Stable long-range interhemispheric coordination is supported by direct anatomical projections

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 20; pp. 6473 - 6478
• Main Authors: Shen, Kelly, Mišić, Bratislav, Cipollini, Ben N., Bezgin, Gleb, Buschkuehl, Martin, Hutchison, R. Matthew, Jaeggi, Susanne M., Kross, Ethan, Peltier, Scott J., Everling, Stefan, Jonides, John, McIntosh, Anthony R., Berman, Marc G.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 19.05.2015; National Acad Sciences
• Subjects: Anatomy & physiology; Animals; Biological Sciences; Brain Mapping; Communication; Comparative analysis; Corpus Callosum - anatomy & histology; Corpus Callosum - physiology; Female; Functional Laterality - physiology; Humans; Hypothesis testing; Macaca; Magnetic Resonance Imaging; Male; Nerve Fibers, Myelinated - physiology; Species Specificity; Synaptic Transmission - physiology; structural connectivity; dynamics; functional connectivity; homotopy
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1503436112

Significance We show that the functional coordination between the two hemispheres of the brain is maintained by strong and stable interactions of a specific subset of connections between homotopic regions. Our data suggest that the stability of those functional interactions is mediated in part by the direct anatomical projections of large, highly myelinated fibers that traverse the corpus callosum. These functional properties were evident in both humans and macaques, suggesting a preserved framework for interhemispheric communication despite an increase in functional lateralization in humans. These results contribute to our fundamental understanding of how dynamic functional interactions between the two hemispheres of the mammalian brain are supported by its underlying anatomical architecture. The functional interaction between the brain’s two hemispheres includes a unique set of connections between corresponding regions in opposite hemispheres (i.e., homotopic regions) that are consistently reported to be exceptionally strong compared with other interhemispheric (i.e., heterotopic) connections. The strength of homotopic functional connectivity (FC) is thought to be mediated by the regions’ shared functional roles and their structural connectivity. Recently, homotopic FC was reported to be stable over time despite the presence of dynamic FC across both intrahemispheric and heterotopic connections. Here we build on this work by considering whether homotopic FC is also stable across conditions. We additionally test the hypothesis that strong and stable homotopic FC is supported by the underlying structural connectivity. Consistent with previous findings, interhemispheric FC between homotopic regions were significantly stronger in both humans and macaques. Across conditions, homotopic FC was most resistant to change and therefore was more stable than heterotopic or intrahemispheric connections. Across time, homotopic FC had significantly greater temporal stability than other types of connections. Temporal stability of homotopic FC was facilitated by direct anatomical projections. Importantly, temporal stability varied with the change in conductive properties of callosal axons along the anterior–posterior axis. Taken together, these findings suggest a notable role for the corpus callosum in maintaining stable functional communication between hemispheres.