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Colored motifs reveal computational building blocks in the C. elegans brain.

Qian J, Hintze A, Adami C - PLoS ONE (2011)

Bottom Line: We discover that particular colorations of motifs are significantly more abundant in the worm brain than expected by chance, and have particular computational functions that emphasize the feed-forward structure of information processing in the network, while evading feedback loops.Some of the most common motifs identified in the search for significant colored motifs play a crucial role in the system of neurons controlling the worm's locomotion.The method is general and should allow a decomposition of any complex networks into its functional (rather than topological) motifs as long as both wiring and functional information is available.

View Article: PubMed Central - PubMed

Affiliation: Keck Graduate Institute, Claremont, California, United States of America.

ABSTRACT

Background: Complex networks can often be decomposed into less complex sub-networks whose structures can give hints about the functional organization of the network as a whole. However, these structural motifs can only tell one part of the functional story because in this analysis each node and edge is treated on an equal footing. In real networks, two motifs that are topologically identical but whose nodes perform very different functions will play very different roles in the network.

Methodology/principal findings: Here, we combine structural information derived from the topology of the neuronal network of the nematode C. elegans with information about the biological function of these nodes, thus coloring nodes by function. We discover that particular colorations of motifs are significantly more abundant in the worm brain than expected by chance, and have particular computational functions that emphasize the feed-forward structure of information processing in the network, while evading feedback loops. Interneurons are strongly over-represented among the common motifs, supporting the notion that these motifs process and transduce the information from the sensor neurons towards the muscles. Some of the most common motifs identified in the search for significant colored motifs play a crucial role in the system of neurons controlling the worm's locomotion.

Conclusions/significance: The analysis of complex networks in terms of colored motifs combines two independent data sets to generate insight about these networks that cannot be obtained with either data set alone. The method is general and should allow a decomposition of any complex networks into its functional (rather than topological) motifs as long as both wiring and functional information is available.

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Colored motif abundances.Histogram of abundances of directed structural motifs of two neurons with particular coloration in C. elegans (black) compared to the average abundance in 1,000 color randomizations of the same network (grey). Green: sensory neuron, red: interneuron, blue: motor neuron. A: directed pairs (the direction of information flow is left-to-right). B: undirected pairs.
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pone-0017013-g003: Colored motif abundances.Histogram of abundances of directed structural motifs of two neurons with particular coloration in C. elegans (black) compared to the average abundance in 1,000 color randomizations of the same network (grey). Green: sensory neuron, red: interneuron, blue: motor neuron. A: directed pairs (the direction of information flow is left-to-right). B: undirected pairs.

Mentions: In previous work that analyzed structural motifs only [16]–[18], the undirectional two-node motif was found to be unremarkable, while the bi-directional motif was deemed over-represented [16], [18] with respect to an ensemble of edge-randomized networks. We can look at both of those motifs in terms of the exceptionality of their colorations. In Fig. 3 we show the measured counts of each of the color realizations of the directed (Fig. 3A) and undirected (Fig. 3B) motifs.


Colored motifs reveal computational building blocks in the C. elegans brain.

Qian J, Hintze A, Adami C - PLoS ONE (2011)

Colored motif abundances.Histogram of abundances of directed structural motifs of two neurons with particular coloration in C. elegans (black) compared to the average abundance in 1,000 color randomizations of the same network (grey). Green: sensory neuron, red: interneuron, blue: motor neuron. A: directed pairs (the direction of information flow is left-to-right). B: undirected pairs.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3049772&req=5

pone-0017013-g003: Colored motif abundances.Histogram of abundances of directed structural motifs of two neurons with particular coloration in C. elegans (black) compared to the average abundance in 1,000 color randomizations of the same network (grey). Green: sensory neuron, red: interneuron, blue: motor neuron. A: directed pairs (the direction of information flow is left-to-right). B: undirected pairs.
Mentions: In previous work that analyzed structural motifs only [16]–[18], the undirectional two-node motif was found to be unremarkable, while the bi-directional motif was deemed over-represented [16], [18] with respect to an ensemble of edge-randomized networks. We can look at both of those motifs in terms of the exceptionality of their colorations. In Fig. 3 we show the measured counts of each of the color realizations of the directed (Fig. 3A) and undirected (Fig. 3B) motifs.

Bottom Line: We discover that particular colorations of motifs are significantly more abundant in the worm brain than expected by chance, and have particular computational functions that emphasize the feed-forward structure of information processing in the network, while evading feedback loops.Some of the most common motifs identified in the search for significant colored motifs play a crucial role in the system of neurons controlling the worm's locomotion.The method is general and should allow a decomposition of any complex networks into its functional (rather than topological) motifs as long as both wiring and functional information is available.

View Article: PubMed Central - PubMed

Affiliation: Keck Graduate Institute, Claremont, California, United States of America.

ABSTRACT

Background: Complex networks can often be decomposed into less complex sub-networks whose structures can give hints about the functional organization of the network as a whole. However, these structural motifs can only tell one part of the functional story because in this analysis each node and edge is treated on an equal footing. In real networks, two motifs that are topologically identical but whose nodes perform very different functions will play very different roles in the network.

Methodology/principal findings: Here, we combine structural information derived from the topology of the neuronal network of the nematode C. elegans with information about the biological function of these nodes, thus coloring nodes by function. We discover that particular colorations of motifs are significantly more abundant in the worm brain than expected by chance, and have particular computational functions that emphasize the feed-forward structure of information processing in the network, while evading feedback loops. Interneurons are strongly over-represented among the common motifs, supporting the notion that these motifs process and transduce the information from the sensor neurons towards the muscles. Some of the most common motifs identified in the search for significant colored motifs play a crucial role in the system of neurons controlling the worm's locomotion.

Conclusions/significance: The analysis of complex networks in terms of colored motifs combines two independent data sets to generate insight about these networks that cannot be obtained with either data set alone. The method is general and should allow a decomposition of any complex networks into its functional (rather than topological) motifs as long as both wiring and functional information is available.

Show MeSH