Cortical Resonance Frequencies Emerge from Network Size and Connectivity

Neural oscillations occur within a wide frequency range with different brain regions exhibiting resonance-like characteristics at specific points in the spectrum. At the microscopic scale, single neurons possess intrinsic oscillatory properties, such that is not yet known whether cortical resonance is consequential to neural oscillations or an emergent property of the networks that interconnect them. Using a network model of loosely-coupled Wilson-Cowan oscillators to simulate a patch of cortical sheet, we demonstrate that the size of the activated network is inversely related to its resonance frequency. Further analysis of the parameter space indicated that the number of excitatory and inhibitory connections, as well as the average transmission delay between units, determined the resonance frequency. The model predicted that if an activated network within the visual cortex increased in size, the resonance frequency of the network would decrease. We tested this prediction experimentally using the steady-state visual evoked potential where we stimulated the visual cortex with different size stimuli at a range of driving frequencies. We demonstrate that the frequency corresponding to peak steady-state response inversely correlated with the size of the network. We conclude that although individual neurons possess resonance properties, oscillatory activity at the macroscopic level is strongly influenced by network interactions, and that the steady-state response can be used to investigate functional networks.Author Summary: When entrained using repetitive stimulation, sensory cortices appear to respond maximally, or resonate, at different driving frequencies: 10Hz in visual cortex; 20Hz and 40Hz in somatosensory and auditory cortices, respectively. The resonance frequencies are inversely correlated to the cortical volume of the respective regions, but it is unclear what drives this relationship. Here we used both computational and empirical data to demonstrate that resonance frequencies are emergent properties of the connectivity parameters of the underlying networks. The experimental paradigm stimulated large and small areas of visual cortex with different size objects made of flickering dots, and varied the driving frequency. Larger cortical areas exhibited maximum response at lower frequency than smaller areas, suggesting the inverse relationship between cortical size and resonance frequency holds, even within the same sensory modality. Computationally, we simulated cortical patches of different sizes and varied their connectivity parameters. We demonstrate that the size of the activated network is inversely related to its resonance frequency and that this change is due to the increased transmission delay and greater node degree within the larger network. The results are important for understanding the functional significance of oscillatory processes, and as a tool for probing changes in functional connectivity.