The role of long-range connections on the specificity of the macaque interareal cortical network

N.T. Markov, M. Ercsey-Ravasz, C. Lamy, A.R. Ribeiro Gomes, L. Magrou, P. Misery, P. Giroud, P. Barone, C. Dehay, Z. Toroczkai, K. Knoblauch, D.C. Van Essen, H. Kennedy
PNAS 2013 110 (13) 5187-5192; published ahead of print March 11, 2013, doi:10.1073/pnas.1218972110
Publication Date: 
March, 2013

We investigated the influence of interareal distance on connectivity patterns in a database obtained from the injection of retrograde tracers in 29 areas distributed over six regions (occipital, temporal, parietal, frontal, prefrontal, and limbic). One-third of the 1,615 pathways projecting to the 29 target areas were reported only recently and deemed new-found projections (NFPs). NFPs are predominantly long-range, low-weight connections. A minimum dominating set analysis (a graph theoretic measure) shows that NFPs play a major role in globalizing input to small groups of areas. Randomization tests show that (i) NFPs make important contributions to the specificity of the connectivity profile of individual cortical areas, and (ii) NFPs share key properties with known connections at the same distance. We developed a similarity index, which shows that intraregion similarity is high, whereas the interregion similarity declines with distance. For area pairs, there is a steep decline with distance in the similarity and probability of being connected. Nevertheless, the present findings reveal an unexpected binary specificity despite the high density (66%) of the cortical graph. This specificity is made possible because connections are largely concentrated over short distances. These findings emphasize the importance of long-distance connections in the connectivity profile of an area. We demonstrate that long-distance connections are particularly prevalent for prefrontal areas, where they may play a prominent role in large-scale communication and information integration.