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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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Differential representation of colored motifs.Comparison of the colored motif counts  obtained from the C. elegans neuron network and the average count from 1,000 color-randomized networks, . Points above the zero line represent the colored motifs with higher frequency in the worm's neuronal network compared to color-randomized networks (over-representation), while those below that line are suppressed. A: colored directed motifs of size 2, B: colored directed motifs with three nodes, C: colored directed motifs with 4 nodes. Logarithm is to the base 2.
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pone-0017013-g002: Differential representation of colored motifs.Comparison of the colored motif counts obtained from the C. elegans neuron network and the average count from 1,000 color-randomized networks, . Points above the zero line represent the colored motifs with higher frequency in the worm's neuronal network compared to color-randomized networks (over-representation), while those below that line are suppressed. A: colored directed motifs of size 2, B: colored directed motifs with three nodes, C: colored directed motifs with 4 nodes. Logarithm is to the base 2.

Mentions: In order to determine whether the abundance of a particular colored motif in C. elegans is biased, we produce random colored control networks by shuffling the color assignments in the C. elegans network while maintaining the relative abundance of each kind. The mean abundance of colored motifs of a particular type for 1,000 independent randomizations then provides the unbiased expectation for that motif, which we compare with the actual count obtained for the colored worm brain. In Fig. 2, we plot the logarithm (base 2) of the ratio for each colored motif as a function of the random count , to determine the extent to which the worm motifs are over- or underrepresented. Most of the motif counts in C. elegans are significantly different from the random control: all of the 2-node colored motif counts are significant, and all but one of the three-node motifs (one-sample two-tailed t-test, ). Of the 4-node motifs, only 156 of the observed 8,310 motifs are not significantly different from the control count at the 5% level.


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

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

Differential representation of colored motifs.Comparison of the colored motif counts  obtained from the C. elegans neuron network and the average count from 1,000 color-randomized networks, . Points above the zero line represent the colored motifs with higher frequency in the worm's neuronal network compared to color-randomized networks (over-representation), while those below that line are suppressed. A: colored directed motifs of size 2, B: colored directed motifs with three nodes, C: colored directed motifs with 4 nodes. Logarithm is to the base 2.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0017013-g002: Differential representation of colored motifs.Comparison of the colored motif counts obtained from the C. elegans neuron network and the average count from 1,000 color-randomized networks, . Points above the zero line represent the colored motifs with higher frequency in the worm's neuronal network compared to color-randomized networks (over-representation), while those below that line are suppressed. A: colored directed motifs of size 2, B: colored directed motifs with three nodes, C: colored directed motifs with 4 nodes. Logarithm is to the base 2.
Mentions: In order to determine whether the abundance of a particular colored motif in C. elegans is biased, we produce random colored control networks by shuffling the color assignments in the C. elegans network while maintaining the relative abundance of each kind. The mean abundance of colored motifs of a particular type for 1,000 independent randomizations then provides the unbiased expectation for that motif, which we compare with the actual count obtained for the colored worm brain. In Fig. 2, we plot the logarithm (base 2) of the ratio for each colored motif as a function of the random count , to determine the extent to which the worm motifs are over- or underrepresented. Most of the motif counts in C. elegans are significantly different from the random control: all of the 2-node colored motif counts are significant, and all but one of the three-node motifs (one-sample two-tailed t-test, ). Of the 4-node motifs, only 156 of the observed 8,310 motifs are not significantly different from the control count at the 5% level.

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