Limits...
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

Communication cost trade-off at Neuron scale of cortical organization. (A) Similar degree of trade-off between path length and wire length economy of intracortical spiny (left) and basket cell axon arbors (right) between corresponding path length optimized star trees and wire length optimized minimal spanning trees (MST), which were all more economical than random arbors (Reprinted from Budd et al., 2010). (B) Examples of spiny pyramidal cell dendritic arbors generated using different trade-off balancing factor (bf) values show that the most realistic looking arbor was obtained for bf = 0.7 (Reprinted from Cuntz et al., 2010). Note bf parameter is equivalent to β parameter in Figure 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3472565&req=5

Figure 4: Communication cost trade-off at Neuron scale of cortical organization. (A) Similar degree of trade-off between path length and wire length economy of intracortical spiny (left) and basket cell axon arbors (right) between corresponding path length optimized star trees and wire length optimized minimal spanning trees (MST), which were all more economical than random arbors (Reprinted from Budd et al., 2010). (B) Examples of spiny pyramidal cell dendritic arbors generated using different trade-off balancing factor (bf) values show that the most realistic looking arbor was obtained for bf = 0.7 (Reprinted from Cuntz et al., 2010). Note bf parameter is equivalent to β parameter in Figure 2.

Mentions: Neocortical axon arbors were not strictly minimized for either total axonal length or average path length; arbors used approximately 10–20% more axonal length than strictly necessary (Budd et al., 2010). Axon arbors used this excess wire to substantially improve average path length from axon origin to axonal boutons (Figure 4A). Strictly minimizing wire length only generated artificial arbors with a tortuous morphology and poorer average path lengths. In contrast, when artificial arbors were strictly minimized for path length only, they used a huge amount of axonal wire. Excess axonal wire in biological arbors was associated with branching close to the parent cell body and internodal axon segments lacking any boutons, which were often found between terminal branch clusters. Extrapolating from reported intracortical axon conduction velocity values (e.g., Luhmann et al., 1990), axonal path length distributions in this study suggested a narrow temporal dispersion of axonal latency within an arbor and a tight relationship between axonal latency and cortical distance (Budd et al., 2010). This prediction receives some support from the strong correlation between EPSP latency and cortical distance in the connections from layer 4 spiny neurons to layer 2/3 interneurons observed in vitro (see Figure 3C in Helmstaedter et al., 2008). Due to their greater branching complexity, the estimated axonal latencies of inhibitory basket cell were less dispersed than those of excitatory spiny cell axons. Thus, as expected for spatial networks generally (see “Spatial Networks”), neocortical axon arbors appear to trade-off communication costs using a small amount of extra axonal wire to ensure rapid and temporally precise signal propagation.


Communication and wiring in the cortical connectome.

Budd JM, Kisvárday ZF - Front Neuroanat (2012)

Communication cost trade-off at Neuron scale of cortical organization. (A) Similar degree of trade-off between path length and wire length economy of intracortical spiny (left) and basket cell axon arbors (right) between corresponding path length optimized star trees and wire length optimized minimal spanning trees (MST), which were all more economical than random arbors (Reprinted from Budd et al., 2010). (B) Examples of spiny pyramidal cell dendritic arbors generated using different trade-off balancing factor (bf) values show that the most realistic looking arbor was obtained for bf = 0.7 (Reprinted from Cuntz et al., 2010). Note bf parameter is equivalent to β parameter in Figure 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Communication cost trade-off at Neuron scale of cortical organization. (A) Similar degree of trade-off between path length and wire length economy of intracortical spiny (left) and basket cell axon arbors (right) between corresponding path length optimized star trees and wire length optimized minimal spanning trees (MST), which were all more economical than random arbors (Reprinted from Budd et al., 2010). (B) Examples of spiny pyramidal cell dendritic arbors generated using different trade-off balancing factor (bf) values show that the most realistic looking arbor was obtained for bf = 0.7 (Reprinted from Cuntz et al., 2010). Note bf parameter is equivalent to β parameter in Figure 2.
Mentions: Neocortical axon arbors were not strictly minimized for either total axonal length or average path length; arbors used approximately 10–20% more axonal length than strictly necessary (Budd et al., 2010). Axon arbors used this excess wire to substantially improve average path length from axon origin to axonal boutons (Figure 4A). Strictly minimizing wire length only generated artificial arbors with a tortuous morphology and poorer average path lengths. In contrast, when artificial arbors were strictly minimized for path length only, they used a huge amount of axonal wire. Excess axonal wire in biological arbors was associated with branching close to the parent cell body and internodal axon segments lacking any boutons, which were often found between terminal branch clusters. Extrapolating from reported intracortical axon conduction velocity values (e.g., Luhmann et al., 1990), axonal path length distributions in this study suggested a narrow temporal dispersion of axonal latency within an arbor and a tight relationship between axonal latency and cortical distance (Budd et al., 2010). This prediction receives some support from the strong correlation between EPSP latency and cortical distance in the connections from layer 4 spiny neurons to layer 2/3 interneurons observed in vitro (see Figure 3C in Helmstaedter et al., 2008). Due to their greater branching complexity, the estimated axonal latencies of inhibitory basket cell were less dispersed than those of excitatory spiny cell axons. Thus, as expected for spatial networks generally (see “Spatial Networks”), neocortical axon arbors appear to trade-off communication costs using a small amount of extra axonal wire to ensure rapid and temporally precise signal propagation.

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