Inter-network interactions: impact of connections between oscillatory neuronal networks on oscillation frequency and pattern

Avella Gonzalez, O. J., Van Aerde, K. I., Mansvelder, H. D., Van Pelt, J., and Van Ooyen, A. (2014). PloS ONE 9(7): e100899. doi:10.1371/journal.pone.0100899. [Full text: PDF] [Supporting text: PDF] [Supporting figures: PDF]

Abstract

Oscillations in electrical activity are a characteristic feature of many brain networks and display a wide variety of temporal patterns. A network may express a single oscillation frequency, alternate between two or more distinct frequencies, or continually express multiple frequencies. In addition, oscillation amplitude may fluctuate over time. The origin of this complex repertoire of activity remains unclear.

Different cortical layers often produce distinct oscillation frequencies. To investigate whether interactions between different networks could contribute to the variety of oscillation patterns, we created two model networks, one generating on its own a relatively slow frequency (20 Hz; slow network) and one generating a fast frequency (32 Hz; fast network). Taking either the slow or the fast network as source network projecting connections to the other, or target, network, we systematically investigated how type and strength of inter-network connections affected target network activity.

For high inter-network connection strengths, we found that the slow network was more effective at completely imposing its rhythm on the fast network than the other way around. The strongest entrainment occurred when excitatory cells of the slow network projected to excitatory or inhibitory cells of the fast network. The fast network most strongly imposed its rhythm on the slow network when its excitatory cells projected to excitatory cells of the slow network. Interestingly, for lower inter-network connection strengths, multiple frequencies coexisted in the target network. Just as observed in rat prefrontal cortex, the target network could express multiple frequencies at the same time, alternate between two distinct oscillation frequencies, or express a single frequency with alternating episodes of high and low amplitude.

Together, our results suggest that input from other oscillating networks may markedly alter a network’s frequency spectrum and may partly be responsible for the rich repertoire of temporal oscillation patterns observed in the brain.