Brain rhythms define distinct interaction networks with differential dependence on anatomy

• Published in: Neuron (Cambridge, Mass.) Mass.), 2021-12, Vol.109 (23), p.3862-3878.e5
• Main Authors: Vezoli, Julien, Vinck, Martin, Bosman, Conrado Arturo, Bastos, André Moraes, Lewis, Christopher Murphy, Kennedy, Henry, Fries, Pascal
• Format: Article
• Language: English
• Subjects: bottom-up; Brain - physiology; Cognition; coherence; feedback; feedforward; functional connectivity; Gamma Rhythm - physiology; Granger causality; hierarchical processing; large-scale cortical networks; Neurons; power correlation; top-down
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2021.09.052

Cognitive functions are subserved by rhythmic neuronal synchronization across widely distributed brain areas. In 105 area pairs, we investigated functional connectivity (FC) through coherence, power correlation, and Granger causality (GC) in the theta, beta, high-beta, and gamma rhythms. Between rhythms, spatial FC patterns were largely independent. Thus, the rhythms defined distinct interaction networks. Importantly, networks of coherence and GC were not explained by the spatial distributions of the strengths of the rhythms. Those networks, particularly the GC networks, contained clear modules, with typically one dominant rhythm per module. To understand how this distinctiveness and modularity arises on a common anatomical backbone, we correlated, across 91 area pairs, the metrics of functional interaction with those of anatomical projection strength. Anatomy was primarily related to coherence and GC, with the largest effect sizes for GC. The correlation differed markedly between rhythms, being less pronounced for the beta and strongest for the gamma rhythm. •Coherence, power correlation, and Granger causality among >200 sites across 15 areas•These interaction metrics peak at the theta, beta, high-beta, and gamma rhythms•The 4 rhythms define distinct interaction networks, largely independent of power•The networks differentially depend on anatomy, strongly for gamma, weakly for beta The brain is much more than the sum of its parts because those parts interact in complex networks. Vezoli et al. show that at least 4 distinct interaction networks coexist, mediated by the neuronal synchronization of 4 brain rhythms. These rhythm-defined networks are differentially dependent on the strengths of anatomical projections.