Quantitative relationship between cerebrovascular network and neuronal cell types in mice

Wu, Ya; Bennett, Hannah C.; Chon, Uree; Vanselow, Daniel J.; Zhang, Qingguang; Muñoz-Castañeda, Rodrigo; Cheng, Keith C.; Osten, Pavel; Drew, Patrick J.; Kim, Yongsoo

doi:10.1016/j.celrep.2022.110978

Cited by 29 publications

(51 citation statements)

References 80 publications

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“…From all quantified vOLs, 22% were located at a vascular branching site in both motor- and somatosensory cortex (309 out of a total of 1392 vOLs from 6 mice, Fig. 1 A and D), which was independent of differences in vascular branching density [ 23 ]. Next, we traced processes from oligodendrocyte cell bodies labeled with CNP to MBP positive myelin sheaths, suggesting that vOLs are myelinating (n = 12 oligodendrocytes, n = 4 mice, Fig.…”

Section: Resultsmentioning

confidence: 99%

Direct association with the vascular basement membrane is a frequent feature of myelinating oligodendrocytes in the neocortex

Palhol

Balia

Terán

et al. 2023

Fluids Barriers CNS

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Background Oligodendrocyte lineage cells interact with the vasculature in the gray matter. Physical and functional interactions between blood vessels and oligodendrocyte precursor cells play an essential role in both the developing and adult brain. Oligodendrocyte precursor cells have been shown to migrate along the vasculature and subsequently detach from it during their differentiation to oligodendrocytes. However, the association of mature oligodendrocytes with blood vessels has been noted since the discovery of this glial cell type almost a century ago, but this interaction remains poorly explored. Results Here, we systematically investigated the extent of mature oligodendrocyte interaction with the vasculature in mouse brain. We found that ~ 17% of oligodendrocytes were in contact with blood vessels in the neocortex, the hippocampal CA1 region and the cerebellar cortex. Contacts were made mainly with capillaries and sparsely with larger arterioles or venules. By combining light and serial electron microscopy, we demonstrated that oligodendrocytes are in direct contact with the vascular basement membrane, raising the possibility of direct signaling pathways and metabolite exchange with endothelial cells. During experimental remyelination in the adult, oligodendrocytes were regenerated and associated with blood vessels in the same proportion compared to control cortex, suggesting a homeostatic regulation of the vasculature-associated oligodendrocyte population. Conclusions Based on their frequent and close association with blood vessels, we propose that vasculature-associated oligodendrocytes should be considered as an integral part of the brain vasculature microenvironment. This particular location could underlie specific functions of vasculature-associated oligodendrocytes, while contributing to the vulnerability of mature oligodendrocytes in neurological diseases.

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Section: Resultsmentioning

confidence: 99%

Direct association with the vascular basement membrane is a frequent feature of myelinating oligodendrocytes in the neocortex

Palhol

Balia

Terán

et al. 2023

Fluids Barriers CNS

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“…Another caveat is that 2PEF imaging performed on parallel plane to the brain surface can only visualize a small fraction of nNOS neurons in layer 2/3. Considering the heterogeneous distribution of nNOS neuron in the neocortex 14 , we cannot exclude that other patterns of activity may be evoked by somatosensory stimuli in nNOS neurons in other layers or cortical areas.…”

Section: Discussionmentioning

confidence: 99%

“…Numerous molecular signals have been implicated in functional hyperemia [9][10][11][12] . However, nitric oxide (NO), a potent vasodilator released by a subpopulation of GABAergic neurons expressing the neuronal isoform of NO synthase (nNOS or Nos1) [13][14][15][16] , is widely recognized as a major contributor 9,12,17 . nNOS neurons fall into distinct types based on their histochemical features 13 .…”

Section: Introductionmentioning

confidence: 99%

Calcium transients in nNOS neurons underlie distinct phases of the neurovascular response to barrel cortex activation in awake mice

Ahn

Anfray

Anrather

et al. 2022

Preprint

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Neuronal nitric oxide (NO) synthase (nNOS), a Ca2+ dependent enzyme, is expressed by distinct populations of neocortical neurons. Although neuronal NO is well known to contribute to the blood flow increase evoked by neural activity, the relationships between nNOS neurons activity and vascular responses in the awake state remain unclear. We imaged the barrel cortex in awake, head-fixed mice through a chronically implanted cranial window. The Ca2+ indicator GCaMP7f was expressed selectively in nNOS neurons using adenoviral gene transfer in nNOScre mice. Air-puffs directed at the contralateral whiskers or spontaneous motion induced Ca2+ transients in 30.2 ± 2.2% or 51.6 ± 3.3% of nNOS neurons, respectively, and evoked local arteriolar dilation. The greatest dilatation (14.8 ± 1.1%) occurred when whisking and motion occurred simultaneously. Ca2+ transients in individual nNOS neurons and local arteriolar dilation showed various degrees of correlation, which was strongest when the activity of whole nNOS neuron ensemble was examined. We also found that some nNOS neurons became active immediately prior to arteriolar dilation, while others were activated gradually after arteriolar dilatation. Discrete nNOS neuron subsets may contribute either to the initiation or to the maintenance of the vascular response, suggesting a previously unappreciated temporal specificity to the role of NO in neurovascular coupling.

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“…Excitatory and inhibitory neurons have many different characteristics, and even different subtypes of inhibitory neurons can play very different roles in neural circuitry (Ferrer & De Marco García, 2022; Keller & Martin, 2015; Schneider‐Mizell et al, 2023; Song et al, 2020; Wagatsuma et al, 2022). Additionally, there are critical differences in neuronal sub‐type specific interactions with the vasculature (Wu et al, 2022). Nevertheless, how vascular feedback influences different cell types is still largely unknown (Kim et al, 2016).…”

Section: Methodsmentioning

confidence: 99%

The development of bi‐directionally coupled self‐organizing neurovascular networks captures orientation‐selective neural and hemodynamic cortical responses

Kumar

O’Herron

Kara

et al. 2023

Eur J of Neuroscience

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Networks of neurons are the primary substrate of information processing. Conversely, blood vessels in the brain are generally viewed to have physiological functions unrelated to information processing, such as the timely supply of oxygen, and other nutrients to the neural tissue. However, recent studies have shown that cerebral microvessels, like neurons, exhibit tuned responses to sensory stimuli. Tuned neural responses to sensory stimuli may be enhanced with experience‐dependent Hebbian plasticity and other forms of learning. Hence, it is possible that the microvascular network might also be subject to some form of competitive learning rules during early postnatal development such that its fine‐scale structure becomes optimized for metabolic delivery to a given neural micro‐architecture. To explore the possibility of adaptive lateral interactions and tuned responses in cerebral microvessels, we modelled the cortical neurovascular network by interconnecting two laterally connected self‐organizing networks. The afferent and lateral connections of the neural and vascular networks were defined by trainable weights. By varying the topology of lateral connectivity in the vascular network layer, we observed that the partial correspondence of feature selectivity between neural and hemodynamic responses could be explained by lateral coupling across local blood vessels such that the central domain receives an excitatory drive of more blood flow and a distal surrounding region where blood flow is reduced. Critically, our simulations suggest a new role for feedback from the vascular to the neural network because the radius of vascular perfusion determines whether the cortical neural map develops into a clustered vs. salt‐and‐pepper organization.

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Quantitative relationship between cerebrovascular network and neuronal cell types in mice

Cited by 29 publications

References 80 publications

Direct association with the vascular basement membrane is a frequent feature of myelinating oligodendrocytes in the neocortex

Direct association with the vascular basement membrane is a frequent feature of myelinating oligodendrocytes in the neocortex

Calcium transients in nNOS neurons underlie distinct phases of the neurovascular response to barrel cortex activation in awake mice

The development of bi‐directionally coupled self‐organizing neurovascular networks captures orientation‐selective neural and hemodynamic cortical responses

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