A Network Architecture for Bidirectional Neurovascular Coupling in Rat Whisker Barrel Cortex

Kumar, Bhadra S.; Khot, Aditi; Chakravarthy, V. Srinivasa; Pushpavanam, S.

doi:10.3389/fncom.2021.638700

Cited by 7 publications

(8 citation statements)

References 83 publications

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“…Many experimental observations [2,3], as well as the results from our previous computational models [30,43,44] support the hypothesis by Moore and Cao [1] that hemodynamics could impact neural activity directly or indirectly. Hence in our NV_LIN model, the vascular layer is designed to send feedback to the neural layer.…”

Section: Introductionsupporting

confidence: 77%

“…There is a continuous flow of vasodilatory signals from the neurons to vessels and a continuous flow of energy substrates from vessels to the neural tissues. It is established by prior studies that any significant change in vascular feedback could alter the neural characteristics, especially during development [30,43,44,52]. The possibility of retrograde signaling from vessels to neurons was confirmed by Kim and colleagues [2] where the tone of the vessels influenced the firing rate of pyramidal neurons.…”

Section: Discussionmentioning

confidence: 90%

“…The vascular feedback to the neural network is critical to ensure the continuous energy supply to the neurons. The impact of vascular feedback on neural network characteristics has been explored by both experimental [52] and modeling studies [30]. The lateral connectivity and the tuned response in vessels define the vascular feedback to the neural layer in a totally different perspective.…”

Section: The Influence Of Vascular Feedback On the Neural Map Formationmentioning

confidence: 99%

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

Kumar

O’Herron

Kara

et al. 2021

Preprint

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The network of neurons in the brain is considered the primary substrate of information processing. Despite growing evidence on the possible role of cerebral blood flow in information processing, the cerebrovascular network is generally viewed as an irrigation system that ensures a timely supply of oxygen, glucose, and nutrients to the neural tissue. However, a recent study has shown that cerebral microvessels, like neurons, also exhibit tuned responses to sensory stimuli. Tuned neural responses to sensory stimuli are certainly enhanced with experience-dependent Hebbian plasticity and other forms of learning. Hence it is possible that the densely interconnected microvascular network might also be subject to some form of plasticity or 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 modeled the cortical neurovascular network by interconnecting two laterally connected self-organizing networks (Laterally Interconnected Synergetically Self-Organizing Map - LISSOM). The afferent and lateral connections of the LISSOM 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 more 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 seems to determine whether the cortical neural map develops into a clustered and columnar vs. salt-and-pepper organization.

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Section: Introductionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 90%

Section: The Influence Of Vascular Feedback On the Neural Map Formationmentioning

confidence: 99%

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

Kumar

O’Herron

Kara

et al. 2021

Preprint

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“…The relevance of a healthy vasculature in shaping the function of the neural network has been discussed extensively [39][40][41][42][43][44][45][46]. Neurodegenerative diseases are being traced back to an impaired neurovascular functional coupling [1,[47][48][49][50].…”

Section: Discussionmentioning

confidence: 99%

The Influence of Neural Activity and Neural Cytoarchitecture on Cerebrovascular Arborization: A Computational Model

Kumar

Menon

et al. 2022

Preprint

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Normal functioning of the brain relies on a continual and efficient delivery of energy by a vast network of cerebral blood vessels. The bidirectional coupling between neurons and blood vessels consists of vasodilatory energy demand signals from neurons to blood vessels, and the retrograde flow of energy substrates from the vessels to neurons, which fuel neural firing, growth and other housekeeping activities in the neurons. Recent works indicate that, in addition to the functional coupling observed in the adult brain, the interdependence between the neural and vascular networks begins at the embryonic stage, and continues into subsequent developmental stages. The proposed Vascular Arborization Model (VAM) captures the effect of neural cytoarchitecture and neural activity on vascular arborization. The VAM describes three important stages of vascular tree growth: (i) The prenatal growth phase, where the vascular arborization depends on the cytoarchitecture of neurons and non-neural cells, (ii) the post-natal growth phase during which the further arborization of the vasculature depends on neural activity in addition to neural cytoarchitecture, and (iii) the settling phase, where the fully grown vascular tree repositions its vascular branch points or nodes to ensure minimum path length and wire length. The vasculature growth depicted by VAM captures structural characteristics like vascular volume density, radii, mean distance to proximal neurons in the cortex. VAM-grown vasculature agrees with the experimental observation that the neural densities do not covary with the vascular density along the depth of the cortex but predicts a high correlation between neural areal density and microvascular density when compared over a global scale (across animals and regions). To explore the influence of neural activity on vascular arborization, the VAM was used to grow the vasculature in neonatal rat whisker barrel cortex under two conditions: (i) Control, where the whiskers were intact and (ii) Lesioned, where one row of whiskers was cauterized. The model captures a significant reduction in vascular branch density in lesioned animals compared to control animals, concurring with experimental observation.

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“… 227 They can be trained to reproduce real-time series data, and the trained network can be reverse engineered to infer mechanisms of interaction between network elements. 228 , 229 Multilayer approaches can also model different interacting compartments of a system, such as neuronal and astrocytic layers 230 but also vascular layers which impose energetic constraints 231 or interact bidirectionally 232 with neuronal layers.…”

Section: Toward the Disentangling Of Neurovascular Networkmentioning

confidence: 99%

Toward an integrative neurovascular framework for studying brain networks

et al. 2022

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. Brain functional connectivity based on the measure of blood oxygen level-dependent (BOLD) functional magnetic resonance imaging (fMRI) signals has become one of the most widely used measurements in human neuroimaging. However, the nature of the functional networks revealed by BOLD fMRI can be ambiguous, as highlighted by a recent series of experiments that have suggested that typical resting-state networks can be replicated from purely vascular or physiologically driven BOLD signals. After going through a brief review of the key concepts of brain network analysis, we explore how the vascular and neuronal systems interact to give rise to the brain functional networks measured with BOLD fMRI. This leads us to emphasize a view of the vascular network not only as a confounding element in fMRI but also as a functionally relevant system that is entangled with the neuronal network. To study the vascular and neuronal underpinnings of BOLD functional connectivity, we consider a combination of methodological avenues based on multiscale and multimodal optical imaging in mice, used in combination with computational models that allow the integration of vascular information to explain functional connectivity.

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A Network Architecture for Bidirectional Neurovascular Coupling in Rat Whisker Barrel Cortex

Cited by 7 publications

References 83 publications

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

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

The Influence of Neural Activity and Neural Cytoarchitecture on Cerebrovascular Arborization: A Computational Model

Toward an integrative neurovascular framework for studying brain networks

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