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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

Total communication delay between neurons separable into a presynaptic axonal conduction delay and a postsynaptic neuronal integration delay. (A) Schematic circuit diagram shows the time taken by an action potential generated in the presynaptic neuron (left neuron, blue) to propagate along the axon to a presynaptic terminal, where it causes the release of neurotransmitter into the synaptic cleft, defines the axonal conduction delay (taxon). The postsynaptic neuronal integration delay (tint) is the sum of the time taken for neurotransmitter molecules to induce a local postsynaptic response (synaptic delay, tsyn) and the latency for this response to propagate down the dendritic tree to the axon initial segment, where its integration produces an action potential in the postsynaptic neuron (right neuron, orange) (dendritic delay, tdend). (B) Total delay (ttotal) between the timing of a presynaptic spike occuring (top, blue line) and the generation of a postsynaptic spike (bottom, orange line) is determined by the sum of presynaptic and postsynaptic delay components.
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Figure 6: Total communication delay between neurons separable into a presynaptic axonal conduction delay and a postsynaptic neuronal integration delay. (A) Schematic circuit diagram shows the time taken by an action potential generated in the presynaptic neuron (left neuron, blue) to propagate along the axon to a presynaptic terminal, where it causes the release of neurotransmitter into the synaptic cleft, defines the axonal conduction delay (taxon). The postsynaptic neuronal integration delay (tint) is the sum of the time taken for neurotransmitter molecules to induce a local postsynaptic response (synaptic delay, tsyn) and the latency for this response to propagate down the dendritic tree to the axon initial segment, where its integration produces an action potential in the postsynaptic neuron (right neuron, orange) (dendritic delay, tdend). (B) Total delay (ttotal) between the timing of a presynaptic spike occuring (top, blue line) and the generation of a postsynaptic spike (bottom, orange line) is determined by the sum of presynaptic and postsynaptic delay components.

Mentions: What is the justification for inferring temporal cost (delay) from path length in spatial networks? The total signaling delay of a stimulus in a cortical network, ttotal, may be separated into two main components (Nowak and Bullier, 1997): a presynaptic component, axonal conduction delay, and a postsynaptic component, neuronal integration delay (see Figure 6). We now examine these distinct components and consider how they should be used in estimating temporal cost in cortical networks at different spatial scales.


Communication and wiring in the cortical connectome.

Budd JM, Kisvárday ZF - Front Neuroanat (2012)

Total communication delay between neurons separable into a presynaptic axonal conduction delay and a postsynaptic neuronal integration delay. (A) Schematic circuit diagram shows the time taken by an action potential generated in the presynaptic neuron (left neuron, blue) to propagate along the axon to a presynaptic terminal, where it causes the release of neurotransmitter into the synaptic cleft, defines the axonal conduction delay (taxon). The postsynaptic neuronal integration delay (tint) is the sum of the time taken for neurotransmitter molecules to induce a local postsynaptic response (synaptic delay, tsyn) and the latency for this response to propagate down the dendritic tree to the axon initial segment, where its integration produces an action potential in the postsynaptic neuron (right neuron, orange) (dendritic delay, tdend). (B) Total delay (ttotal) between the timing of a presynaptic spike occuring (top, blue line) and the generation of a postsynaptic spike (bottom, orange line) is determined by the sum of presynaptic and postsynaptic delay components.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Total communication delay between neurons separable into a presynaptic axonal conduction delay and a postsynaptic neuronal integration delay. (A) Schematic circuit diagram shows the time taken by an action potential generated in the presynaptic neuron (left neuron, blue) to propagate along the axon to a presynaptic terminal, where it causes the release of neurotransmitter into the synaptic cleft, defines the axonal conduction delay (taxon). The postsynaptic neuronal integration delay (tint) is the sum of the time taken for neurotransmitter molecules to induce a local postsynaptic response (synaptic delay, tsyn) and the latency for this response to propagate down the dendritic tree to the axon initial segment, where its integration produces an action potential in the postsynaptic neuron (right neuron, orange) (dendritic delay, tdend). (B) Total delay (ttotal) between the timing of a presynaptic spike occuring (top, blue line) and the generation of a postsynaptic spike (bottom, orange line) is determined by the sum of presynaptic and postsynaptic delay components.
Mentions: What is the justification for inferring temporal cost (delay) from path length in spatial networks? The total signaling delay of a stimulus in a cortical network, ttotal, may be separated into two main components (Nowak and Bullier, 1997): a presynaptic component, axonal conduction delay, and a postsynaptic component, neuronal integration delay (see Figure 6). We now examine these distinct components and consider how they should be used in estimating temporal cost in cortical networks at different spatial scales.

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