Oscillatory coherence mediates flexible multi-frequency cortico-cortical interactions. Bottom-up and top-down influences along the cortical hierarchy rely, respectively, on faster or slower frequency bands. Besides the observation that directed inter-regional functional connectivity (dFC) does exploit multiple frequencies, it is not clear why this should be the case. Simple explanations for the frequency-specificity of dFC rest in the layered organization of the cortex. Our computational modeling suggests that inter-layer interactions are sufficient to cause deeper layers to oscillate at a slower frequency even when all interneurons are homogeneous and resonating at a fast frequency. Thus, we explore the dynamical regimes of a set of randomized canonic cortical columns and find that only 0.125% of the tested connectomes are “good” (including a phase with empiric-like frequency-specific dFC). Thus, the frequency-specific dFC emerges as a “free lunch” in the model when cortical layers are wired according to the empirical cortical column but not for arbitrary connectomes. We hypothesize that the wiring of the cortical column is constrained to achieve strong integration realized by synergies between different layers. We reveal that “good” connectomes are associated with maximal s-information, proportional to “high integration”; and minimal o-information, denoting a dominance of synergistic over redundant interactions. Indeed, dynamical regimes with peaks of s- and o-information co-localize with the regimes of frequency-specific dFC. The fact that frequency-specificity of dFC emerges could thus be not an aim per se but a trait of non-trivial dynamical regimes occurring only in canonic connectomes because they allow the emergence of synergistic-integrated interactions.

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