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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

Most estimated intrinsic and extrinsic axonal conduction delays are within an order of magnitude of neuronal integration delays apart from when axons conduct at their slowest rate and neurons operate in a high-conductance state. (A) Intrinsic axon path lengths of spiny neuron within gray matter in adult cat cerebral cortex (n = 22,001 paths from 19 neuron reconstructions). Data taken from Budd et al. (2010). (B) Extrinsic axonal fiber tract lengths in adult macaque cerebral cortex (n = 2309 pathways). Data taken from Kaiser and Hilgetag (2006).
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Figure 7: Most estimated intrinsic and extrinsic axonal conduction delays are within an order of magnitude of neuronal integration delays apart from when axons conduct at their slowest rate and neurons operate in a high-conductance state. (A) Intrinsic axon path lengths of spiny neuron within gray matter in adult cat cerebral cortex (n = 22,001 paths from 19 neuron reconstructions). Data taken from Budd et al. (2010). (B) Extrinsic axonal fiber tract lengths in adult macaque cerebral cortex (n = 2309 pathways). Data taken from Kaiser and Hilgetag (2006).

Mentions: Figure 7 shows the results for both single intrinsic axon and extrinsic fiber tract data were quite similar. For the low-conductance state, virtually all axonal conduction delays were within an order of magnitude of neuronal integration delay almost regardless of mean conduction velocity (Figures 7A,B, square symbols). For the high-conductance state, except at the very lowest conduction velocities, the majority of the conduction delays were comparable to integration delays (Figures 7A,B, circle symbols). These results suggest that in both local and macroscopic cortical networks presynaptic axonal conduction delays may be mostly of a similar order of magnitude as postsynaptic neuronal integration delays (i.e., taxon ~ tint). To determine the shortest path length between a pair of neural elements, therefore, it is important to take into account both the number of neural elements in the path as well as its physical length estimated from measuring axonal and/or dendritic processes. It is unclear whether assigning a cost for each vertex as well as each edge would significantly affect the results for cortical networks previously analyzed (Kaiser and Hilgetag, 2006; Bassett et al., 2010).


Communication and wiring in the cortical connectome.

Budd JM, Kisvárday ZF - Front Neuroanat (2012)

Most estimated intrinsic and extrinsic axonal conduction delays are within an order of magnitude of neuronal integration delays apart from when axons conduct at their slowest rate and neurons operate in a high-conductance state. (A) Intrinsic axon path lengths of spiny neuron within gray matter in adult cat cerebral cortex (n = 22,001 paths from 19 neuron reconstructions). Data taken from Budd et al. (2010). (B) Extrinsic axonal fiber tract lengths in adult macaque cerebral cortex (n = 2309 pathways). Data taken from Kaiser and Hilgetag (2006).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Most estimated intrinsic and extrinsic axonal conduction delays are within an order of magnitude of neuronal integration delays apart from when axons conduct at their slowest rate and neurons operate in a high-conductance state. (A) Intrinsic axon path lengths of spiny neuron within gray matter in adult cat cerebral cortex (n = 22,001 paths from 19 neuron reconstructions). Data taken from Budd et al. (2010). (B) Extrinsic axonal fiber tract lengths in adult macaque cerebral cortex (n = 2309 pathways). Data taken from Kaiser and Hilgetag (2006).
Mentions: Figure 7 shows the results for both single intrinsic axon and extrinsic fiber tract data were quite similar. For the low-conductance state, virtually all axonal conduction delays were within an order of magnitude of neuronal integration delay almost regardless of mean conduction velocity (Figures 7A,B, square symbols). For the high-conductance state, except at the very lowest conduction velocities, the majority of the conduction delays were comparable to integration delays (Figures 7A,B, circle symbols). These results suggest that in both local and macroscopic cortical networks presynaptic axonal conduction delays may be mostly of a similar order of magnitude as postsynaptic neuronal integration delays (i.e., taxon ~ tint). To determine the shortest path length between a pair of neural elements, therefore, it is important to take into account both the number of neural elements in the path as well as its physical length estimated from measuring axonal and/or dendritic processes. It is unclear whether assigning a cost for each vertex as well as each edge would significantly affect the results for cortical networks previously analyzed (Kaiser and Hilgetag, 2006; Bassett et al., 2010).

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