vivo that NVC undergoes a physiological shift during the first month of life. In the mature CNS it is well accepted that cortical sensory processing results in a rise in regional cerebral blood flow (rCBF). We show in P7 animals that rCBF decreases during prolonged multi-whisker stimulation and goes along with multi unit activity (MUA) fatigue. In contrast at P30, MUA remains stable during repetitive stimulation and is associated with an increase in rCBF. Further we characterize in both age groups the responses in NVC to single sensory stimuli. We suggest that the observed shift in NVC is an important process in cortical development that may be of high relevance for the correct interpretation of brain activity e.g. in fMRI studies of the immature central nervous system (CNS).

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Murine cortices are less myelinated at P7 compared with P30.In order to determine myelination MBP expression was studied in cortices of P7 and P30 mice. Representative z-stack maximum projections (700 nm thickness of stacks) from 3 animals per group are shown (MBP green, the axonal marker SMI 31-R in red, DAPI blue). Note that MBP is nearly absent in the P7 cortex whilst there is high MBP expression at P30. Note the highly myelinated intermediate zone marked with an arrowhead. Asterisk marks a preparation artifact. Quantitative analyses of MBP fluorescence (AU: arbitrary units) demonstrate a significantly smaller MBP expression at P7. Pictures were acquired using equal time exposures and laser intensities.
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pone-0080749-g004: Murine cortices are less myelinated at P7 compared with P30.In order to determine myelination MBP expression was studied in cortices of P7 and P30 mice. Representative z-stack maximum projections (700 nm thickness of stacks) from 3 animals per group are shown (MBP green, the axonal marker SMI 31-R in red, DAPI blue). Note that MBP is nearly absent in the P7 cortex whilst there is high MBP expression at P30. Note the highly myelinated intermediate zone marked with an arrowhead. Asterisk marks a preparation artifact. Quantitative analyses of MBP fluorescence (AU: arbitrary units) demonstrate a significantly smaller MBP expression at P7. Pictures were acquired using equal time exposures and laser intensities.

Mentions: Because cortical MUA response at P7 was significantly delayed compared with P30 the underlying cellular mechanism were studied in more detail. Nerve conducting velocity is crucially dependent on myelination of nerve fibers[27]. It is known that murine myelination is not fully established at neonatal age[28]. Therefore we analyzed myelination in P7 and P30 mice cortices via immunohistochemical visualization of myelin basic protein (MBP), a key component for proper myelination[28,29]. Here we found a significant difference in MBP levels in P7 compared to P30 animals (cortical MBP fluorescent intensity at P7 11.4 + 1.3 arbitrary units (AU) vs. at P30 39.3 + 4.9 AU, P < 0.0001, unpaired t-test, n = 12 cortical regions of interest from 3 animals per group, Figure 4).


Developmental switch in neurovascular coupling in the immature rodent barrel cortex.

Zehendner CM, Tsohataridis S, Luhmann HJ, Yang JW - PLoS ONE (2013)

Murine cortices are less myelinated at P7 compared with P30.In order to determine myelination MBP expression was studied in cortices of P7 and P30 mice. Representative z-stack maximum projections (700 nm thickness of stacks) from 3 animals per group are shown (MBP green, the axonal marker SMI 31-R in red, DAPI blue). Note that MBP is nearly absent in the P7 cortex whilst there is high MBP expression at P30. Note the highly myelinated intermediate zone marked with an arrowhead. Asterisk marks a preparation artifact. Quantitative analyses of MBP fluorescence (AU: arbitrary units) demonstrate a significantly smaller MBP expression at P7. Pictures were acquired using equal time exposures and laser intensities.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3818260&req=5

pone-0080749-g004: Murine cortices are less myelinated at P7 compared with P30.In order to determine myelination MBP expression was studied in cortices of P7 and P30 mice. Representative z-stack maximum projections (700 nm thickness of stacks) from 3 animals per group are shown (MBP green, the axonal marker SMI 31-R in red, DAPI blue). Note that MBP is nearly absent in the P7 cortex whilst there is high MBP expression at P30. Note the highly myelinated intermediate zone marked with an arrowhead. Asterisk marks a preparation artifact. Quantitative analyses of MBP fluorescence (AU: arbitrary units) demonstrate a significantly smaller MBP expression at P7. Pictures were acquired using equal time exposures and laser intensities.
Mentions: Because cortical MUA response at P7 was significantly delayed compared with P30 the underlying cellular mechanism were studied in more detail. Nerve conducting velocity is crucially dependent on myelination of nerve fibers[27]. It is known that murine myelination is not fully established at neonatal age[28]. Therefore we analyzed myelination in P7 and P30 mice cortices via immunohistochemical visualization of myelin basic protein (MBP), a key component for proper myelination[28,29]. Here we found a significant difference in MBP levels in P7 compared to P30 animals (cortical MBP fluorescent intensity at P7 11.4 + 1.3 arbitrary units (AU) vs. at P30 39.3 + 4.9 AU, P < 0.0001, unpaired t-test, n = 12 cortical regions of interest from 3 animals per group, Figure 4).

Bottom Line: In the mature CNS it is well accepted that cortical sensory processing results in a rise in regional cerebral blood flow (rCBF).In contrast at P30, MUA remains stable during repetitive stimulation and is associated with an increase in rCBF.Further we characterize in both age groups the responses in NVC to single sensory stimuli.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physiology, University Medical Center of the Johannes Gutenberg-University, Mainz, Germany.

ABSTRACT
Neurovascular coupling (NVC) in the adult central nervous system (CNS) is a mechanism that provides regions of the brain with more oxygen and glucose upon increased levels of neural activation. Hemodynamic changes that go along with neural activation evoke a blood oxygen level-dependent (BOLD) signal in functional magnetic resonance imaging (fMRI) that can be used to study brain activity non-invasively. A correct correlation of the BOLD signal to neural activity is pivotal to understand this signal in neuronal development, health and disease. However, the function of NVC during development is largely unknown. The rodent whisker-to-barrel cortex is an experimentally well established model to study neurovascular interdependences. Using extracellular multi-electrode recordings and laser-Doppler-flowmetry (LDF) we show in the murine barrel cortex of postnatal day 7 (P7) and P30 mice in vivo that NVC undergoes a physiological shift during the first month of life. In the mature CNS it is well accepted that cortical sensory processing results in a rise in regional cerebral blood flow (rCBF). We show in P7 animals that rCBF decreases during prolonged multi-whisker stimulation and goes along with multi unit activity (MUA) fatigue. In contrast at P30, MUA remains stable during repetitive stimulation and is associated with an increase in rCBF. Further we characterize in both age groups the responses in NVC to single sensory stimuli. We suggest that the observed shift in NVC is an important process in cortical development that may be of high relevance for the correct interpretation of brain activity e.g. in fMRI studies of the immature central nervous system (CNS).

Show MeSH
Related in: MedlinePlus