TY - JOUR
T1 - Specificity and robustness of long-distance connections in weighted, interareal connectomes
AU - Betzel, Richard F.
AU - Bassett, Danielle S.
N1 - Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.
PY - 2018/5/22
Y1 - 2018/5/22
N2 - Brain areas’ functional repertoires are shaped by their incoming and outgoing structural connections. In empirically measured networks, most connections are short, reflecting spatial and energetic constraints. Nonetheless, a small number of connections span long distances, consistent with the notion that the functionality of these connections must outweigh their cost. While the precise function of long-distance connections is unknown, the leading hypothesis is that they act to reduce the topological distance between brain areas and increase the efficiency of interareal communication. However, this hypothesis implies a nonspecificity of long-distance connections that we contend is unlikely. Instead, we propose that long-distance connections serve to diversify brain areas’ inputs and outputs, thereby promoting complex dynamics. Through analysis of five weighted interareal network datasets, we show that long-distance connections play only minor roles in reducing average interareal topological distance. In contrast, areas’ long-distance and short-range neighbors exhibit marked differences in their connectivity profiles, suggesting that long-distance connections enhance dissimilarity between areal inputs and outputs. Next, we show that—in isolation—areas’ long-distance connectivity profiles exhibit nonrandom levels of similarity, suggesting that the communication pathways formed by long connections exhibit redundancies that may serve to promote robustness. Finally, we use a linearization of Wilson–Cowan dynamics to simulate the covariance structure of neural activity and show that in the absence of long-distance connections a common measure of functional diversity decreases. Collectively, our findings suggest that long-distance connections are necessary for supporting diverse and complex brain dynamics.
AB - Brain areas’ functional repertoires are shaped by their incoming and outgoing structural connections. In empirically measured networks, most connections are short, reflecting spatial and energetic constraints. Nonetheless, a small number of connections span long distances, consistent with the notion that the functionality of these connections must outweigh their cost. While the precise function of long-distance connections is unknown, the leading hypothesis is that they act to reduce the topological distance between brain areas and increase the efficiency of interareal communication. However, this hypothesis implies a nonspecificity of long-distance connections that we contend is unlikely. Instead, we propose that long-distance connections serve to diversify brain areas’ inputs and outputs, thereby promoting complex dynamics. Through analysis of five weighted interareal network datasets, we show that long-distance connections play only minor roles in reducing average interareal topological distance. In contrast, areas’ long-distance and short-range neighbors exhibit marked differences in their connectivity profiles, suggesting that long-distance connections enhance dissimilarity between areal inputs and outputs. Next, we show that—in isolation—areas’ long-distance connectivity profiles exhibit nonrandom levels of similarity, suggesting that the communication pathways formed by long connections exhibit redundancies that may serve to promote robustness. Finally, we use a linearization of Wilson–Cowan dynamics to simulate the covariance structure of neural activity and show that in the absence of long-distance connections a common measure of functional diversity decreases. Collectively, our findings suggest that long-distance connections are necessary for supporting diverse and complex brain dynamics.
KW - Communication
KW - Complex networks
KW - Connectome
KW - Wiring cost
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U2 - 10.1073/pnas.1720186115
DO - 10.1073/pnas.1720186115
M3 - Article
C2 - 29739890
AN - SCOPUS:85047310886
SN - 0027-8424
VL - 115
SP - E4880-E4889
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 21
ER -