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Communication and wiring in the cortical connectome.

Budd JM, Kisvárday ZF - Front Neuroanat (2012)

Bottom Line: We report three main conclusions.To avoid neglecting neuron and microcircuit levels of cortical organization, the connectome framework should incorporate more morphological description.We conclude the hypothesized trade-off between spatial and temporal costs may potentially offer a powerful explanation for cortical wiring patterns.

View Article: PubMed Central - PubMed

Affiliation: Department of Informatics, University of Sussex Falmer, East Sussex, UK.

ABSTRACT
In cerebral cortex, the huge mass of axonal wiring that carries information between near and distant neurons is thought to provide the neural substrate for cognitive and perceptual function. The goal of mapping the connectivity of cortical axons at different spatial scales, the cortical connectome, is to trace the paths of information flow in cerebral cortex. To appreciate the relationship between the connectome and cortical function, we need to discover the nature and purpose of the wiring principles underlying cortical connectivity. A popular explanation has been that axonal length is strictly minimized both within and between cortical regions. In contrast, we have hypothesized the existence of a multi-scale principle of cortical wiring where to optimize communication there is a trade-off between spatial (construction) and temporal (routing) costs. Here, using recent evidence concerning cortical spatial networks we critically evaluate this hypothesis at neuron, local circuit, and pathway scales. We report three main conclusions. First, the axonal and dendritic arbor morphology of single neocortical neurons may be governed by a similar wiring principle, one that balances the conservation of cellular material and conduction delay. Second, the same principle may be observed for fiber tracts connecting cortical regions. Third, the absence of sufficient local circuit data currently prohibits any meaningful assessment of the hypothesis at this scale of cortical organization. To avoid neglecting neuron and microcircuit levels of cortical organization, the connectome framework should incorporate more morphological description. In addition, structural analyses of temporal cost for cortical circuits should take account of both axonal conduction and neuronal integration delays, which appear mostly of the same order of magnitude. We conclude the hypothesized trade-off between spatial and temporal costs may potentially offer a powerful explanation for cortical wiring patterns.

No MeSH data available.


Related in: MedlinePlus

Elementary graphical representations of cortical organization at different spatial scales. (A)Neuron scale. Each vertex represents the location of a cellular landmark obtained from the 3D reconstruction of individual axonal or dendritic arbors (e.g., location of the presynaptic terminal boutons) with an undirected edge representing the section of membrane linking these vertices either by the actual path length or the direct distance between a vertex pair. (B)Local Circuit scale. Each vertex represents the somatic location of a single neuron with a directed (or undirected) edge representing the sum of the axonal and dendritic lengths connecting a pair of neuronal somata. (C)Pathway scale. Each vertex represents a distinct cortical brain region in grey matter with a directed (or undirected) edge representing the axonal fiber tract connecting a pair of cortical regions, where its length describes the actual path or direct distance of its course within white matter.
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Figure 3: Elementary graphical representations of cortical organization at different spatial scales. (A)Neuron scale. Each vertex represents the location of a cellular landmark obtained from the 3D reconstruction of individual axonal or dendritic arbors (e.g., location of the presynaptic terminal boutons) with an undirected edge representing the section of membrane linking these vertices either by the actual path length or the direct distance between a vertex pair. (B)Local Circuit scale. Each vertex represents the somatic location of a single neuron with a directed (or undirected) edge representing the sum of the axonal and dendritic lengths connecting a pair of neuronal somata. (C)Pathway scale. Each vertex represents a distinct cortical brain region in grey matter with a directed (or undirected) edge representing the axonal fiber tract connecting a pair of cortical regions, where its length describes the actual path or direct distance of its course within white matter.

Mentions: To evaluate the proposed multi-scale wiring principle, we now examine the results from the analyses of graphical representations of cortical organization at three different spatial scales (see Figure 3): neuron, local circuit, and pathway scales. The reason for choosing these scales is that they offer a simple hierarchical organization of cerebral cortex into individual functional elements, connectivity within a cortical region, and connectivity between cortical regions, respectively. Local circuit (microscopic) and pathway (macroscopic) scales are represented in both approaches discussed in the previous section. But this scheme includes a neuron scale, which is absent in the Human Connectome proposal, because we are interested in how communication costs may have shaped neuronal morphology as well as cortical circuits. We recognize that this scheme limits our consideration to specific spatial scales and so may neglect subtle intermediate-scale wiring strategies.


Communication and wiring in the cortical connectome.

Budd JM, Kisvárday ZF - Front Neuroanat (2012)

Elementary graphical representations of cortical organization at different spatial scales. (A)Neuron scale. Each vertex represents the location of a cellular landmark obtained from the 3D reconstruction of individual axonal or dendritic arbors (e.g., location of the presynaptic terminal boutons) with an undirected edge representing the section of membrane linking these vertices either by the actual path length or the direct distance between a vertex pair. (B)Local Circuit scale. Each vertex represents the somatic location of a single neuron with a directed (or undirected) edge representing the sum of the axonal and dendritic lengths connecting a pair of neuronal somata. (C)Pathway scale. Each vertex represents a distinct cortical brain region in grey matter with a directed (or undirected) edge representing the axonal fiber tract connecting a pair of cortical regions, where its length describes the actual path or direct distance of its course within white matter.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472565&req=5

Figure 3: Elementary graphical representations of cortical organization at different spatial scales. (A)Neuron scale. Each vertex represents the location of a cellular landmark obtained from the 3D reconstruction of individual axonal or dendritic arbors (e.g., location of the presynaptic terminal boutons) with an undirected edge representing the section of membrane linking these vertices either by the actual path length or the direct distance between a vertex pair. (B)Local Circuit scale. Each vertex represents the somatic location of a single neuron with a directed (or undirected) edge representing the sum of the axonal and dendritic lengths connecting a pair of neuronal somata. (C)Pathway scale. Each vertex represents a distinct cortical brain region in grey matter with a directed (or undirected) edge representing the axonal fiber tract connecting a pair of cortical regions, where its length describes the actual path or direct distance of its course within white matter.
Mentions: To evaluate the proposed multi-scale wiring principle, we now examine the results from the analyses of graphical representations of cortical organization at three different spatial scales (see Figure 3): neuron, local circuit, and pathway scales. The reason for choosing these scales is that they offer a simple hierarchical organization of cerebral cortex into individual functional elements, connectivity within a cortical region, and connectivity between cortical regions, respectively. Local circuit (microscopic) and pathway (macroscopic) scales are represented in both approaches discussed in the previous section. But this scheme includes a neuron scale, which is absent in the Human Connectome proposal, because we are interested in how communication costs may have shaped neuronal morphology as well as cortical circuits. We recognize that this scheme limits our consideration to specific spatial scales and so may neglect subtle intermediate-scale wiring strategies.

Bottom Line: We report three main conclusions.To avoid neglecting neuron and microcircuit levels of cortical organization, the connectome framework should incorporate more morphological description.We conclude the hypothesized trade-off between spatial and temporal costs may potentially offer a powerful explanation for cortical wiring patterns.

View Article: PubMed Central - PubMed

Affiliation: Department of Informatics, University of Sussex Falmer, East Sussex, UK.

ABSTRACT
In cerebral cortex, the huge mass of axonal wiring that carries information between near and distant neurons is thought to provide the neural substrate for cognitive and perceptual function. The goal of mapping the connectivity of cortical axons at different spatial scales, the cortical connectome, is to trace the paths of information flow in cerebral cortex. To appreciate the relationship between the connectome and cortical function, we need to discover the nature and purpose of the wiring principles underlying cortical connectivity. A popular explanation has been that axonal length is strictly minimized both within and between cortical regions. In contrast, we have hypothesized the existence of a multi-scale principle of cortical wiring where to optimize communication there is a trade-off between spatial (construction) and temporal (routing) costs. Here, using recent evidence concerning cortical spatial networks we critically evaluate this hypothesis at neuron, local circuit, and pathway scales. We report three main conclusions. First, the axonal and dendritic arbor morphology of single neocortical neurons may be governed by a similar wiring principle, one that balances the conservation of cellular material and conduction delay. Second, the same principle may be observed for fiber tracts connecting cortical regions. Third, the absence of sufficient local circuit data currently prohibits any meaningful assessment of the hypothesis at this scale of cortical organization. To avoid neglecting neuron and microcircuit levels of cortical organization, the connectome framework should incorporate more morphological description. In addition, structural analyses of temporal cost for cortical circuits should take account of both axonal conduction and neuronal integration delays, which appear mostly of the same order of magnitude. We conclude the hypothesized trade-off between spatial and temporal costs may potentially offer a powerful explanation for cortical wiring patterns.

No MeSH data available.


Related in: MedlinePlus