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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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Significance of uncolored vs. colored motifs.A: Non-significant motif from an uncolored analysis [16] becomes highly significant (B) if colors are used to attach functional tags to the nodes. Green: sensor neurons, red: interneurons, blue: motor neurons.
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pone-0017013-g001: Significance of uncolored vs. colored motifs.A: Non-significant motif from an uncolored analysis [16] becomes highly significant (B) if colors are used to attach functional tags to the nodes. Green: sensor neurons, red: interneurons, blue: motor neurons.

Mentions: Indeed, the identification of the feedforward and bifan motifs does not allow us to determine how these motifs are used, or how they contribute to the worm's behavior. A simple example can illustrate this point: in Fig. 1A, we show a three-node motif that was not found to be significantly overrepresented in previous analyses [16]–[18]. However, if we color each neuron according to three possible functional tags such as motorneuron (blue), sensor neuron (green), or interneuron (red), several colored motifs stand out with high significance (see below), among which the motif shown in Fig. 1B. The functional significance of this motif is immediately obvious: it relays sensory information via an interneuron towards a muscle. Indeed, previous studies have shown that the connections between neurons of the three types chosen here are heavily biased: neurons do not connect indiscriminately between types [18], [21]–[23]. Also, an analysis of colored motifs using GO annotations in the yeast protein-protein interaction network [24] suggests that differently colored motifs are differentially evolutionarily conserved, pointing to a diversity of functional roles for motifs with the same structure.


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

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

Significance of uncolored vs. colored motifs.A: Non-significant motif from an uncolored analysis [16] becomes highly significant (B) if colors are used to attach functional tags to the nodes. Green: sensor neurons, red: interneurons, blue: motor neurons.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0017013-g001: Significance of uncolored vs. colored motifs.A: Non-significant motif from an uncolored analysis [16] becomes highly significant (B) if colors are used to attach functional tags to the nodes. Green: sensor neurons, red: interneurons, blue: motor neurons.
Mentions: Indeed, the identification of the feedforward and bifan motifs does not allow us to determine how these motifs are used, or how they contribute to the worm's behavior. A simple example can illustrate this point: in Fig. 1A, we show a three-node motif that was not found to be significantly overrepresented in previous analyses [16]–[18]. However, if we color each neuron according to three possible functional tags such as motorneuron (blue), sensor neuron (green), or interneuron (red), several colored motifs stand out with high significance (see below), among which the motif shown in Fig. 1B. The functional significance of this motif is immediately obvious: it relays sensory information via an interneuron towards a muscle. Indeed, previous studies have shown that the connections between neurons of the three types chosen here are heavily biased: neurons do not connect indiscriminately between types [18], [21]–[23]. Also, an analysis of colored motifs using GO annotations in the yeast protein-protein interaction network [24] suggests that differently colored motifs are differentially evolutionarily conserved, pointing to a diversity of functional roles for motifs with the same structure.

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
Related in: MedlinePlus